· Google Scholar: Author Only Title Only Author and Title Shi T, Bibby TS, Jiang L, Irwin AJ,...

1

Short title Synthetic biology of photosynthesis 1

2

Author for contact details 3

Dario Leister 4

Ludwig-Maximilians-University Munich 5

Faculty of Biology 6

Groszlighaderner Str 2 7

D-82152 Planegg-Martinsried 8

Germany 9

Phone +49-892180 74550 10

Fax +49-892180 74599 11

Email leisterlmude 12

13

Genetic engineering synthetic biology and the light reactions of photosynthesis1 14

15

Dario Leister 16

17

Plant Molecular Biology Faculty of Biology Ludwig-Maximilians-University Munich D-18

82152 Planegg-Martinsried Germany 19

20

21

One-sentence summary Applications of synthetic biology to photosynthesis currently range 22

from exchanging photosynthetic proteins to the utilization of photosynthesis as a source of 23

electrons for entirely unrelated reactions 24

25

Plant Physiology Preview Published on July 10 2018 as DOI101104pp1800360

Copyright 2018 by the American Society of Plant Biologists

wwwplantphysiolorgon April 12 2020 - Published by Downloaded from Copyright copy 2018 American Society of Plant Biologists All rights reserved

2

1 This work was funded by the Deutsche Forschungsgemeinschaft (DFG TRR 175 and GRK 26

2062) 27

28

Address correspondence to leisterlmude 29

ORCID IDs 0000-0003-1897-8421 (DL) 30

31

Oxygenic photosynthesis is imperfect and the evolutionarily conditioned patchwork nature of 32

the light reactions in plants provides ample scope for their improvement (Leister 2012 33

Blankenship and Chen 2013) In fact only around 40 of the incident solar energy is used 34

for photosynthesis Two obvious ways of reducing energy loss are to expand the spectral 35

band used for photosynthesis and to shift saturation of the process to higher light intensities 36

Indeed even minor enhancements to the efficiency or stress resistance of the light reactions 37

of photosynthesis should have a positive impact on biomass production and yield (Leister 38

2012 Blankenship and Chen 2013 Long et al 2015) 39

However modifications to the essential structure of the light reactions of plant 40

photosynthesis are currently limited by two main factors One is the high degree of 41

conservation of their structural components which limits the efficiency gains attainable by 42

conventional breeding approaches (Dann and Leister 2017) The second is that the 43

organization of these structural components into multiprotein complexes requires the 44

simultaneous tailoring of several proteins some of them encoded by different genetic systems 45

in different subcellular compartments (nucleus and chloroplasts) in land plants Therefore 46

successful modification of the light reactions of plant photosynthesis has been limited to a 47

few cases Similarly modification of the activity of auxiliary proteins involved in the 48

regulation of the light reactions to enhance plant growth and yield has only recently resulted 49


3

in successful outcomes and is limited to a small subset of regulatory proteins (Pribil et al 50

2010 Kromdijk et al 2016 Glowacka et al 2018) 51

In addition to enhancing the light reactions for improved biomass production and 52

yield concepts have been developed for the direct coupling of photosynthesis to other 53

important pathways that are indirectly connected to photosynthesis in natural systems for 54

instance because they reside in different subcellular compartments (Lassen et al 2014a) 55

Direct coupling would be expected to boost the production of rare compounds in cells and 56

contribute to the biotechnological production of high-value compounds in vivo 57

In vitro it is possible to functionally link components of photosynthesis with entirely 58

unrelated biotic or abiotic catalysts or with abiotic electrode materials In fact Photosystem I 59

(PSI) is naturally adapted for highly efficient light harvesting and charge separation (Kargul 60

et al 2012 Nguyen and Bruce 2014 Martin and Frymier 2017) and has been described as 61

the most efficient natural nano-photochemical machine (Nelson 2009) Upon light excitation 62

PSI produces the most powerful naturally occurring reducing agent ndash P700 ndash which 63

together with an exceptionally long-lived charge-separated state provides sufficient driving 64

force to reduce protons to H2 at neutral pH PSI operates with a quantum yield close to 10 65

and currently no synthetic system has approached its remarkable efficiency Moreover PSI 66

preparations are generally robust especially those obtained from extremophilic microalgae 67

(Kubota et al 2010 Haniewicz et al 2018) The superior qualities of PSI have stimulated 68

strategies designed to generate in vitro hybrids of PSI and various types of redox-active 69

catalysts or other materials 70

In sum the light reactions of photosynthesis are a prime target for genetic engineering 71

and synthetic biology approaches for three major reasons (1) Enhancement of the process in 72

vivo to increase the efficiency of light use promises to increase biomass and crop yields (2) 73

Coupling of the light reactions of photosynthesis to previously unconnected pathways will 74


4

enable us to utilize the reducing power of the light reactions directly to produce large 75

amounts of high-value compounds in vivo (3) The high efficiency and robustness of PSI 76

should allow it to be used in hybrids with biotic or abiotic components to generate hydrogen 77

simple carbon-based solar fuels or electricity in vitro In this review the background to and 78

recent developments in these three strategies are discussed 79

80

Natural building blocks of photosynthesis 81

During photosynthesis carbon dioxide (CO2) is converted into organic compounds 82

principally sugars using sunlight as energy In plants algae and cyanobacteria 83

photosynthesis uses water as the electron donor for chemical reduction of CO2 and releases 84

oxygen Algae and plants derive from a lineage that arose from an endosymbiotic relationship 85

between a protist and a cyanobacterium Chloroplasts the photosynthetic organelles in 86

modern plants are in fact the descendants of this ancient symbiotic cyanobacterium and 87

possess an internal membrane system that resembles the thylakoid membranes of modern-day 88

cyanobacteria Indeed during the evolutionary transition from cyanobacteria to chloroplasts 89

the overall organization and mode of action of the photosynthetic machinery was retained 90

(Box 1) However significant changes have occurred in the subunit composition of 91

photosystems (Fig 1) their posttranslational modification (Pesaresi et al 2011) the 92

harvesting of light energy pigment composition and regulation of photosynthesis (Box 93

2)(Mullineaux and Emlyn-Jones 2005 Rochaix 2007 Holt et al 2004 de Bianchi et al 94

2010) 95

Its evolutionary history makes photosynthesis well-suited for synthetic biology 96

strategies The evolutionary diversification of the photosynthetic machinery has provided a 97

set of building blocks ranging from single proteins such as the soluble electron transporters 98

(plastocyanin cytochrome c6 flavodoxin and ferredoxin) to multiprotein complexes like 99


5

photosystems and antenna complexes (phycobiliosomes and light-harvesting complexes 100

(LHCs)) In principle the building blocks should be interchangeable between cyanobacteria 101

algae and plants Instances of the swapping of homologous photosynthetic proteins between 102

species by means of genetic engineering are discussed in the next section to highlight the 103

complications associated with apparently straightforward approaches The focus then shifts to 104

genuinely synthetic approaches in which specific photosynthetic building blocks have been 105

introduced into photosynthetic species that lack them In the subsequent two sections the 106

combination of non-photosynthetic (Bio-bio hybrids using photosynthesis as an electron 107

source for unrelated biological processes) and non-biological building blocks (Bio-nano 108

hybrids using photosynthesis as an electron source for non-biological processes) with 109

components of the photosynthetic machinery are described An overview of these approaches 110

is provided in Figure 2 111

112

Exchange of conserved photosynthetic modules 113

Theoretically it should be relatively easy to exchange individual conserved photosynthetic 114

proteins between different species even in such distantly related organisms as cyanobacteria 115

and plants However in practice these simple genetic engineering exercises can be 116

problematic (Table 1) Several individual proteins from cyanobacterial PSII (D1 CP43 and 117

PsbH) and PSI (PsaA) have indeed been genetically replaced by their plant counterparts with 118

varying success Synechocystis strains expressing the D1 protein from Poa annua or PsbH 119

from maize (Zea mays) could still perform photosynthesis ndash albeit with less efficiency than 120

the WT strain (Nixon et al 1991 Chiaramonte et al 1999) ndash but replacement of 121

Synechocystis CP43 or CP47 by their homologs from spinach (Spinacia oleracea) was 122

incompatible with photoautotrophy (Carpenter et al 1993 Vermaas et al 1996) Similarly 123


6

in Synechocystis strains equipped with Arabidopsis thaliana PsaA PSI function was severely 124

disrupted (Viola et al 2014) 125

Such complications resulting from the replacement of core subunits of photosystems 126

despite their high similarity (78ndash86 identity between the cyanobacterial and plant proteins 127

Table 1) reflect the so-called ldquofrozen metabolic staterdquo of the photosynthetic multiprotein 128

complexes This term was coined by Gimpel et al (2016) but was originally introduced as 129

ldquofrozen metabolic accidentrdquo by Shi et al (2005) The ldquofrozen metabolic accidentrdquo concept 130

refers to the observation that selection has not significantly altered biophysically and 131

physiologically inefficient photosynthetic proteins (including the D1 protein of PSII or 132

RuBisCO of the Calvin-Benson cycle) over billions of years of evolution In fact 133

bioinformatic analysis of photosynthetic cyanobacterial genes suggests that the evolution rate 134

of proteins at the core of the photosynthetic apparatus is highly constrained by protein-135

protein protein-lipid and protein-cofactor interactions (Shi et al 2005) This provides an 136

internal selection pressure conserving the sequence of proteins in photosynthetic 137

multiprotein complexes and ndash in case of prokaryotes ndash also the genomic organization of their 138

genes (Shi et al 2005) The term ldquofrozen metabolic accidentrdquo was generalized to ldquofrozen 139

metabolic staterdquo by Gimpel et al (2016) and implies that in each photosynthetic species 140

slightly distinct modules of the cores of photosynthetic multiprotein complexes have evolved 141

that are optimized with respect to their intrinsic interactions and that rarely tolerate the 142

alteration of single proteins by exchange or mutation In consequence the simultaneous 143

exchange of entire sets of core proteins (or ldquomodulesrdquo) with all their intrinsic interactions 144

should be more feasible than substituting individual proteins that may disrupt the ldquofrozen 145

metabolic staterdquo Such an experiment has been performed in the green alga Chlamydomonas 146

reinhardtii where the six PSII core proteins D1 CP47 CP43 D2 Cyt b559- and were 147

swapped for their homologs from two other green algal species (Gimpel et al 2016) 148


