1 Running head: Gatekeeper phosphorylated SYMRK …...6 161 region. Unlike the nfr mutants that lack...

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Running head: Gatekeeper phosphorylated SYMRK critical for RNS. 1

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Corresponding author: 4

Maitrayee DasGupta 5

Department of Biochemistry, 6

University of Calcutta, 7

35, Ballygunge Circular Road, 8

Kolkata-700019, India. 9

Phone No. +91-33-2475-4680; Fax: +91-33-2476-4419; E-mail: [email protected] 10

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Journal research area: 12

Signaling and Response 13

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Plant Physiology Preview. Published on March 9, 2016, as DOI:10.1104/pp.15.01962

Copyright 2016 by the American Society of Plant Biologists

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Gatekeeper Tyrosine phosphorylation of SYMRK is essential for synchronising the 26 epidermal and cortical responses in root nodule symbiosis. 27 28

Sudip Sahaa, Anindita Paula, Laura Herringb,1, Ayan Duttaa, Avisek Bhattacharyaa, Sandip 29

Samaddara,2, Michael B. Gosheb and Maitrayee DasGuptaa,#. 30

a Department of Biochemistry, University of Calcutta, Kolkata, India 31 b Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC, USA 32

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One-sentence summary: 38

Gatekeeper Tyr phosphorylation of SYMRK is essential for guiding the infection threads through 39

the epidermal-cortical barrier towards the nodule primordia during progress of root nodule 40

symbiosis. 41

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55 Footnotes 56

This work was funded by Grants from Govt. of India: DBT-CEIB (Centre of excellence and 57

innovation in Biotechnology), BT/01/CEIB/09/VI/10 (to M.DG), DBT-IPLS, 58

BT/PR14552/INF/22/123/2010, and fellowships to S.S (CSIR 09/028(0830)/2010-EMR-I), 59

A.P (UGC/1269), A.D. (RFSMS/F.5-19/2007BSR) and A.B. (UGC/307). This work was also 60

funded by a grant from the U.S. National Science Foundation DBI-1126244 (to M.B.G.). 61

Present address: 1 Proteomics Core, University of North Carolina, Chapel Hill, NC, USA. 62 2 New Chemistry Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, 63

Bangalore, India. 64 # Address correspondence to [email protected] 65

Author contributions: S.S., A.P., L.H., A.D., A.B. and Sa.S. performed research. Acquisition 66

of data, phenotypic (S.S.), biochemical (A.P., A.B., Sa.S.), recombinant techniques (A.D., 67

A.B.), mass spectrometry (L.H., M.B.G.). S.S., A.P., M.DG. designed, analyzed and 68

interpreted data and wrote the paper. 69

The authors declare no conflict of interest. 70

The author responsible for distribution of materials integral to the findings presented in this 71

article in accordance with the Journal policy described in the Instructions for Authors 72

(http://www.plantphysiol.org) is: Maitrayee DasGupta ([email protected]) 73

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Abstract 87

Symbiosis receptor kinase (SYMRK) is indispensable for activation of root nodule symbiosis 88

(RNS) at both epidermal and cortical levels and is functionally conserved in legumes. 89

Previously we reported SYMRK to be phosphorylated on ‘gatekeeper’ Tyr both in vitro as 90

well as in planta (Samaddar et al., 2013). Since gatekeeper phosphorylation was not 91

necessary for activity, the significance remained elusive. Herein we show that substituting 92

gatekeeper with non-phosphorylatable residues like Phe or Ala significantly affected 93

autophosphorylation on selected targets on activation segment/αEF and β3-αC loop of 94

SYMRK. In addition, the same gatekeeper mutants failed to restore proper symbiotic 95

features in a symrk null mutant where rhizobial invasion of the epidermis and nodule 96

organogenesis was unaffected but rhizobia remain restricted to the epidermis in infection 97

threads migrating parallel to the longitudinal axis of the root resulting in extensive infection 98

patches at the nodule apex. Thus gatekeeper phosphorylation is critical for synchronizing 99

epidermal/cortical responses in RNS. 100

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102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126



