Winslow R. Briggs John L . Spudich

Handbook of Photosensory Receptors

Preface XVII

List of Authors XIX

1

Microbial Rhodopsins: Phylogenetic and Functional Diversity 1John L . Spudich and Kwang-Hwan Jung

1,1

Introduction 11 .2

Archaeal Rhodopsins 2

1 .3

Clues to Newfound Microbial Rhodopsin Function from Primar ySequence Comparison to Archaeal Rhodopsins 7

1 .4

Bacterial Rhodopsins 1 0

1 .4 .1

Green-absorbing Proteorhodopsin ("GPR") from Monterey Bay Surfac ePlankton 10

1 .4.2

Blue-absorbing Proteorhodopsin ("BPR") from Hawaiian Deep SeaPlankton 1 2

1 .4.3

Anabaena Sensory Rhodopsin 131 .4 .4

Other Bacterial Rhodopsins 1 5

1 .5

Eukaryotic Microbial Rhodopsins 1 61 .5 .1

Fungal Rhodopsins 1 61 .5 .2

Algal Rhodopsins 1 7

1 .6

Spectral Tuning 1 81 .7

A Unified Mechanism for Molecular Function? 1 91 .8

Opsin-related Proteins without the Retinal-binding Site 2 0

1 .9

Perspective 2 0

References 2 1

2

Sensory Rhodopsin Signaling in Green Flagellate Algae 25

Oleg A. Sineshchekov and John L . Spudic h2 .1

Introduction 25

2 .1 .1

Retinylidene Receptors 25

2 .L2 .