7

Photoautotrophy was not affected by the exchange of this synthetic biology module although 149

the fully altered strains performed suboptimally compared to strains in which only 1ndash5 genes 150

were exchanged However in control experiments where the synthetic C reinhardtii six-gene 151

module was re-introduced to the C reinhardtii deletion strain that lacked all six genes only 152

about 86 of wild-type PSII functionality was rescued Tentative explanations for this 153

decreased efficiency include (i) off-target effects of the PSII gene deletions on the operon 154

components and tRNA genes associated with these PSII loci (ii) misregulation of the 155

transferred PSII genes because their expression cassettes lacked unidentified cis-acting DNA 156

elements and (iii) perturbation of polycistron-dependent post-transcriptional regulation of the 157

transformed genes since they were no longer part of an operon (Gimpel et al 2016) 158

Taken together the outcomes of these replacement experiments indicate that 159

exchanging conserved photosynthetic proteins from multiprotein complexes can be 160

problematic given the highly integrated nature of the photosynthetic machinery Therefore 161

approaches designed to enhance photosynthesis such as introducing the high-light-resistant 162

D1 protein from a green alga that lives under extreme conditions (Treves et al 2016) into 163

crop plants do not appear promising Instead entire (sub)complexes with their internal 164

network of evolutionarily optimized interactions should be transferable between species 165

166

Exchange of non-conserved photosynthetic modules 167

Inspection of the repertoire of subunits of the photosynthetic machinery in the three model 168

species Synechocystis PCC6803 C reinhardtii and A thaliana which represent different 169

stages in the evolution of oxygen-generating photosynthesis shows that the most dramatic 170

changes in the photosynthetic proteome occurred during the transition from the 171

cyanobacterial endosymbiont (for which Synechocystis serves as a proxy) to the chloroplast 172

of unicellular algae (with C reinhardtii as proxy) (Fig 3 Supplemental Table 1) In 173


8

particular phycobilisomes flavodoxin and several photosystem subunits were lost while 174

LHCs some novel photosystem subunits and several proteins involved in alternative electron 175

pathways or photoprotection evolved During the transition from algal chloroplasts to those 176

of flowering plants relatively few proteins were lost (eg flavodiiron proteins and the 177

canonical cytochrome c6) or acquired (Lhcb6CP24) (Fig 3 Supplemental Table 1) The 178

NAD(P)H dehydrogenase (NDH) complex involved in antimycin A-insensitive cyclic 179

electron flow (see Box 1) is a special case since the chloroplast NDH from flowering plants 180

traces back to the cyanobacterial complex but the complex was lost during evolution in C 181

reinhardtii (Fig 3 Supplemental Table 1) 182

Several attempts have been made to introduce photosynthetic proteins into species 183

that lack the corresponding homolog (Table 2) These heterologous expression approaches 184

have been successful for the soluble electron transporters flavodoxin cytochrome c6 and 185

flavodiiron proteins Indeed cyanobacterial flavodoxin can at least partially replace plant 186

ferredoxin and confer enhanced stress tolerance when expressed in addition to ferredoxin 187

(Tognetti et al 2006 Tognetti et al 2007 Blanco et al 2011) Similarly red algal 188

cytochrome c6 enhances growth and photosynthesis of A thaliana plants (Chida et al 2007) 189

Since A thaliana lacks a functional cytochrome c6 that can transfer electrons from the Cyt b6f 190

complex to PSI (Molina-Heredia et al 2003 Weigel et al 2003) it is plausible that the 191

more oxidized plastoquinone pool in the transgenic plants is a direct consequence of 192

additional PSI reduction mediated by the algal protein (Chida et al 2007) Interestingly it 193

seems to make no difference if an endogenous soluble electron transport protein (see Box 3) 194

or its heterologous equivalent from a distant species is overexpressed For instance 195

overexpression of the endogenous soluble proteins plastocyanin and ferredoxin can also 196

enhance growth in plants (Pesaresi et al 2009 Lin et al 2013 Chang et al 2017 Zhou et 197

al 2018) Interestingly and rather unexpectedly this concept can also work for certain 198


9

proteins that are part of multiprotein complexes (Simkin et al 2017 see Box 3) This 199

indicates that the quantity of such proteins is relevant for growth enhancement and not its 200

evolutionary origin 201

More recently the two Physcomitrella patens flavodiiron protein (FLV) genes FlvA 202

and FlvB were introduced into A thaliana which like other angiosperms has lost FLVs 203

during evolution (Yamamoto et al 2016) FLVs are the main mediators of pseudo-cyclic 204

electron flow in photosynthetic organisms but heterologous expression of FLVs in A 205

thaliana had no effect on steady-state photosynthesis and growth of the transgenic plants 206

(Yamamoto et al 2016) However the Arabidopsis FLV lines displayed higher 207

photosynthetic yields just after the onset of actinic light following a long dark adaptation 208

suggesting that the FLVs mediated a large electron sink during the induction of 209

photosynthesis In fluctuating light experiments the Arabidopsis FLV lines had much less 210

PSI acceptor side limitation implying that the large FLV-mediated electron sink makes 211

photosynthesis more resistant to the fluctuating light Consequently this protective effect of 212

FLVs is more pronounced in Arabidopsis lines that are more sensitive to fluctuating light like 213

the pgr5 mutant defective in antimycin A-sensitive cyclic electron flow (see Box 1 Leister 214

and Shikanai 2013 Yamamoto et al 2016) Similarly expression of FLVs in a rice (Oryza 215

sativa) line with markedly reduced cyclic electron flow restored CO2 assimilation and growth 216

rate to wild-type levels (Wada et al 2018) Like FLVs LHcxLHCSR proteins play a role in 217

photoprotection in green algae and mosses but have been lost in angiosperms during 218

evolution Heterologous expression of P patens LHCSR1 in Nicotiana benthamiana and 219

Nicotiana tabacum yielded an active protein that has properties similar if not identical to 220

those of moss LHCSR1 (Pinnola et al 2015) 221


10

Efforts to create LHCII complexes like those in plants by heterologously expressing 222

the membrane-spanning light-harvesting chlorophyll ab-binding protein Lhcb from Pisum 223

sp (pea) in Synechocystis were unsuccessful 224

Although the pea Lhcb protein was synthesized in Synechocystis and integrated into 225

the membrane it did not accumulate to steady-state levels detectable by immunoblot analysis 226

(He et al 1999) Possible explanations are that Lhcb is rapidly degraded either because its 227

ldquounfamiliarrdquo structure makes it a good substrate for the cyanobacterial proteolytic system or 228

it cannot foldassemble properly due to the lack of plant-specific pigments or assembly 229

factors Interestingly chlorophyll b production (see Box 2) after introduction of plant 230

chlorophyll a oxygenase (CAO) is boosted when Lhcb is expressed even though LHCII does 231

not accumulate in detectable amounts (Xu et al 2001) 232

Even soluble multiprotein complexes can be heterologously expressed as has been 233

impressively demonstrated from the carbon-fixation end of photosynthesis For example by 234

coexpression of five auxiliary factors a functional plant RuBisCo complex was successfully 235

assembled in Escherichia coli (Aigner et al 2017) This result is in line with the ldquofrozen 236

metabolic staterdquo concept showing that photosynthetic proteins embedded in a network of 237

interactions with other proteins and auxiliary factors can be introduced into distantly related 238

species but only with their own interaction networks While Gimpel et al (2016) showed that 239

efficient gene expression needs to be accounted for when designing synthetic modules for the 240

transfer of photosystem subunits from one species to another Aigner et al (2017) 241

demonstrated that auxiliary factors required for the biogenesis of photosynthetic 242

(sub)complexes need to be considered in such experiments adding additional facets to the 243

ldquofrozen metabolic staterdquo concept 244

Auxiliary factors required for the accumulation of photosynthetic multiprotein 245

complexes include (i) cofactors like iron-sulfur clusters and pigments (see Box 2) (ii) 246


11

chaperones that are required for the insertion of co-factors (eg pigments into LHCs Schmid 247

2008) and (iii) assembly factors Assembly factors are required to support the stepwise 248

assembly and functionality of the multiproteinpigment complexes and many of these are 249

conserved between photosynthetic species (Nixon et al 2010 Nickelsen and Rengstl 2013 250

Jensen and Leister 2014) Therefore the exchange of entire multiprotein complexes between 251

distantly related species will not be simple due to the repertoire of auxiliary factors that has 252

markedly changed during evolution Since the species that Gimpel et al (2016) studied were 253

closely related this aspect could be neglected In consequence the impact of these auxiliary 254

factors on the formation of multiproteinpigment complexes will have to be fully elucidated 255

to understand which factors are sufficient to assemble a photosynthetic multiprotein complex 256

previous (genetic) approaches only identified factors required for this process Hence the 257

transfer of entire photosynthetic (sub)complexes between distantly related species by a 258

ldquosynthetic photosynthetic modulerdquo must include entire sets of strongly interacting proteins (to 259

address the ldquofrozen metabolic staterdquo) as well as all genetic elements and auxiliary factors 260

sufficient for efficient expression biogenesis and function of the proteins in the module 261

262

Bio-bio hybrids using photosynthesis as an electron source for unrelated biological 263

processes 264

The idea of using the reducing power of photosynthesis to drive unrelated metabolic reactions 265

has inspired several biotechnological concepts The photosynthesis-driven formation of 266

secondary metabolites has been demonstrated in vivo whereas light-driven generation of H2 267

by bio-bio hybrids so far works only in vitro and is closely related to bio-nano approaches 268

Therefore coupling of photosynthesis to previously unrelated pathways is discussed here 269

first followed by bio-bio systems for H2 generation 270


12

Redirection of PSI reducing equivalents to drive reactions catalyzed by cytochrome 271

P450 enzymes has been achieved in vivo by genetic modifications of plants and 272

cyanobacteria (Lassen et al 2014a Nielsen et al 2016 Mellor et al 2017) Cytochrome 273

P450s constitute the largest family of plant enzymes that acts on various endogenous and 274

xenobiotic molecules (Rasool and Mohamed 2016) Their extreme versatility and 275

irreversibility of catalyzed reactions make these enzymes very attractive for use in 276

biotechnology medicine and phytoremediation P450s are monooxygenases that insert an 277

oxygen atom into hydrophobic molecules which enhances their reactivity and hydrophilicity 278