5

Introduction 127

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The establishment of root nodule symbiosis (RNS) involves rhizobial invasion in the root 129

epidermis and nodule organogenesis in the root cortical cells. In the epidermis recognition of 130

compatible rhizobia induces root hair curls in the host plant to entrap the rhizobia in an 131

infection pocket (Gage, 2004). In these infection pockets or chambers, rhizobia multiply to 132

form a microcolony that is believed to generate threshold levels of bacterial signal molecules 133

required for initiation and progression of infection threads (IT) through the epidermis into 134

the cortex of the root (Fournier et al., 2015). A compatible host-symbiont interaction in the 135

epidermis also leads to formation of nodule primordia in the cortex where eventually the 136

rhizobia is endocytically accommodated from the invading ITs to develop nitrogen fixing 137

symbiosomes in mature nodules. The epidermal and cortical processes are coordinated both 138

spatially and temporally in order to ensure rhizobial accommodation in the subtending 139

nodule primordia (Popp and Ott, 2011; Oldroyd, 2013; Miri et al., 2015). 140

At the molecular level these host responses are initiated with the recognition of rhizobial Nod 141

factors by two LysM receptor-like kinases NFR1 and NFR5 in Lotus japonicus and LYK3 142

and NFP in Medicago truncatula (Limpens et al., 2003; Madsen et al., 2003; Broghammer et 143

al., 2012). Recently another Nod factor induced LysM-RLK (EPR3) was shown to monitor 144

rhizobial EPS structures in Lotus, indicating a two-stage mechanism involving sequential 145

receptor-mediated recognition of Nod factor and EPS signals to ensure host symbiont 146

compatibility (Kawaharada et al., 2015). Following the perception of Nod factors, Ca2+ influx 147

at the tip of the root hair and Ca2+ spiking at the perinuclear region of the root hair are 148

induced (Oldroyd, 2013). Components that function upstream of Ca2+ spiking include 149

Symbiosis Receptor Kinase (SYMRK)/ Doesn’t Make Infections (DMI) 2 (Endre et al., 2002; 150

Stracke et al., 2002), the nuclear envelope-localized cation channels and components of the 151

nucleopore complex. A nuclear calcium- and calmodulin-dependent protein kinase 152

(CCaMK/DMI3) (Levy et al., 2004; Mitra et al., 2004) decodes the Ca2+ spiking and 153

phosphorylates a transcription factor (TF) CYCLOPS /Interacting Protein of DMI3 (IPD3) 154

(Messinese et al., 2007; Singh et al., 2014) which along with several other TFs orchestrates 155

the gene expression required for rhizobial infection and nodule organogenesis (Oldroyd, 156

2013; Suzaki et al., 2015). 157

SYMRK is a functionally conserved central component of symbiotic signaling that 158

experienced structural diversification during evolution (Markmann et al., 2008). It contains 159

an ectodomain composed of a malectin-like domain (MLD), and a leucine-rich repeat (LRR) 160



6

region. Unlike the nfr mutants that lack most cellular and physiological responses including 161

induction of Ca2+ influx and Ca2+-spiking in response to rhizobia, the root hairs of symrk 162

mutants respond with Ca2+ influx but not with Ca2+-spiking, and do not develop ITs, 163

indicating SYMRK to be positioned downstream of the NFRs (Miwa et al., 2006). Recently, 164

LjSYMRK is shown to interact with NFR5 through its ectodomain suggesting a role of 165

SYMRK in initiating symbiotic signaling in concert with the NFRs (Antolin-Llovera et al., 166

2014). Unlike the NFRs, specificity of recognition of bacterial partners in RNS is 167

independent of the source of SYMRK (Gherbi et al., 2008; Markmann et al., 2008; Saha et 168

al., 2014). SYMRK is indispensable at both epidermal and cortical levels and is important for 169

coupling the epidermal /cortical events in RNS guided by a GDPC motif in its ectodomain 170

(Kosuta et al., 2011; Antolin-Llovera et al., 2014). The kinase activity of SYMRK is also 171

vital for its role in symbiosis as several SYMRK mutants have missense or nonsense 172

mutations in the catalytic domain (Yoshida and Parniske, 2005). Several interactors are 173

known for SYMRK that indicated this RLK to be nodal to various downstream cellular 174

responses associated with inception of RNS (Antolin-Llovera et al., 2014). 175

The majority of plant Receptor Like Kinases (RLKs) including SYMRK are distinguished by 176

having tyrosine in the ‘gatekeeper’ position adjacent to the hinge region of their kinase 177

domains (Shiu and Bleecker, 2001). This residue helps dictate the size of a hydrophobic 178

pocket that forms in the DFG-out conformation of protein kinases (Hari et al., 2013; Sohl et 179

al., 2015). Though importance of the gatekeeper residue is primarily because it is the 180

architect of this deep catalytic cleft, several lines of evidence now indicate that protein 181

kinases have adopted mechanisms of regulation mediated by their gatekeeper residues 182