Physiology of Algal Phototaxis and the Photophobic Response 262 .1 .3

Photoelectrical Currents and their Relationship to SwimmingBehavior 27

2 .2

The Photosensory Receptors : CSRA and CSRB 3 0

2 .2 .1

Genomics, Sequence, and Predicted Structure 31

2 .2 .2

Cellular Content and Roles in Phototaxis and Photophobic Behavior 3 2

2 .2 .3

Molecular Mechanism of Action 3 6

2 .3

Other Algae 3 9

2 .4

Conclusion and Future Perspectives 4 0Acknowledgements 4 1

References 4 1

3

Visual Pigments as Photoreceptors 43

Masato Kumauchi and Thomas Ebre y

3A

Introduction 43

3 .1 .1

General Considerations 43

3 .1 .2

Photoreceptors and Pigments 4 9

3 .1 .3

Non-photoreceptor or "Non-rod", "Non-cone" Retinal Pigments 5 0

3 .1 .4

Retinal Photoisomerases 51

3 .2

The Unphotolyzed State of Vertebrate Visual Pigments 51

3 .2 .1

Structure of Visual Pigments : the Chromophore 5 1

3 .2 .2

Overall Topology of the Pigment 5 2

3 .2 .3

Cytoplasmic Domain 54

3 .2 .4

The Hydrophobic Core of Rhodopsin and the Retinal Binding Pocket 55

3 .2 .5

The Extracellular Domain of Rhodopsin 5 6

3 .2 .6

Structure of Other Visual Pigments 56

3 .2 .7

Protonation State of Some of the Carboxylic Acids of Rhodopsin 5 7

3 .2 .8

Internal Waters in Visual Pigments 5 7

3 .2 .9

Is Rhodopsin a Dimer in vivo? 58

3 .2 .10

Functional Properties of the Unphotolyzed State of a "Good" Visua lPigment 58

3 .2 .11

Quantum Efficiency of Visual Pigment Photochemistry 62

3 .2 .12

Dark Noise Originating from the Photoreceptor Pigment 6 3

3 .3

Activation of Vertebrate Visual Pigments 65

3 .3 .1

Introduction 65

3 .3 .2

The Primary Event, Photoisomerization 65

3 .3 .3

The Meta I Meta II Transition 6 6

3 .3 .4

Molecular Changes upon the Formation of Meta I and Meta II 6 7

3 .3 .5

Internal Water Molecules 67

3 .3 .6

Required Steps for Rhodopsin Activation 67

3 .3 .7

The Transmembrane Signaling Pathway 6 8

3 .4

The Unphotolyzed State of Invertebrate Visual Pigments 69

3 .4 .1

Introduction 6 9

3 .4 .2

Wavelength Regulation of Invertebrate Pigments 703 .5

Mechanism of Activation of Invertebrate Visual Pigments 71

3 .5 .1

The Initial Photochemical Events 71

3 .5 .2

Formation of Acid Metarhodopsin 71

3 .5 .3

Required Steps for Photolyzed Octopus Rhodopsin to Activate it sG-protein 71

3 .5 .4

Purification of the Active Form of an Invertebrate Visual Pigment 72

Acknowledgements 72

References 72

4

Structural and Functional Aspects of the Mammalian Rod-Cell Photoreceptor

Rhodopsin 77

Najmoutin G . Abdulaev and Kevin D. Ridge

4.1

Introduction 77

4.2

Rhodopsin and Mammalian Visual Phototransduction 79

4.2 .1

Signal Amplification by Light-activated Rhodopsin 79

4.2 .2

Inactivation of Light-activated Rhodopsin 7 9

4.3

Properties of Rhodopsin 80

4 .3 .1

Isolation of Rhodopsin 80

4,3 .2

Biochemical and Physicochemical Properties of Rhodopsin 8 1

4.3 .3

Post-translational Modifications in Rhodopsin 82

4.3 .4

Membrane Topology of Rhodopsin and Functional Domains 82

4 .4

Chromophore Binding Pocket and Photolysis of Rhodopsin 8 5

4 .5

Structure of Rhodopsin 8 6

4 .5 .1

Crystal Structure of Rhodopsin 8 6

4 .5 .2

Atomic Force Microscopy of Rhodopsin in the Disk Membrane 88

4 .6

Activation Mechanism of Rhodopsin 8 8