Most eukaryotic P450s require NADPHcytochrome P450 reductase as the electron donor 279

The ER membrane is generally accepted to be the primary subcellular repository of 280

eukaryotic P450s and their NADPHcytochrome P450 reductase By relocating cytochrome 281

P450s to the chloroplasts the reducing power of photosynthesis can be directly targeted to 282

the reactions catalyzed by these enzymes thus providing the basis for the large-scale 283

production of valuable products Initial attempts to couple P450s with photosynthesis were 284

conducted in vitro (Table 3 Fig 4A) Spinach chloroplasts were combined with microsomes 285

from yeast cells that had been stably transformed with a fusion gene expressing the rat 286

CYP1A1-NADPHcytochrome P450 reductase fusion enzyme (Kim et al 1996) These 287

experiments confirmed that it is feasible to drive P450-mediated reactions using electrons 288

derived from photosynthetically generated NADPH Intriguingly the NADPHcytochrome 289

P450 reductase is not always essential as demonstrated by co-incubating CYP79A1 from 290

sorghum (Sorghum bicolor) with barley (Hordeum vulgare) PSI and employing ferredoxin to 291

directly deliver electrons from PSI to the P450 (Jensen et al 2011) This approach was also 292

shown to be practicable in vivo CYP79A1 either alone or in combination with CYP71E1 293

and the UDP-glucosyltransferase UGT85B1 was first targeted in vivo to cyanobacterial or 294

plant thylakoid membranes where they catalyzed the same reactions as in their original 295


13

cellular compartment (the ER) utilizing photosynthetically reduced ferredoxin as the electron 296

donor (Nielsen et al 2013 Lassen et al 2014b Gnanasekaran et al 2016 Wlodarczyk et 297

al 2016) Genetic fusions have also been employed for the coupling of P450s to PSI 298

CYP79A1 has been fused to either cyanobacterial PsaM or Arabidopsis ferredoxin and the 299

engineered enzyme showed light-driven activity both in vivo and in vitro (Lassen et al 300

2014b Mellor et al 2016) In the latter case the efficiency of the system was enhanced 301

because the fusion could compete better with endogenous electron sinks coupled to metabolic 302

pathways (Mellor et al 2016) 303

In contrast to PSI-P450 hybrids PSI-hydrogenase hybrids currently function only in 304

vitro Unlike fossil fuels H2 is environmentally benign as it produces only water when 305

combusted Therefore in principle harnessing of the reducing power of photosynthesis for 306

the direct production of H2 (ie ultimately using sunlight and water) would yield a fully 307

sustainable system of energy generation PSI but not PSII provides a standard midpoint 308

potential that is sufficiently negative to power the reduction of protons to H2 (Utschig et al 309

2015) Hence approaches have been developed to engineer PSI to produce H2 either as 310

replacement or in addition to its natural product NADPH (see Figure 1 in Box 1) by 311

redirecting PSI electrons to a catalytic component This catalytic component can be abiotic or 312

biotic (hydrogenases) The feasibility of coupling H2 generation to photosynthesis was 313

demonstrated 45 years ago by mixing chloroplast preparations with ferredoxin and 314

hydrogenase (Benemann et al 1973) Twenty-five years later hydrogen evolution by direct 315

electron transfer (without ferredoxin) from PSI to hydrogenases was accomplished for the 316

first time (McTavish 1998) 317

Hydrogenases catalyze the reversible interconversion of H2 into protons and electrons 318

and are widespread in nature they occur in bacteria and archaea but also in some eukarya In 319

vivo hydrogenases can mediate photosynthetic H2 production albeit mostly indirectly or 320


14

under anaerobic conditions due to their oxygen sensitivity (Ghirardi 2015 Oey et al 2016) 321

Hydrogenases can be classified according to their metal-ion composition eg [NiFe] and 322

[FeFe] hydrogenases (Lubitz et al 2014 Martin and Frymier 2017) [FeFe] hydrogenases 323

preferentially catalyze proton reduction and can evolve H2 at high rates but are extremely 324

sensitive to O2 and are the only type of hydrogenases found in eukaryotic microorganisms 325

[NiFe] hydrogenases are less sensitive to O2 but preferentially oxidize H2 under 326

physiological conditions (Lubitz et al 2014) In vitro both types of hydrogenases have been 327

directly linked to PSI (Table 3 Fig 4B) PSI-[NiFe] hydrogenase complexes have been 328

generated by fusing the hydrogenase genetically to the PsaE protein (Ihara et al 2006a) PSI-329

[FeFe] hydrogenase complexes were obtained by genetically fusing the hydrogenase to 330

ferredoxin (Yacoby et al 2011) or covalently linking the FeS clusters present in the 331

hydrogenase to PSI via a molecular wire (Lubner et al 2010 Lubner et al 2011) 332

Two parameters characterize the efficiency of these in-vitro systems their H2 333

production rate and longevity While low rates of H2 production (in the range from 01 to 10 334

μmol H2mg chlorophyllh) were described for the early chloroplast extract experiments and 335

genetic fusions of PSI to [NiFe] or [FeFe] hydrogenases (McTavish 1998 Ihara et al 2006a 336

Yacoby et al 2011) higher rates of between 2000 and 3000 μmol H2mg chlorophyllh have 337

been achieved with wired PSI-[FeFe] hydrogenase complexes and genetically fused PSI-338

[NiFe] hydrogenase complexes assembled on a gold electrode (Krassen et al 2009 Lubner 339

et al 2011) Few data are available with respect to the longevity of the PSI-hydrogenase 340

systems however a minimum lifetime of 64 days was reported for a wired [FeFe] 341

hydrogenase-PSI complex at room temperature and under ambient illumination (Lubner et 342

al 2010) 343

The future use of hydrogenases in photosynthesis-driven H2 production will strongly 344

depend on whether or not it is possible to overcome the O2 sensitivity of many hydrogenases 345


15

by for instance employing oxygen-tolerant [NiFe] hydrogenases (Burgdorf et al 2005 346

Schiffels et al 2013) If this is not possible their efficient use in vivo in thylakoids which 347

inevitably generate O2 during linear electron flow will be impossible However as 348

demonstrated with the gold surface system (Krassen et al 2009) the design of novel 349

matrices into which the hybrid system can be incorporated may markedly enhance the 350

efficiency 351

352

Bio-nano hybrids Use of photosynthesis as a source of electrons for non-biological 353

processes 354

From bio-bio hybrids it is only a small step to developing bio-nano hybrids as demonstrated 355

by PSI hybrids that employ abiotic catalysts for photosynthetic hydrogen production instead 356

of hydrogenase In fact abiotic catalysts have the advantage of bypassing the lability of 357

hydrogenases in the presence of oxygen PSI-platinum hybrids have been produced by 358

combining PSI with platinum nanoparticles (either directly or via tethering by nanowires) or 359

platinum nanoclusters (Kargul et al 2012 Fukuzumi 2015 Utschig et al 2015) (Fig 5A 360

Table 4) Current PSI-platinum hybrids are less efficient than the most advanced PSI-361

hydrogenase systems but are extremely robust (Utschig et al 2015) However future 362

widespread usage of the PSI-platinum system will be limited by the high cost of platinum A 363

more economical alternative to precious metals are earth-abundant molecular catalysts 364

However hybrids consisting of PSI and earth-abundant molecular catalysts have a much 365

shorter working life than platinum-based configurations (Utschig et al 2015) likely due to 366

instability of the molecular catalyst 367

PSI-based photocurrent-producing devices constitute another class of photosynthesis-368

derived nano-bio systems (Table 4 Fig 5) In such devices PSI is immobilized onto 369

electrodes Many variants of this concept have been tested such as varying the electrode 370


16

materials immobilizationorientation strategies andor artificial redox mediators (Nguyen and 371

Bruce 2014 Janna Olmos and Kargul 2015 Plumereacute and Nowaczyk 2017 Kargul et al 372

2018) PSI must be immobilized on the electrode surface in such a way that electron transfers 373

between the electrodes and the oxidizing (P700) and reducing (FB - the terminal [4Fe-4S] 374

cluster or an intermediate electron transporter) sites of PSI can proceed with the required 375

efficiency Electrons are transferred between the electrodes and the oxidizing or reducing 376

sides of PSI either by a diffusible redox mediator or molecular wires Examples of electrode 377

materials and redox mediators are provided in Table 4 After P700 photo-excitation electrons 378

are transferred from P700 via several factors (P700 rarr A0 rarr A1 rarr FX rarr FA rarr FB) to the 379

iron-sulfur cluster FB (see legend of Box 1) As in the case of PSI-hydrogenase and PSI-380

platinum nanoparticles PSI can be wired to its electrodes This has been achieved by wiring 381

the A1 cofactor (phylloquinone) to the substrate surface such that electrons are directly 382

transferred from A1 to the electrode thus bypassing the downstream FeS clusters (FX FA FB) 383

in the stromal domain of PSI (Terasaki et al 2007 Miyachi et al 2009 Terasaki et al 384

2009 Miyachi et al 2010) 385

Modifications of PSI have been utilized to enhance the efficiency of the photocurrent-386

generating system (Das et al 2004 Frolov et al 2005 Carmeli et al 2010) As mentioned 387

previously fusions to the stroma-faced PSI subunit PsaE can be used to link new components 388

to PSI however in this case PsaD fusions were used To this end recombinant His-tagged 389

PsaD was immobilized on the functionalized electrode surface which was then exposed to 390

native PSI complexes resulting in immobilized PSI with P700 facing away from the 391

electrode (Das et al 2004) Another way to control the orientation of PSI during 392

immobilization involves introducing cysteine mutations To allow for direct thiol coupling to 393

an Au surface various residues on the lumen-exposed face of PSI were replaced by cysteine 394

and tested (Frolov et al 2005) PSI attachment was achieved with all single mutants even 395


17

those placed further from the P700 site suggesting that a specific location is not required as 396

long as the cysteine is exposed at the luminal surface of PSI The concept of targeted 397

attachment via introduced cysteine residues was exploited in subsequent studies to link PSI to 398

maleimide-functionalized gallium arsenide (Frolov et al 2008) to immobilize PSI between 399

the substrate and a metallized scanning near-field optical microscopy tip (Gerster et al 400

2012) and to bind PSI to carbon nanotubes (Kaniber et al 2010) Another modification of 401

PSI is represented by the attachment of plasmonic metal nanoparticles which resulted in 402

enhanced light absorption (Carmeli et al 2010) even in the green part of the solar spectrum 403

that is not normally absorbed (Szalkowski et al 2017) This suggests that it is possible to 404

enhance light absorption by PSI in vitro through the attachment of abiotic components that 405

act as optical antennae to extend the spectrum of photons available for P700 activation 406

Taken together these efforts demonstrate that PSI-based photocurrent-generating 407

systems are still in an exploratory phase with many variants under development In the next 408

phase viable building blocks and reference systems should be established that can serve as 409

starting points for the systematic engineering of superior systems This will require the 410

modification of PSI for optimal effect in artificial systems and will undoubtedly differ 411

substantially from the original environment in which PSI was molded by biological 412

evolution 413

414

Concluding remarks and outlook 415

Enhancing photosynthesis and growth can be achieved by a simple overexpression of certain 416

photosynthetic proteins and PSI can be coupled to previously unconnected biotic or abiotic 417

components to generate valuable compounds hydrogen or electricity Moreover entire 418

photosynthetic complexes can be functionally expressed in distantly related species (as 419

demonstrated for RuBisCO Aigner et al 2017) Thus what are the next goals and which 420


18

challenges need to be overcome Two challenges for the in vivo systems are obvious (i) 421

enhancing the efficiency of in-vivo bio-bio hybrids and (ii) upscaling the size of ldquosynthetic 422

photosynthetic modulesrdquo to cover entire photosystems or complex antenna systems 423

With respect to the enhancement of in vivo cyanobacterial and algal systems 424

harboring hybrid configurations in which photosynthesis directly drives previously 425

unconnected pathways the use of laboratory evolution offers a unique opportunity to tailor 426

these systems for their intended purpose Laboratory evolution utilizes the high rate of 427

evolution typical in microbial systems (in particular if suitable selection conditions can be 428

designed) to fine tune and optimize processes through selection of advantageous genetic 429

variation While this strategy has been employed in E coli and yeast with impressive success 430

now photosynthetic microbial systems are emerging as attractive targets for this approach 431

(Leister 2017) 432

The exchange of entire multiprotein complexes between distantly related species will 433

not be a simple exercise because the ldquofrozen metabolic staterdquo of the core photosynthetic 434

complexes will necessitate the exchange of major parts of photosystems rather than 435

individual subunits The RuBisCO case study by Aigner et al (2017) represents of promising 436

proof of principle but one needs to consider that the synthetic RuBisCO module comprised 437

only the two different subunits present in the mature complex and five auxiliary factors for its 438

assembly Entire photosystems will require much larger ldquosynthetic photosynthetic modulesrdquo 439

and many of the auxiliary factors have not been identified yet Therefore when designing 440

these complex ldquosynthetic photosynthetic modulesrdquo we will identify the set of components 441

that are sufficient (and not only necessary) to drive photosynthesis providing an 442

unprecedentedly deep understanding of this fundamental and complex process 443

Given that the problems described above can be solved what will be the next steps in 444

the synthetic biology of the light reactions of photosynthesis The combination of ldquosynthetic 445


19

photosynthetic modulesrdquo from diverse species could allow the design of novel variants of 446

photosynthesis Numerous instances of such ldquorecombined photosynthetic variantsrdquo can be 447

imagined including plants that employ cyanobacteria-derived phycobilisomes for highly 448

sufficient photosynthesis under low light conditions cyanobacteria that employ plant-derived 449

LHCs as antenna to shift light saturation of photosynthesis to higher intensities or the 450

integration of cyanobacterial Chl d and Chl f (which can absorb far-red and near infra-red 451

light) into algal or plant photosynthesis to expand the spectral region available to drive 452

photosynthesis (Loughlin et al 2013 Ho et al 2016) Moreover such variants of 453

recombined photosynthesis could be further optimized by laboratory evolution within a 454

suitable microbial chassis However such recombined photosynthetic variants cannot be 455

considered a truly novel type of photosynthesis because they would only bring preexisting 456

pieces together that evolution has separated Nevertheless they could be an important step 457

towards the ambitious goal to design truly novel ldquosynthetic photosynthetic modulesrdquo that 458

contain more efficient substitutes of the ldquofrozen metabolic accidentsrdquo discussed above 459

Ample proof of functionality for in-vivo hybrids (between photosynthesis and 460

previously unconnected metabolic pathways) and in-vitro hybrids (between PSI and biotic or 461

abiotic catalysts) has been obtained but such systems will only be commercially successful if 462

they can compete with established non-biological systems Tailoring of PSI in cyanobacteria 463

where techniques like gene replacement and gene modification are routine may contribute to 464

further improving the efficiency and robustness of in vitro and in vivo hybrids One 465

promising route could be to identify those parts of the original PSI (which evolved under 466

constraints imposed by the cyanobacterial cell) that are necessary for hybrid devices (a 467

ldquominimalrdquo PSI) Such bio-nano systems can be optimized to include novel non-biological 468

components that replace or complement natural pigments andor the protein-based backbone 469

of photosystems going far beyond the limited toolbox of Naturersquos chemistry Such novel 470


20

systems inspired by natural photosynthesis could be used to engage biologists in the design 471

of fundamentally different types of photosynthesis in living organisms 472

473

SUPPLEMENTAL DATA 474

Supplemental Table 1 Absencepresence of photosynthetic proteins in the three model 475

species Synechocystis PCC6803 (Syn) Chlamydomonas reinhardtii (Cr) and Arabidopsis 476

thaliana (At) 477

478

ACKNOWLEDGMENTS 479

The authors thank Paul Hardy for critical reading of the manuscript 480

481

482


21

Table 1 Replacement of conserved individual or multiple photosynthetic proteins 483

GeneProtein Description Protein

identity

Reference

psbAD1 Synechocystis D1 was replaced by its homolog from

Poa annua which resulted in slower growth This is

likely to be due to increased charge recombination

between the donor and acceptor sides of the reaction

center

86 Nixon et al

1991

psbBCP47 Synechocystis CP47 was replaced by its homolog

from spinach and photoautotrophy was lost

80 Vermaas et

al 1996

psbCCP43 Synechocystis CP43 was replaced by its homolog


85 Carpenter et

al 1993

psbHPsbH Synechocystis PsbH was replaced by its counterpart

from maize The resulting strain displayed increased

light sensitivity and lower chlorophyll content

78 Chiaramonte

et al 1999

psaAPsaA Synechocystis PsaA was replaced by its equivalent

from A thaliana This resulted in reduced photo-

autotrophical growth and a drastically reduced

ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+

All six core subunits of C reinhardtii were replaced

by their counterparts from two different green algae

(V carteri and S obliquus) The resulting strains

were photoautotrophic but showed reduced

photosynthetic efficiency and the heterologous

82 -

99

Gimpel et al

2016


22

proteins reached only between 10 and 20 of the

levels of those they replaced

484

485


23

Table 2 Introduction of heterologous photosynthetic proteins (protein complexes) 486

GeneProtein Description Reference

PetJCytochrome c6 Growth and photosynthesis of Arabidopsis

thaliana plants was enhanced by the

expression of a red algal (Porphyra yezoensis)

cytochrome c6 gene

Chida et al

2007

flavodoxinflavodoxin Tobacco lines expressing a plastid-targeted

cyanobacterial flavodoxin in addition to

endogenous ferredoxin display increased

tolerance to environmental stress Flavodoxin

can at least partially replace ferredoxin in

tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)

FlvA and FlvB from the moss Physcomitrella

patens mediate pseudocyclic electron flow in

A thaliana

Yamamoto et

al 2016

LhcbLHCII Pea Lhcb protein is synthesized in

Synechocystis and integrated into the

membrane but is then degraded such that it

cannot be detected by immunoblot analysis

He et al

1999

487

488


24

Table 3 Combination of PSI with non-photosynthetic proteins or complexes bio-bio 489

hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)

Spinach chloroplasts were combined with

microsomes from yeast expressing the rat

CYP1A1CPR fusion enzyme In this system

NADP+ was photosynthetically reduced to

NADPH to supply the electrons for P450 thus

enabling light-driven conversion of 7-

ethoxycoumarin to 7-hydroxycoumarin

Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)

The ER-derived P450 CYP79A1 was capable of

converting tyrosine to hydroxyphenyl-

acetaldoxime employing ferredoxin reduced by

barley PSI (without the need for NADPH and

CPR) In the next step CYP79A1 was fused to

cyanobacterial PsaM or Arabidopsis ferredoxin

The engineered fusions exhibited light-driven

activity both in vivo and in vitro

Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)

The two P450s CYP79A1 and CYP71E1 and the

UDP-glucosyltransferase UGT85B1 were

targeted to N benthamiana or Synechocystis

thylakoid membranes where they converted

tyrosine to dhurrin employing photosynthetically

Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin

PSI-hydrogenase hybrids

Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)

A fusion of cyanobacterial PsaE to an [NiFe]

hydrogenase from the -proteobacterium

Ralstonia eutropha was reconstituted into a

PsaE-deficient PSI from Synechocystis by self-

assembly In a modified version of this system

cytochrome c3 from Desulfovibrio vulgaris was

cross-linked to the docking site of ferredoxin in

PsaE targeting electrons directly from PSI via

cytochrome c3 to the hydrogenase This gave the

hydrogenase a competitive advantage over the

natural acceptors of electrons from PSI

In a third variant of this system the R eutropha

hydrogenase was genetically fused to

Synechocystis PsaE and reconstituted into a

PsaE-deficient PSI from Synechocystis His-

tagging of PsaF enabled assembly of the PSI-

hydrogenase hybrid onto a gold electrode

Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)

The Chlamydomonas hydrogenase was fused to

ferredoxin This switched the bias of electron

transfer from FNR to hydrogenase and resulted

in an increased rate of hydrogen

photoproduction in vitro

Yacoby et al

2011

Bacterial [FeFe] To enable transfer of electrons from the terminal Lubner et al


26

hydrogenase wired

to cyanobacterial

PSI (in vitro)