4.7

Conclusions 8 9

Acknowledgements 90

References 90

5

A Novel Light Sensing Pathway in the Eye : Conserved Features of Inner Retinal

Photoreception in Rodents, Man and Teleost Fish 93

Mark W. Hankins and Russell G. Foste r

Summary 93

5 .1

Introduction 94

5 .1 .1

A Novel Photoreceptor within the Eye 94

5 .1 .2

Biological Clocks and their Regulation by Light 95

5 .2

Non-rod, Non-cone Photoreception in Rodents 96

5 .2 .1

An Irradiance Detection Pathway in the Eye 9 6

5 .2 .2

The Discovery of a Novel Ocular Photopigment in Mice (OP°ß°) 97

5 .2 .3

Melanopsin and Non-rod, Non-cone Photoreception 9 9

5 .2 .4

A Functional Syncitium of Directly Light-sensitive Ganglion Cells 101

5 .3

Non-rod, Non-cone Photoreception in Humans 104

5 .3 .1

Introduction 104

5 .3 .2

Novel Photoreceptors Regulate Melatonin 105

5 .3 .3

Novel Photoreceptors Regulate the Primary Visual Cone Pathway 10 S5 .4

Non-rod, Non-cone Photoreception in Teleost Fish 10 7

5 .4 .1

Background 107

5 .4.2

Vertebrate Ancient (VA) Opsin and Inner Retinal Photoreception i n

Teleost Fish 1085 .4 .3

A Novel Light Response from VA-opsin- and Melanopsin-expressing

Horizontal Cells 108

5 .4 .4

Action Spectra for the HC-RSD Light Response Identify a Nove l

Photopigment 10 9

5 .4 .5

The Possible Function of HC-RSD Neurones 11 1

5 .5

Opsins can be Photosensors or Photoisomerases 11 2

5 .6

Placing Candidate Genes and Photopigments into Context 113

5 .7

Conclusions 114

References 115

6

The Phytochromes 12 1

Shih-Long Tu and J. Clark Lagarias

6 .1

Introduction 121

6 .1 .1

Photomorphogenesis and Phytochromes 12 1

6 .1 .2

The Central Dogma of Phytochrome Action 122

6 .2

Molecular Properties of Eukaryotic and Prokaryotic Phytochromes 123

6 .2 .1

Molecular Properties of Plant Phytochromes 123

6 .2 .2

Molecular Properties of Cyanobacterial Phytochromes 125

6 .3

Photochemical and Nonphotochemical Conversions ofPhytochrome 127

6 .3 .1

The Phytochrome Chromophore 12 7

6 .3 .2

Phytochrome Photointerconversions 129

6 .3 .3

Dark Reversion 13 2

6 .4

Phytochrome Biosynthesis and Turnover 13 3

6 .4 .1

Phytobilin Biosynthesis in Plants and Cyanobacteria 13 36 .4 .2

Apophytochrome Biosynthesis and Holophytochrome Assembly 13 86 .4 .3

Phytochrome Turnover 14 1

6.5

Molecular Mechanism of Phytochrome Signaling: FuturePerspective 14 2

6.5 .1

Regulation of Protein-Protein Interactions by Phosphorylation 142

6 .5 .2

Regulation of Tetrapyrrole Metabolism 143

Acknowledgements 145

References 145

7

Phytochrome Signaling 151

Enamul Huq and Peter H. Quai l7 .1

Introduction 151

7.2

Photosensory and Biological Functions of Individual Phytochromes 152

7 .3

phy Domains Involved in Signaling 154

7.4

phy Signaling Components 155

7 .4.1

Second Messenger Hypothesis 155

7.4 .2

Genetically Identified Signaling Components 15 6

7.4.3

phy-Interacting Factors 159

7 .4 .4

Early phy-Responsive Genes 162

7 .5

Biochemical Mechanism of Signal Transfer 164

7 .6

phy Signaling and Circadian Rhythms 16 57 .7

Future Prospects 16 6

Acknowledgements 16 7

References 16 8

8

Phytochromes in Microorganisms 171

Richard D . Vierstra and Baruch Karniol8 .1

Introduction 171

8 .2

Higher Plant Phys 172

8 .3