Fe4S4 cluster in PSI of Synechococcus sp PCC

7002 to the distal Fe4S4 cluster in the

hydrogenase from Clostridium acetobutylicum

the two components were covalently coupled to

each other via a molecular wire ndash the thiolated

organic molecule octanedithiol This allowed

electrons to tunnel through the wire from PSI to

the hydrogenase Self-assembly of the PSI-wire-

hydrogenase complex was obtained in vitro

2010 Lubner

et al 2011

491

492

493


27

Table 4 Combination of PSI with non-biological materials bio-nano hybrids 494

System non-biological

components

Description Reference

H2-producing PSI bio-

nano hybrids

PSI-biohybrid photocatalytic systems for H2

production contain cyanobacterial PSI and

precious metal catalysts including platinum

nanoparticles platinum nanowires and

platinum nanoclusters Examples for earth-

abundant molecular catalysts in PSI-

biohybrids include cobaloxime Ni

diphosphine and Ni-apoflavodoxin

reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based

photocurrent-generating

bio-nano hybrids

PSI-based photocurrent-generating devices

contain PSI from either plants or

cyanobacteria immobilized on electrode

materials such as Au graphene indium tin

oxide (ITO) fluorine-doped tin oxide

(FTO) TiO2 glass ZnO or alumina The

most commonly utilized immobilization

strategies involve the usage of organothiol-

based self-assembled monolayers (SAMs)

Electron donors to PSI include sodium

ascorbate 26-dichlorophenolindophenol

reduced ferricyanide osmium complexes

ruthenium hexamine trichloride PSI or the

reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28

immobilization wire (NTAndashNindashHis6ndashPSI)

Acceptors of PSI electrons include

naphthoquinone-derivative molecular wire

methyl viologen oxidized ferricyanide

composite Bis-aniline nanoparticle-

ferredoxin and methylene blue Also all-

solid-state PSI-based solar cells that do not

employ any exogenous redox mediators or

buffer solutions have been generated

495


29

FIGURE LEGENDS 496

497

Figure 1 Subunit composition of cyanobacterial (Synechocystis) and plant 498

(Arabidopsis) thylakoid multiprotein complexes 499

Subunits specific to either the cyanobacterium Synechocystis or the flowering plant 500

Arabidopsis are indicated by black shading subunits with domains specific to one group of 501

organisms are shown in dark grey conserved subunits in light grey c6 cytochrome c6 Cyt 502

b6f cytochrome b6f complex Fd ferredoxin Fv flavodoxin FLV flavodiiron protein FNR 503

ferredoxin-NADP reductase LHCI (II) light-harvesting complex I (II) PSI (II) photosystem 504

I (II) 505

For reasons of clarity the ATP synthase and NAD(P)H dehydrogenase complex are not 506

shown 507

508

Figure 2 Overview of genetic engineering and synthetic biology approaches related to 509

the light reactions of photosynthesis 510

Different shading is used to indicate cyanobacterial (blue) and plant (green) proteins 511

(complexes) and proteins (complexes) that are typically not directly associated with 512

photosynthesis (red) Yellow shading indicates non-biological materials For designation of 513

proteins see Fig Box 1 514

515

Figure 3 Evolutionary plasticity of the photosynthetic proteome 516

The changes in the composition of the inventory of photosynthetic proteins (top panel) during 517

evolution from the cyanobacterial endosymbiont to the chloroplast in flowering plants 518

(bottom panel) are shown As proxies for the original endosymbiont and the unicellular 519

chloroplast-containing protist that gave rise to flowering plants the model cyanobacterium 520


30

Synechocystis PCC6803 the model green alga C reinhardtii (middle) and the model 521

flowering plant A thaliana (right) are used In the top panel left side the entire inventory of 522

photosynthetic proteins in the Synechocystis PCC6803 is listed and assigned to the five 523

different classes ldquoPSIIrdquo ldquoPSIrdquo other electron transport components (ldquoother ETrdquo) ldquoantennardquo 524

and ldquophotoprotectionrdquo whereby the transition from ldquoother ETrdquo to ldquophotoprotectionrdquo is fluid 525

The proteins that have been acquired or lost during evolution in C reinhardtii and A thaliana 526

are listed in the middle and right section respectively of the top panel Note that for reasons 527

of simplicity we have not considered the ATP synthase complex in this figure The NDH 528

complex (or Nda2 in case of C reinhardtii) appears only as a whole (without its individual 529

subunits) in this figure NDH listed in parentheses indicates that the NDH complex is 530

specifically lost only in C reinhardtii and that therefore the plant NDH complex is not a re-531

acquisition Accordingly Nda2 replaces the NDH complex in C reinhardtii A detailed 532

catalogue of the indicated proteins with their full names functions and further literature links 533

is available in Supplemental Table 1 The bottom panel provides a sketch of the evolution of 534

flowering plants that traces back to the endosymbiosis between a unicellular eukaryote and a 535

cyanobacterium resulting (besides the red algal and glaucophyte lineages that are not shown) 536

in chloroplast-containing protists that further evolved to plants 537

538

Figure 4 Design of bio-bio hybrids 539

A Harnessing the reducing power of photosynthesis for cytochrome P450 enzymes (red) has 540

been demonstrated in vitro and in vivo In-vitro approaches were based either on a CPR-541

CYP1A1 fusion protein that could use NADPH produced by photosynthesis or on CYP79A1 542

that can directly utilize photoreduced ferredoxin The latter approach was also realized in 543

vivo by fusing CYP79A1 to ferredoxin (not shown) or the PSI subunit PsaM The most 544


31

elaborate approach reported utilizes three enzymes (CYP79A1 CYP71E1 and UGT85B1) to 545

couple dhurrin synthesis with photosynthesis 546

B PSI-hydrogenase complexes are either based on genetic fusions of the hydrogenase (Hyd) 547

to PsaE or ferredoxin or on covalent linking of the hydrogenase and PSI via a molecular 548

wire Currently these bio-bio hybrids function only in vitro 549

550

Figure 5 Design of selected bio-nano hybrids 551

A PSI-platinum hybrids are generated by combining platinum nanoparticles (dots) or 552

nanoclusters (star) with PSI Platinum nanoparticles can also be linked to PSI via nanowires 553

B PSI-based photocurrent-generating system A variety of such systems have been 554

developed which consist of PSI molecules immobilized on electrodes and implement electron 555

transfer by means of diffusible redox mediators or nanowires Moreover all-solid-state PSI-556

based solar cells and systems in which cytochrome c was employed to interface PSI with 557

electrode materials have been generated (Gordiichuk et al 2014 Gizzie et al 2015 Janna 558

Olmos et al 2017 Ciornii et al 2017) The circle-containing cross indicates a current-using 559

device and the yellow rectangles symbolize the electrodes 560

561

562

563

564


32

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566

Aigner H Wilson RH Bracher A Calisse L Bhat JY Hartl FU Hayer-Hartl M (2017) 567

Plant RuBisCo assembly in E coli with five chloroplast chaperones including BSD2 568

Science 358 1272-1278 569

Benemann JR Berenson JA Kaplan NO Kamen MD (1973) Hydrogen evolution by a 570

chloroplast-ferredoxin-hydrogenase system Proc Natl Acad Sci U S A 70 2317-2320 571

Blanco NE Ceccoli RD Segretin ME Poli HO Voss I Melzer M Bravo-Almonacid FF 572

Scheibe R Hajirezaei MR Carrillo N (2011) Cyanobacterial flavodoxin 573

complements ferredoxin deficiency in knocked-down transgenic tobacco plants Plant 574

J 65 922-935 575

Blankenship RE Chen M (2013) Spectral expansion and antenna reduction can enhance 576

photosynthesis for energy production Curr Opin Chem Biol 17 457-461 577

Burgdorf T Lenz O Buhrke T van der Linden E Jones AK Albracht SP Friedrich B 578

(2005) [NiFe]-hydrogenases of Ralstonia eutropha H16 modular enzymes for 579

oxygen-tolerant biological hydrogen oxidation J Mol Microbiol Biotechnol 10 181-580

96 581

Carmeli I Lieberman I Kraversky L Fan Z Govorov AO Markovich G Richter S 582

(2010) Broad band enhancement of light absorption in photosystem I by metal 583

nanoparticle antennas Nano Lett 10 2069-2074 584

Carpenter SD Ohad I Vermaas WF (1993) Analysis of chimeric spinachcyanobacterial 585

CP43 mutants of Synechocystis sp PCC 6803 the chlorophyll-protein CP43 affects 586

the water-splitting system of Photosystem II Biochim Biophys Acta 1144 204-212 587

Chang H Huang HE Cheng CF Ho MH Ger MJ (2017) Constitutive expression of a 588

plant ferredoxin-like protein (pflp) enhances capacity of photosynthetic carbon 589

assimilation in rice (Oryza sativa) Transgenic Res 26 279-289 590

Chiaramonte S Giacometti GM Bergantino E (1999) Construction and characterization of 591

a functional mutant of Synechocystis 6803 harbouring a eukaryotic PSII-H subunit 592

Eur J Biochem 260 833-843 593

Chida H Nakazawa A Akazaki H Hirano T Suruga K Ogawa M Satoh T Kadokura 594

K Yamada S Hakamata W Isobe K Ito T Ishii R Nishio T Sonoike K Oku T 595

(2007) Expression of the algal cytochrome c6 gene in Arabidopsis enhances 596

photosynthesis and growth Plant Cell Physiol 48 948-957 597


33

Ciornii D Riedel M Stieger KR Feifel SC Hejazi M Lokstein H Zouni A Lisdat F 598

(2017) Bioelectronic Circuit on a 3D Electrode Architecture Enzymatic Catalysis 599

Interconnected with Photosystem I J Am Chem Soc 139 16478-16481 600

Dann M Leister D (2017) Enhancing (crop) plant photosynthesis by introducing novel 601

genetic diversity Philos Trans R Soc Lond B Biol Sci 372 602

Das R Kiley PJ Segal M Norville J Yu AA Wang L Trammell SA Reddick LE 603

Kumar R Stellacci F Lebedev N Schnur J Bruce BD Zhang S Baldo M (2004) 604

Integration of photosynthetic protein molecular complexes in solid-state electronic 605

devices Nano Letters 4 1079-1083 606

de Bianchi S Ballottari M Dallosto L Bassi R (2010) Regulation of plant light harvesting 607

by thermal dissipation of excess energy Biochem Soc Trans 38 651-660 608

Frolov L Rosenwaks Y Carmeli C Carmeli I (2005) Fabrication of a photoelectronic 609

device by direct chemical binding of the photosynthetic reaction center protein to 610

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between GaAs and photosynthetic reaction center protein J Phys Chem C 112 613

13426-13430 614

Fukuzumi S (2015) Artificial photosynthetic systems for production of hydrogen Curr Opin 615

Chem Biol 25 18-26 616

Gerster D Reichert J Bi H Barth JV Kaniber SM Holleitner AW Visoly-Fisher I 617

Sergani S Carmeli I (2012) Photocurrent of a single photosynthetic protein Nat 618

Nanotechnol 7 673-676 619

Ghirardi ML (2015) Implementation of photobiological H2 production the O2 sensitivity of 620

hydrogenases Photosynth Res 125 383-93 621

Gimpel JA Nour-Eldin HH Scranton MA Li D Mayfield SP (2016) Refactoring the six-622

gene photosystem II core in the chloroplast of the green algae Chlamydomonas 623

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Gizzie EA Niezgoda JS Robinson MT Harris AG Jennings GK Rosenthal SJ 625

Cliffel DE (2015) Photosystem I-polyanilineTiO2 solid-state solar cells simple 626

devices for biohybrid solar energy conversion Energy Environ Sci 8 3572-3576 627

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Gautier DA Catarci S Pesce D Richter S Blom PW Herrmann A (2014) Solid-629

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DR Niyogi KK Long SP (2018) Photosystem II subunit S overexpression increases 632

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Gnanasekaran T Karcher D Nielsen AZ Martens HJ Ruf S Kroop X Olsen CE 634

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cytochrome P450-dependent dhurrin pathway from Sorghum bicolor into Nicotiana 636

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R Kargul JM (2018) Molecular mechanisms of photoadaptation of photosystem I 639

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176 1433-1451 641

He Q Schlich T Paulsen H Vermaas W (1999) Expression of a higher plant light-642

harvesting chlorophyll ab-binding protein in Synechocystis sp PCC 6803 Eur J 643

Biochem 263 561-570 644

Ho MY Shen G Canniffe DP Zhao C Bryant DA (2016) Light-dependent chlorophyll f 645

synthase is a highly divergent paralog of PsbA of photosystem II Science 353 646

Holt NE Fleming GR Niyogi KK (2004) Toward an understanding of the mechanism of 647

nonphotochemical quenching in green plants Biochemistry 43 8281-8289 648

Ihara M Nishihara H Yoon KS Lenz O Friedrich B Nakamoto H Kojima K Honma 649

D Kamachi T Okura I (2006a) Light-driven hydrogen production by a hybrid 650

complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I Photochem 651

Photobiol 82 676-682 652

Ihara M Nakamoto H Kamachi T Okura I Maeda M (2006b) Photoinduced hydrogen 653

production by direct electron transfer from photosystem I cross-linked with 654

cytochrome c3 to [NiFe]-hydrogenase Photochem Photobiol 82 1677-1685Janna 655

Olmos JD Kargul J (2015) A quest for the artificial leaf Int J Biochem Cell Biol 656

66 37-44 657

Janna Olmos JD Becquet P Gront D Sar J Dąbrowski A Gawlik G Teodorczyk M 658

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c553 minimises charge recombination and enhances photovoltaic performance of the 660

all-solid-state photosystem I-based biophotoelectrode RSC Adv 7 47854-47866 661

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ACS Chem Biol 6 533-539 663


35

Jensen PE Leister D (2014) Chloroplast evolution structure and functions F1000Prime 664

Rep 6 40 665

Kaniber SM Brandstetter M Simmel FC Carmeli I Holleitner AW (2010) On-chip 666

functionalization of carbon nanotubes with photosystem I J Am Chem Soc 132 667

2872-2873 668

Kargul J Janna Olmos JD Krupnik T (2012) Structure and function of photosystem I and 669

its application in biomimetic solar-to-fuel systems J Plant Physiol 169 1639-1653 670

Kargul J Bubak G Andryianau G (2018) Biophotovoltaic systems based on 671

photosynthetic complexes In Wandelt K (Ed) Encyclopedia of Interfacial 672

Chemistry Surface Science and Electrochemistry vol 7 pp 43-63 673

Kim YS Hara M Ikebukuro K Miyake J Ohkawa H Karube I (1996) Photo-induced 674

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chloroplasts Biotechnol Tech 10 717minus720 676

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hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase 678

ACS Nano 3 4055-4061 679

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Improving photosynthesis and crop productivity by accelerating recovery from 681

photoprotection Science 354 857-861 682

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EM Wada H (2010) Purification and characterization of photosystem I complex 684

from Synechocystis sp PCC 6803 by expressing histidine-tagged subunits Biochim 685

Biophys Acta 1797 98-105 686

Lassen LM Nielsen AZ Ziersen B Gnanasekaran T Moller BL Jensen PE (2014a) 687

Redirecting photosynthetic electron flow into light-driven synthesis of alternative 688

products including high-value bioactive natural compounds ACS Synth Biol 3 1-12 689

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Anchoring a plant cytochrome P450 via PsaM to the thylakoids in Synechococcus sp 691

PCC 7002 evidence for light-driven biosynthesis PLoS One 9 e102184 692

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Plant Sci 3 199 694

Leister D (2017) Experimental evolution in photoautotrophic microorganisms as a means of 695

enhancing chloroplast functions Essays Biochem DOI 101042EBC20170010 696


36

Leister D Shikanai T (2013) Complexities and protein complexes in the antimycin A-697

sensitive pathway of cyclic electron flow in plants Front Plant Sci 4 161 698

Lin YH Pan KY Hung CH Huang HE Chen CL Feng TY Huang LF (2013) 699

Overexpression of ferredoxin PETF enhances tolerance to heat stress in 700

Chlamydomonas reinhardtii Int J Mol Sci 14 20913-20929 701

Long SP Marshall-Colon A Zhu XG (2015) Meeting the global food demand of the future 702

by engineering crop photosynthesis and yield potential Cell 161 56-66 703

Loughlin P Lin Y Chen M (2013) Chlorophyll d and Acaryochloris marina current status 704

Photosynth Res 116 277-293 705

Lubitz W Ogata H Rudiger O Reijerse E (2014) Hydrogenases Chem Rev 114 4081-706

4148 707

Lubner CE Applegate AM Knorzer P Ganago A Bryant DA Happe T Golbeck JH 708

(2011) Solar hydrogen-producing bionanodevice outperforms natural photosynthesis 709

Proc Natl Acad Sci U S A 108 20988-20991 710

Lubner CE Knorzer P Silva PJ Vincent KA Happe T Bryant DA Golbeck JH (2010) 711

Wiring an [FeFe]-hydrogenase with photosystem I for light-induced hydrogen 712

production Biochemistry 49 10264-10266 713

Martin BA Frymier PD (2017) A review of hydrogen production by photosynthetic 714

organisms using whole-cell and cell-free systems Appl Biochem Biotechnol 183 715

503-519 716

McTavish H (1998) Hydrogen evolution by direct electron transfer from photosystem I to 717

hydrogenases J Biochem 123 644-649 718

Mellor SB Nielsen AZ Burow M Motawia MS Jakubauskas D Moller BL Jensen PE 719

(2016) Fusion of ferredoxin and cytochrome P450 enables direct light-driven 720

biosynthesis ACS Chem Biol 11 1862-1869 721

Mellor SB Vavitsas K Nielsen AZ Jensen PE (2017) Photosynthetic fuel for heterologous 722

enzymes the role of electron carrier proteins Photosynth Res 134 329-342 723

Miyachi M Yamanoi Y Shibata Y Matsumoto H Nakazato K Konno M Ito K Inoue 724

Y Nishihara H (2010) A photosensing system composed of photosystem I 725

molecular wire gold nanoparticle and double surfactants in water Chem Commun 726

(Camb) 46 2557-2559 727

Miyachi M Yamanoi Y Yonezawa T Nishihara H Iwai M Konno M Iwai M Inoue Y 728

(2009) Surface immobilization of PSI using vitamin K1-like molecular wires for 729

fabrication of a bio-photoelectrode J Nanosci Nanotechnol 9 1722-1726 730


37

Molina-Heredia FP Wastl J Navarro JA Bendall DS Hervas M Howe CJ De La Rosa 731

MA (2003) Photosynthesis a new function for an old cytochrome Nature 424 33-34 732

Mullineaux CW Emlyn-Jones D (2005) State transitions an example of acclimation to 733

low-light stress J Exp Bot 56 389-393 734

Nelson N (2009) Plant photosystem I--the most efficient nano-photochemical machine J 735

Nanosci Nanotechnol 9 1709-1713 736

Nguyen K Bruce BD (2014) Growing green electricity progress and strategies for use of 737

photosystem I for sustainable photovoltaic energy conversion Biochim Biophys Acta 738

1837 1553-1566 739

Nickelsen J Rengstl B (2013) Photosystem II assembly from cyanobacteria to plants Annu 740

Rev Plant Biol 64 609-635 741

Nielsen AZ Mellor SB Vavitsas K Wlodarczyk AJ Gnanasekaran T Perestrello 742

Ramos HdJM King BC Bakowski K Jensen PE (2016) Extending the 743

biosynthetic repertoires of cyanobacteria and chloroplasts Plant J 87 87-102 744

Nielsen AZ Ziersen B Jensen K Lassen LM Olsen CE Moller BL Jensen PE (2013) 745

Redirecting photosynthetic reducing power toward bioactive natural product 746

synthesis ACS Synth Biol 2 308-315 747

Nixon PJ Michoux F Yu J Boehm M Komenda J (2010) Recent advances in 748

understanding the assembly and repair of photosystem II Ann Bot 106 1-16 749

Nixon PJ Rogner M Diner BA (1991) Expression of a higher plant psbA gene in 750

Synechocystis 6803 yields a functional hybrid photosystem II reaction center 751

complex Plant Cell 3 383-395 752

Oey M Sawyer AL Ross IL Hankamer B (2016) Challenges and opportunities for 753

hydrogen production from microalgae Plant Biotechnol J 14 1487-99 754

Pesaresi P Pribil M Wunder T Leister D (2011) Dynamics of reversible protein 755

phosphorylation in thylakoids of flowering plants the roles of STN7 STN8 and 756

TAP38 Biochim Biophys Acta 1807 887-896 757

Pesaresi P Scharfenberg M Weigel M Granlund I Schroder WP Finazzi G 758

Rappaport F Masiero S Furini A Jahns P Leister D (2009) Mutants 759

overexpressors and interactors of Arabidopsis plastocyanin isoforms revised roles of 760

plastocyanin in photosynthetic electron flow and thylakoid redox state Mol Plant 2 761