The Discovery of Microbial Phys 1748 .4

Phylogenetic Analysis of the Phy Superfamily 1768 .4 .1

Cyanobacterial Phy (Cph) Family 179

8 .4 .2

Bacteriophytochrome (BphP) Family 17 9

8.4.3

Fungal Phy (Fph) Family 184

8.4.4

Phy-like Sequences 18 5

8.5

Downstream Signal-Transduction Cascades 18 6

8.6

Physiological Roles of Microbial Phys 1888.6 .1

Regulation of Phototaxis 188

8.6 .2

Enhancement of Photosynthetic Potential 18 9

8.6 .3

Photocontrol of Pigmentation 191

8.7

Evolution of the Phy Superfamily 19 1

8.8

Perspectives 19 2

Acknowledgements 19 3

References 19 4

9

Light-activated Intracellular Movement of Phytochrome 19 7

Eberhard Schäfer and Ferenc Nagy9 .1

Introduction 197

9 .2

The Classical Methods 197

9 .2 .1

Spectroscopic Methods 197

9 .2 .2

Cell Biological Methods 198

9 .2 .3

Immunocytochemical Methods 198

9 .3

Novel Methods 199

9 .4

Intracellular Localization of PHYB in Dark and Light 200

9 .5

Intracellular Localization of PHYA in Dark and Light 20 1

9 .6

Intracellular Localization of PHYC, PHYD and PHYEin Dark and Light 202

9 .7

Intracellular Localization of Intragenic Mutant Phytochromes 203

9 .7.1

Hyposensitive, Loss-of-function Mutants 203

9.7.2

Hypersensitive Mutants 20 4

9.8

Protein Composition of Nuclear Speckles Associated with phyB 204

9.9

The Function of Phytochromes Localized in Nuclei and Cytosol 207

9 .10

Concluding Remarks 20 8

References 20 9

10

Plant Cryptochromes : Their Genes, Biochemistry, and Physiologica l

Roles 21 1

Alfred Batschaue rSummary 21 1

10 .1

Cryptochrome Genes and Evolution 21 2

10.1 .1

The Discovery of Cryptochromes 21 210.1 .2

Distribution of Cryptochromes and their Evolution 21 3

10.2

Cryptochrome Domains, Cofactors and Similarities with Photolyase 214

10 .3

Biological Function of Plant Cryptochromes 21 9

10.3 .1

Control of Growth 22 0

10 .3 .2

Role of Cryptochromes in Circadian Clock Entrainment andPhotoperiodism 22 3

10 .3 .3

Regulation of Gene Expression 228

10 .4

Localization of Cryptochromes 232

10 .5

Biochemical Properties of Cryptochromes 23 4

10 .5 .1

Protein Stability 23 4

10 .5 .2

Phosphorylation 23 6

10 .5 .3

DNA Binding 23 9

10 .5 .4

Electron Transfer 240

10 .6

Summary 24 1

Acknowledgements 24 1

References 242

11

Plant Cryptochromes and Signaling 24 7

Anthony R. Cashmore11 .1

Introduction 247

11 .2

Photolyases 24 7

11 .3

Cryptochrome Photochemistry 248

11 .4

Cryptochrome Action Spectra 24 9

11 .5

Cryptochromes and Blue Light-dependent Inhibitionof Cell Expansion 25 0

11 .6

Signaling Mutants 251

11 .7

Signaling by Cryptochrome CNT and CCT Domains 25 1

11 .8

Arabidopsis Cryptochromes Exist as Dimers 252

11 .9

COP1, a Signaling Partner of Arabidopsis Cryptochromes 253

11 .10

Cryptochrome and Phosphorylation 253

11 .11

Cryptochrome and Gene Expression 254

11 .12

Concluding Thoughts 25 5

References 257

12

Animal Cryptochromes 25 9

Russell N . Van Gelder and Aziz Sanca r12 .1

Introduction 25 9

12 .2

Discovery of Animal Cryptochromes 26 0

12 .3

Structure-Function Considerations 26 0

12 .4

Drosophila melanogaster Cryptochrome 26 312 .5

Mammalian Cryptochromes, Circadian Rhythmicity, and Nonvisua lPhotoreception 26 6

12 .6

Cryptochromes of Other Animals 27312 .7 .