236-248 762

Pinnola A Ghin L Gecchele E Merlin M Alboresi A Avesani L Pezzotti M Capaldi 763

S Cazzaniga S Bassi R (2015) Heterologous expression of moss light-harvesting 764


38

complex stress-related 1 (LHCSR1) the chlorophyll a-xanthophyll pigment-protein 765

complex catalyzing non-photochemical quenching in Nicotiana sp J Biol Chem 290 766

24340-24354 767

Plumereacute N Nowaczyk MM (2016) Biophotoelectrochemistry of photosynthetic proteins 768

Adv Biochem Eng Biotechnol 158 111-136 769

Pribil M Pesaresi P Hertle A Barbato R Leister D (2010) Role of plastid protein 770

phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow PLoS 771

Biol 8 e1000288 772

Rasool S Mohamed R (2016) Plant cytochrome P450s nomenclature and involvement in 773

natural product biosynthesis Protoplasma 253 1197-1209 774

Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation FEBS 775

Lett 581 2768-2775 776

Schiffels J Pinkenburg O Schelden M Aboulnaga el-HA Baumann ME Selmer T 777

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of an oxygen-tolerant [NiFe]-hydrogenase from Cupriavidus necator in Escherichia 779

coli PLoS One 8 e6881 780

Schmid VH (2008) Light-harvesting complexes of vascular plants Cell Mol Life Sci 65 781

3619-3639 782

Shi T Bibby TS Jiang L Irwin AJ Falkowski PG (2005) Protein interactions limit the 783

rate of evolution of photosynthetic genes in cyanobacteria Mol Biol Evol 22 2179-784

2189 785

Simkin AJ McAusland L Lawson T Raines CA (2017) Overexpression of the RieskeFeS 786

Protein Increases Electron Transport Rates and Biomass Yield Plant Physiol 175 787

134-145 788

Szalkowski M Janna Olmos JD Buczyńska D Maćkowski S Kowalska D Kargul J 789

(2017) Plasmon-induced absorption of blind chlorophylls in photosynthetic proteins 790

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792

Terasaki N Yamamoto N Hiraga T Yamanoi Y Yonezawa T Nishihara H Ohmori T 793

Sakai M Fujii M Tohri A Iwai M Inoue Y Yoneyama S Minakata M Enami I 794

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1585-1587 797


39

Terasaki N Yamamoto N Tamada K Hattori M Hiraga T Tohri A Sato I Iwai M 798

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(2006) Functional replacement of ferredoxin by a cyanobacterial flavodoxin in 804

tobacco confers broad-range stress tolerance Plant Cell 18 2035-2050 805

Tognetti VB Zurbriggen MD Morandi EN Fillat MF Valle EM Hajirezaei MR 806

Carrillo N (2007) Enhanced plant tolerance to iron starvation by functional 807

substitution of chloroplast ferredoxin with a bacterial flavodoxin Proc Natl Acad Sci 808

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843

844







ADVANCES

bull Individual photosynthetic proteins can be exchanged between species but the replacement of proteins embedded in photosynthetic multiprotein complexes is complicated due to their ldquofrozen metabolic staterdquo

bull Entire multiprotein (sub)complexes can be exchanged via ldquosynthetic photosynthetic modulesrdquo that contain a sufficient number of proteins to overcome the ldquofrozen metabolic staterdquo as well as all genetic elements and auxiliary factors for their efficient expression biogenesis and function

bull Overexpression of photosynthetic proteins that are not organized in complexes can enhance photosynthetic efficiency and growth

bull Photosynthesis can be coupled in vivo to previously unrelated enzymes and pathways to enable light-driven production of valuable compounds

bull Photosystem I is a highly efficient and robust nano-photochemical machine that can be technically applied in vitro for the production of hydrogen or electricity


OUTSTANDING QUESTIONS

bull Can photosynthesis be enhanced by combining ldquosynthetic photosynthetic modulesrdquo from different species

bull Can the ldquofrozen metabolic accidentsrdquo be substituted by more efficient proteins via re-designing ldquosynthetic photosynthetic modulesrdquo

bull Can a fundamentally different type of photosynthesis be realized

bull Can bio-bio and bio-nano hybrids be generated efficiently and provide valuable substances and energy safely and economically


BOX 1 The Conserved Basic Principle of

Photosynthesis

Cyanobacteria and plants possess two photosystems photosystems I (PSI) and II (PSII see Fig 1 and Fig Box 1) which respond optimally to light of different wavelengths Upon absorption of light PSII transfers electrons to plastoquinone (an electron carrier located in the thylakoid membrane) and these electrons are replaced by electrons obtained through the oxidation of water which produces oxygen Plastoquinone transfers its electrons to PSI via the cytochrome b6f complex (Cyt b6f) and a soluble electron carrier in the thylakoid lumen (plastocyanin or cytochrome c6) Upon an additional light absorption step electrons are transferred from the reaction center of PSI (P700 chlorophyll a) via a number of cofactors (P700 rarr A0 rarr A1 rarr FX rarr FA rarr FB with A0 being a chlorophyll a molecule A1 a phylloquinone molecule and FA FB and FX being iron-sulfur clusters) to soluble electron carriers (ferredoxin or flavodoxin) on the other side of the thylakoid membrane and from there to NADP+ to generate NADPH Protons accumulate in the thylakoid lumen during the oxidation of water and electron transfer through Cyt b6f The energy released by the passage of protons back across the thylakoid membrane is harnessed by the ATPase complex to produce ATP This process involving both photosystems is known as linear electron flow (see Fig Box 1) Cyclic electron flow is an alternative process that involves the movement of electrons around PSI only and drives the formation of ATP without the production of NADPH The basic structure of the multiprotein complexes involved in linear or cyclic electron flow is conserved between cyanobacteria and plants but both cyanobacteria and plants contain a number of specific subunits (see Fig 1)

Figure Box 1 Scheme of linear (A) and cyclic electron flow (B)

Components specific to cyanobacteria or plants are highlighted in blue and green respectively Conserved components are shown in gray AA antimycin A NDH NAD(P)H dehydrogenase complex OEC oxygen-evolving complex otherwise the same abbreviations as in Fig 1 are used



BOX 2 Where Photosynthesis Varies Most

Antennas Pigments and Regulation

The photosynthetic machineries of cyanobacteria and plants differ markedly in their light-harvesting pigment-protein complexes and their regulation Cyanobacteria harvest light with phycobilisomes giant soluble complexes associated with the inner membrane surface that contain phycobiliproteins Plants employ intramembranous antennae the light-harvesting complexes I (LHCI) and II (LHCII) Additional Lhc proteins (CP24 CP26 CP29 and PsbS) are present in the PSII of plants but not in cyanobacteria (see Fig 1)

In addition the pigment composition-- particularly that of the light-harvesting systems--differs between cyanobacteria and plants In both cyanobacteria and plants PSI and PSII (without CP24 CP26 and CP29) bind chlorophyll (Chl) a and β-carotene molecules but phycobilisomes contain linear tetrapyrroles (bilins) as pigments LHCI contains Chl a and b and the carotenoids violaxanthin lutein and β-carotene In LHCII and the inner antenna proteins CP24 CP26 and CP29 neoxanthin substitute for β-carotene Both cyanobacteria and plants utilize Chl a and β-carotene but plants use Chl b and the carotenoids lutein violaxanthin and neoxanthin although cyanobacteria can synthesize their precursors (zeaxanthin and lycopene)

Photosynthetic electron flow is regulated at various levels of which three are highlighted here (1) Adjustment of the ratio of linear to cyclic electron flow (CEF) controls the output of photosynthesis in terms of the ATPNADPH ratio One major CEF route is antimycin A-sensitive and involves the PGRL1PGR5 complex in plants cyanobacteria lack this complex (Leister and Shikanai 2013 see Fig Box 1 and Fig 1) (2) In plants excess energy absorbed during exposure to high light levels can be dissipated by LHCII via a mechanism known as the energy-dependent component (qE) of non-photochemical quenching (NPQ) which involves the xanthophyll cycle (with enzymes like violaxanthin de-epoxidase and zeaxanthin epoxidase) and the PSII subunit PsbS and is activated by a decrease in pH in the thylakoid lumen (Holt et al 2004 de Bianchi et al 2010) (3) Reversible relocation of phycobilisomes (Mullineaux and Emlyn-Jones 2005) or LHCII (Rochaix 2007) from PSII to PSI depending on light conditions is used to balance the distribution of excitation energy between the photosystems and is referred to as ldquostate transitionsrdquo In plants but not in cyanobacteria the process depends on reversible protein phosphorylation (Pesaresi et al 2011)


BOX 3 Overexpression of Photosynthetic

Proteins Can Enhance Photosynthesis

Boosting the efficiency of the photosynthetic light reactions by synthetic biology is a long-term project whereas optimizing the process under agriculturally relevant conditions is already feasible by much simpler means A prominent example of this is represented by the parallel overexpression of the three photoprotective proteins PsbS violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZE) in tobacco (Kromdijk et al 2016) This PsbS-VDE-ZE overexpressor line displayed an accelerated photoprotective response to natural shading events resulting in increased plant dry matter productivity under field conditions Moreover tobacco plants overexpressing PsbS alone showed less stomatal opening in response to light decreasing water loss under field conditions (Glowacka et al 2018)

Also overexpression of soluble electron transporters can enhance photosynthesis These proteins can be easily overexpressed because their actions are not dependent on strict stoichiometries For instance overexpression of both the endogenous thylakoid lumen protein plastocyanin and the heterologous red algal cytochrome c6 protein can enhance growth in plants (Chida et al 2007 Pesaresi et al 2009 Zhou et al 2018) and a similar effect is seen for cyanobacterial flavodoxin and endogenous plant

ferredoxins (Tognetti et al 2006 Tognetti et al 2007 Blanco et al 2011 Lin et al 2013 Chang et al 2017)

A third instance for enhancing photosynthesis is provided by overexpression of the tobacco Rieske protein (PETC) in Arabidopsis (Simkin et al 2017) resulting in enhanced levels of other Cyt b6f complex subunits together with enhanced plant growth and dry weight production This implies that PETC may be rate-limiting for the accumulation of the Cyt b6f complex and that the additional tobacco PETC copies can escape the limitations of the ldquofrozen metabolic staterdquo due to the high similarity with their Arabidopsis counterparts