Conclusions and Future Directions 274

References 274

13

Blue Light Sensing and Signaling by the Phototropins 277

John M. Christie and Winslow R . Briggs13 .1

Introduction 277

13 .2

Phototropin Structure and Function 278

13 .2 .1

Discovery of Phototropin 278

13 .2 .2

Photl : a Blue Light-activated Receptor Kinase 279

13 .2 .3

Phot2: a Second Phototropic Receptor 280

13 .2 .4

Phototropins : Photoreceptors for Movement and More 28 1

13 .2 .5

Overview of Phototropin Activation 28 3

13 .3

LOV Domain Structure and Function 28 4

13,3 .1

Light Sensing by the LOV Domains 284

13 .3 .2

LOV is all Around 28 6

13 .3 .3

Are Two LOVs Better than One? 28 8

13 .4

From Light Sensing to Receptor Activation 29 0

13 .4 .1

LOV Connection 290

13 .4 .2

Phototropin Autophosphorylation 291

13 .4 .3

Phototropin Recovery 29 2

13 .5

Phototropin Signalling 294

13 .5 .1

Beyond Photoreceptor Activation 294

13 .5 .2

Phototropism 294

13 .5 .3

Stomatal Opening 29 6

13 .5 .4

Chloroplast Movement 297

13 .5 .5

Rapid Inhibition of Hypocotyl Growth by Blue Light 29 9

13 .6

Future Prospects 30 0

References 300

14

LOV-domain Photochemistry 305

Trevor E . Swartz and Roberto A . Bogomoln i

14.1

Introduction 305

14 .2

The Chromoprotein Ground State Structure and Spectroscopy 30 6

14.2 .1

Structure of the Chromoprotein and its Chromophore Environment 306

14 .2 .2

FMN Electrostatic Environment within the Protein 30 7

14 .3

Photochemistry 312

14 .3 .1

Photocycle Kinetics and Structure of its Intermediates 31 2

14 .3 .2

Photo-backreaction 31 6

14 .4

Reaction Mechanisms 31 6

14 .4 .1

Adduct Formation 31 6

14 .4 .2

Adduct Decay 319

14 .4

Future Perspectives 32 0

References 32 1

15

LOV-Domain Structure, Dynamics, and Diversity 323

Sean Crosson

15 .1

Overview 323

15 .2

LOV Domain Architecture and Chromophore Environment 324

15 .3

Photoexcited-State Structural Dynamics of LOV Domains 326

15 .4

Comparative Structural Analysis of LOV Domains 328

15 .5

LOV-Domain Diversity 33 0

Acknowledgements 334

References 33 5

16

The ZEITLUPE Family of Putative Photoreceptors 33 7

Thomas F . Schult z16 .1

Introduction 33 7

16 .2

Circadian Clocks 33 7

16 .3

SCF Ubiquitin Ligases 34 0

16 .4

Photoperception 341

16 .5

The ZTL Gene Family 342

16 .5 .1

ZTL 343

16 .5 .2

FKF1 34416 .5 .3

LKP2 345

16 .6

Summary 346

References 346

17

Photoreceptor Gene Families in Lower Plants 349

Noriyuki Suetsugu and Masamitsu Wad a17 .1

Introduction 34 9

17 .2

Cryptochromes 352

17 .2 .1

Adiantum capillus-veneris 352

17 .2 .2

Physcomitrella patens 35 4

17 .2.3

Chlamydomonas reinhardtii 35617 .3

Phototropins 357

17 .3 .1

Adiantum capillus-veneris 35 7

17 .3 .2

Physcomitrella patens 358

17 .3 .3

Chlamydomonas reinhardtii 36 117 .4

Phytochromes in Lower Plants 36 3

17 .4 .1

Conventional Phytochromes 363

17 .4 .2

Phytochrome 3 in Polypodiaceous Ferns 364

17 .5

Concluding Remarks 36 6

Acknowledgements 366

References 36 7

18

Neurospora Photoreceptors 37 1

Jay C. Dunlap and Jennifer J. Loros18 .1

Introduction and Overview 371

18 .2

The Photobiology of Fungi in General and Neurospora in Particular 371

18 .2 .1

Photoresponses are Widespread 371

18 .2 .2

Photobiology of Neurospora 37218 .3

Light Perception - the Nature of the Primary Blue Ligh tPhotoreceptor 375

18 .3 .1

Flavins as Chromophores 375

18 .3 .2

Genetic Dissection of the Light Response 375

18 .3 .3

New Insights into Photoreceptors from Genomics 376

18 .4

How do the Known Photoreceptors Work? 37 7

18 .4.1

WC-1 and WC-2 contain PAS Domains and Act as a Complex 37 7

18 .4.2

WC-1 is the Blue Light Photoreceptor 378

18 .4.3

Post-activation Regulation of WC-1 38 2

18 .4.4

A Non-photobiological Role for WC-1 and the WCC 383

18 .5

VIVID, a Second Photoreceptor that Modulates Light Responses 384

18 .5 .1

Types of Photoresponse Modulation 38 4

18 .5 .2

Proof of VVD Photoreceptor Function 38 6

18 .6

Complexities in Light Regulatory Pathways 38 7

18 .7

Summary and Conclusion 38 7

References 388

19

Photoactive Yellow Protein, the Xanthopsin 39 1

Michael A . van der Horst, Johnny Hendriks, Jocelyne Vreede,Sergei Yeremenko, Wins Crielaard and Klaas J . Hellingwerf