These instances of enhancing photosynthesis by ldquosimplerdquo overexpression of (endogenous) photosynthetic proteins raise the question of why evolution has not already produced such plants in nature by positively selecting mutations in regulatory regions that increase the expression of such genes The most plausible explanation is that under natural conditions overexpression of these genes involves a trade-off This hypothetical trade-off should be related to plant fitness in terms of reproductive efficiency which might not necessarily interfere with crop yield under non-natural (agricultural) conditions


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Pesaresi P Pribil M Wunder T Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants theroles of STN7 STN8 and TAP38 Biochim Biophys Acta 1807 887-896


Pesaresi P Scharfenberg M Weigel M Granlund I Schroder WP Finazzi G Rappaport F Masiero S Furini A Jahns P Leister D (2009)Mutants overexpressors and interactors of Arabidopsis plastocyanin isoforms revised roles of plastocyanin in photosyntheticelectron flow and thylakoid redox state Mol Plant 2 236-248


Pinnola A Ghin L Gecchele E Merlin M Alboresi A Avesani L Pezzotti M Capaldi S Cazzaniga S Bassi R (2015) Heterologousexpression of moss light-harvesting complex stress-related 1 (LHCSR1) the chlorophyll a-xanthophyll pigment-protein complexcatalyzing non-photochemical quenching in Nicotiana sp J Biol Chem 290 24340-24354


Plumereacute N Nowaczyk MM (2016) Biophotoelectrochemistry of photosynthetic proteins Adv Biochem Eng Biotechnol 158 111-136Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title

Pribil M Pesaresi P Hertle A Barbato R Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation andthylakoid electron flow PLoS Biol 8 e1000288


Rasool S Mohamed R (2016) Plant cytochrome P450s nomenclature and involvement in natural product biosynthesis Protoplasma253 1197-1209


Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation FEBS Lett 581 2768-2775Pubmed Author and TitleGoogle Scholar Author Only Title Only Author and Title

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Szalkowski M Janna Olmos JD Buczyńska D Maćkowski S Kowalska D Kargul J (2017) Plasmon-induced absorption of blindchlorophylls in photosynthetic proteins assembled on silver nanowires Nanoscale 9 10475-10486


Terasaki N Yamamoto N Hiraga T Yamanoi Y Yonezawa T Nishihara H Ohmori T Sakai M Fujii M Tohri A Iwai M Inoue YYoneyama S Minakata M Enami I (2009) Plugging a molecular wire into photosystem I reconstitution of the photoelectric conversionsystem on a gold electrode Angew Chem Int Ed Engl 48 1585-1587


Terasaki N Yamamoto N Tamada K Hattori M Hiraga T Tohri A Sato I Iwai M Iwai M Taguchi S Enami I Inoue Y Yamanoi YYonezawa T Mizuno K Murata M Nishihara H Yoneyama S Minakata M Ohmori T Sakai M Fujii M (2007) Bio-photosensorCyanobacterial photosystem I coupled with transistor via molecular wire Biochim Biophys Acta 1767 653-659


Tognetti VB Palatnik JF Fillat MF Melzer M Hajirezaei MR Valle EM Carrillo N (2006) Functional replacement of ferredoxin by acyanobacterial flavodoxin in tobacco confers broad-range stress tolerance Plant Cell 18 2035-2050


Tognetti VB Zurbriggen MD Morandi EN Fillat MF Valle EM Hajirezaei MR Carrillo N (2007) Enhanced plant tolerance to ironstarvation by functional substitution of chloroplast ferredoxin with a bacterial flavodoxin Proc Natl Acad Sci U S A 104 11495-11500


Treves H Raanan H Kedem I Murik O Keren N Zer H Berkowicz SM Giordano M Norici A Shotland Y Ohad I Kaplan A (2016) Themechanisms whereby the green alga Chlorella ohadii isolated from desert soil crust exhibits unparalleled photodamage resistanceNew Phytol 210 1229-1243


Utschig LM Soltau SR Tiede DM (2015) Light-driven hydrogen production from Photosystem I-catalyst hybrids Curr Opin Chem Biol25 1-8


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Yacoby I Pochekailov S Toporik H Ghirardi ML King PW Zhang S (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxinNADP+-oxidoreductase (FNR) enzymes in vitro Proc Natl Acad Sci U S A 108 9396-9401


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Zhou XT Wang F Ma YP Jia LJ Liu N Wang HY Zhao P Xia GX Zhong NQ (2018) Ectopic expression of SsPETE2 a plastocyanin fromSuaeda salsa improves plant tolerance to oxidative stress Plant Sci 268 1-10



Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box

Outstanding Questions Box

Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

2

1 This work was funded by the Deutsche Forschungsgemeinschaft (DFG TRR 175 and GRK 26

2062) 27

28

Address correspondence to leisterlmude 29

ORCID IDs 0000-0003-1897-8421 (DL) 30

31

Oxygenic photosynthesis is imperfect and the evolutionarily conditioned patchwork nature of 32

the light reactions in plants provides ample scope for their improvement (Leister 2012 33

Blankenship and Chen 2013) In fact only around 40 of the incident solar energy is used 34

for photosynthesis Two obvious ways of reducing energy loss are to expand the spectral 35

band used for photosynthesis and to shift saturation of the process to higher light intensities 36

Indeed even minor enhancements to the efficiency or stress resistance of the light reactions 37

of photosynthesis should have a positive impact on biomass production and yield (Leister 38

2012 Blankenship and Chen 2013 Long et al 2015) 39

However modifications to the essential structure of the light reactions of plant 40

photosynthesis are currently limited by two main factors One is the high degree of 41

conservation of their structural components which limits the efficiency gains attainable by 42

conventional breeding approaches (Dann and Leister 2017) The second is that the 43

organization of these structural components into multiprotein complexes requires the 44

simultaneous tailoring of several proteins some of them encoded by different genetic systems 45

in different subcellular compartments (nucleus and chloroplasts) in land plants Therefore 46

successful modification of the light reactions of plant photosynthesis has been limited to a 47

few cases Similarly modification of the activity of auxiliary proteins involved in the 48

regulation of the light reactions to enhance plant growth and yield has only recently resulted 49


3



























4






80















2010) 95






5













112













6



























7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

3



























4






80















2010) 95






5













112













6



























7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

4






80















2010) 95






5













112













6



























7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

5













112













6



























7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

6



























7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

7


















166









8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

8



























9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

9

























10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

10



























11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

11
















262


processes 264








12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

12



























13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

13



























14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

14























al 2010) 343




15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

15






efficiency 351

352


processes 354


















16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

16















2009 Miyachi et al 2010) 385












17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

17


















evolution 413

414








18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

18












(Leister 2017) 432















19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

19



























20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

20



473




thaliana (At) 477

478

ACKNOWLEDGMENTS 479


481

482


21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

21



identity

Reference





center

86 Nixon et al

1991



80 Vermaas et

al 1996



85 Carpenter et

al 1993




78 Chiaramonte

et al 1999




ChlPC ratio

80 Viola et al

2014

psbABCDEF

D1CP47CP43D2

Cyt b559-+






82 -

99

Gimpel et al

2016


22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

22



484

485


23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

23






cytochrome c6 gene

Chida et al

2007






tobacco

Tognetti et

al 2006

Tognetti et

al 2007

Blanco et al

2011

FlvA+BFlavodiiron

protein (FLV)



A thaliana

Yamamoto et

al 2016





He et al

1999

487

488


24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

24


hybrids 490


PSI-P450 hybrids

Fusion enzyme of

rat CYP1A1 and

yeast NADPH-

P450 reductase (in

vitro)








Kim et al

1996

CP79A1 from

Sorghum bicolor

(in vitro an in

vivo)









Jensen et al

2011 Lassen

et al 2014b

Mellor et al

2016

CYP79A1

CYP71E1

UGT85B1 from

Sorghum bicolor

(in vivo)






Nielsen et al

2013

Wlodarczyk et

al 2016


25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

25

reduced ferredoxin


Proteobacterial

[NiFe]

hydrogenase

genetically fused

to cyanobacterial

PSI (in vitro)


















Ihara et al

2006a Ihara et

al 2006b

Krassen et al

2009

Green algal [FeFe]

hydrogenase

genetically fused

to ferredoxin (in

vitro)






Yacoby et al

2011



26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

26

hydrogenase wired

to cyanobacterial

PSI (in vitro)










2010 Lubner

et al 2011

491

492

493


27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












U S A 104 11495-11500 809























40



14168-14173 833




A 108 9396-9401 837






843

844







ADVANCES














Photosynthesis











































































































































































































Parsed Citations

Article File

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Advances Box


Box 1

Box 1 Figure

Box 2

Box 3

Parsed Citations

27



components



nano hybrids









reviewed in

Kargul et al

2012

Fukuzumi

2015 Utschig

et al 2015

PSI-based


bio-nano hybrids














reviewed in

Nguyen and

Bruce 2014

Gordiichuk et

al 2014

Gizzie et al

2015 Janna

Olmos et al

2017


28










495


29

FIGURE LEGENDS 496

497








I (II) 505


shown 507

508







515







30


















538








31






550











561

562

563

564


32

References 565

566



Science 358 1272-1278 569






J 65 922-935 575






96 581












Eur J Biochem 260 833-843 593






33

















13426-13430 614


Chem Biol 25 18-26 616
















34











176 1433-1451 641



Biochem 263 561-570 644








Photobiol 82 676-682 652





66 37-44 657








35


Rep 6 40 665



2872-2873 668











ACS Nano 3 4055-4061 679







Biophys Acta 1797 98-105 686








Plant Sci 3 199 694




36











4148 707









503-519 716











(Camb) 46 2557-2559 727





37









1837 1553-1566 739























236-248 762




38



24340-24354 767





Biol 8 e1000288 772




Lett 581 2768-2775 776






3619-3639 782



2189 785



134-145 788




792





1585-1587 797


39












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176 1433-1451 641



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· Google Scholar: Author Only Title Only Author and Title Shi T, Bibby TS, Jiang L, Irwin AJ,...

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Transcript of · Google Scholar: Author Only Title Only Author and Title Shi T, Bibby TS, Jiang L, Irwin AJ,...