19 .1

Introduction 39 1

19 .1 .1

Discovery of the Photoactive Yellow Protein 39 1

19 .1 .2

A Family of Photoactive Yellow Proteins : the Xanthopsins 392

19 .1 .3

Differentiation of Function among the Xanthopsins 39 2

19 .1 .4

PYP: The Prototype PAS Domain 393

19 .2

Structure 394

19 .2 .1

Primary, Secondary, and Tertiary Structure 39 4

19 .2 .2

Solution Structure vs . Crystal Structure 395

19 .2 .3

The Xanthopsins Compared 39 6

19 .3

Photoactivity of the Xanthopsins 39 7

19 .3 .1

The Basic Photocycle 39 7

19 .3 .2

Photocycle Nomenclature 39 9

19 .3 .3

Experimental Observation : Context Dependence 39 9

19 .3 .4

Mutants and Hybrids 400

19 .3 .5

Photo-activation in the Different Xanthopsins Compared 400

19 .4

The Photocycle of Photoactive Yellow Protein 40 1

19 .4.1

Initial Events 40 1

19 .4 .2

Signaling State Formation and Ground State Recovery 403

19 .4 .3

Structural Relaxation of pR 404

19 .4 .4

Protonation Change upon pB' Formation 404

19 .4 .5

Structural Change upon pB Formation 405

19 .4 .6

Recovery of the Ground State 40 7

19 .5

Spectral Tuning of Photoactive Yellow Protein 408

19 .5 .1

Ground State Tuning 40 9

19 .5 .2

Spectral Tuning in Photocycle Intermediates 41 0

19 .6

Summary and Future Perspective 41 1

References 412

20

Hypericin-like Photoreceptors 41 7

Pill-Soon SongAbstract 41 7

20.1

Introduction 41 7

20.2

Ciliate Photoreceptors 420

20.2 .1

Action Spectra 42 0

20.2 .2

The Chromophores 421

20.2 .3

Proteins and Localization 423

20.3

Photochemistry 42 5

20 .3 .1

Photosensitization? 42 5

20 .3 .2

Primary Photoprocesses 425

20 .4

Photosensory Signal Transduction 42 7

20 .4 .1

Signal Generation 428

20 .4 .2

Signal Amplification 42 9

20 .4 .3

Signal Transduction 42 9

20 .5

Concluding Remarks 43 0

Acknowledgements 43 0

References 431

21

The Antirepressor AppA uses the Novel Flavin-Binding BLUF Domain as a

Blue-Light-Absorbing Photoreceptor to Control Photosystem Synthesis 433

Shinji Masuda and Carl E. Baue r21 .1

Overview 43 3

21 .2

Oxygen and Light Intensity Control Synthesis of the Bacteria l

Photosystem 434

21 .2 .1

PpsR is a DNA-binding Transcription Factor that Coordinates bot h

Oxygen and Light Regulation 43 5

21 .2 .2

Discovery of AppA, a Redox Responding, Blue Light Absorbing,

Antirepressor of PpsR 43 5

21 .3

Mechanism of the BLUF Photocycle in AppA 438

21 .4

Other BLUF Containing Proteins 441

21 .5

Concluding Remarks 443

Acknowledgement 44 4References 444

22

Discovery and Characterization of Photoactivated Adenylyl Cyclase (PAC) ,a Novel Blue-Light Receptor Flavoprotein, from Euglena gracilis 44 7Masakatsu Watanabe and Mineo Isek i

22 .1

Introduction 44 7

22 .2

Action Spectroscopy 44 722 .3

PAC Discovery and its Identification as the Blue-light Receptor fo rPhotoavoidance 449

22 .4

PAC Involvement in Phototaxis 45 622 .5

PAC Origin 45 7

22 .6

Future Prospects 45 7

Acknowledgements 45 9

References 460