(Emrick et al., 2006; Chen et al., 2007; Azam et al., 2008). Most importantly, oncogenic 183

activation of several receptor tyrosine kinases (RTKs) has been shown to be due to changes 184

in the gatekeeper (Azam et al., 2008). The importance of the gatekeeper Tyr residue is also 185

emerging in the well characterised RLKs like brassinosteroid-insensitive 1 (BRI1), and lysin 186

motif domain-containing receptor like kinase-3 (LYK3) or receptor-like cytoplasmic kinase 187

like Botrytis-induced kinase 1 (BIK1) where structure–mimic substitutions of the gatekeeper 188

affects either kinase activity or biological activity or both (Oh et al., 2009; Oh et al., 2009; 189

Klaus-Heisen et al., 2011; Lin et al., 2014). RLKs are also shown to adopt an active 190

conformation by forming a hydrogen bonded triad between the invariant Lys-Glu salt-bridge 191

and the gatekeeper Tyr (Bojar et al., 2014). But considering the contrasting effects of the 192

gatekeeper substitution in RLKs, the involvement of the free hydroxyl group of gatekeeper 193



7

tyrosine in an H-bonding network cannot be considered as a quintessential signature of the 194

activated state for all RLKs. 195

In an earlier report, we demonstrated SYMRK from Arachis hypogaea (AhSYMRK) to 196

predominantly autophosphorylate on gatekeeper tyrosine (Y670) both in vitro and in planta 197

(Samaddar et al., 2013). Apart from SYMRK, autophosphorylation of gatekeeper Tyr is only 198

evidenced in BRI1 (Oh et al., 2009). Autophosphorylation on gatekeeper tyrosine was not a 199

prerequisite for AhSYMRK to be catalytically active and hence the significance of gatekeeper 200

phosphorylation remained elusive (Samaddar et al., 2013; Paul et al., 2014). Here we report 201

the biochemical and biological importance of gatekeeper phosphorylation by demonstrating 202

its role in autoactivation of AhSYMRK and progress of RNS. AhSYMRK with non-203

phosphorylatable residues in the gatekeeper position significantly increased or 204

suppressed autophosphorylation on specific sites in the activation segment/αEF and β3-αC 205

loop indicating the identity of SYMRK’s gatekeeper residue to be important for determining 206

the state of autoactivation of this RLK. This change of autophosphorylation profile with non-207

phosphorylatable gatekeepers led to complete loss of coordination between rhizobial invasion 208

in the epidermis and nodule organogenesis in the cortex in RNS restricting the rhizobia in the 209

epidermal-cortical interface. 210

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8

Results 214

Gatekeeper Tyr defines a distinct autoactivation state of AhSYMRK. 215

Gatekeeper Tyr (Y670) was identified previously as a potential site of autophosphorylation in 216

AhSYMRK by mutagenesis and sequence-specific antibodies both in vitro and in planta 217

(Samaddar et al., 2013). Here we first verified Y670 phosphorylation by mass spectrometry 218

to reconfirm phosphorylation on this residue (Fig. 1A, Supplemental Table S1). To probe into 219

the importance of gatekeeper phosphorylation, we substituted Y670 with another hydroxyl-220

containing amino acid residue like Thr (Y670T), or non-phosphorylatable residues like Phe 221

or Ala (Y670F, Y670A) or a phosphomimic like Glu (Y670E) and monitored the catalytic 222

consequences of the modifications in recombinant AhSYMRK. The level of intrinsic 223

autophosphorylation was higher in wild type (WT) and Y670T but in vitro 224

autophosphorylation activity was at least 4-5 fold higher in Y670F and Y670A (Fig. 1B). The 225

phosphomimic substitution Y670E that permanently introduces a negative charge in the 226

catalytic groove (Paul et al., 2014), drastically reduced both intrinsic and in vitro 227

autophosphorylation activities of AhSYMRK but did not render the kinase catalytically dead 228

like K625E. While pThr was detectable in all the mutants including Y670E, pTyr was only 229

detectable in WT and Y670T indicating that a phosphorylatable residue in the gatekeeper 230

position was necessary for the kinase to autophosphorylate on Tyr residues and become dual 231

specific. Gatekeeper phosphorylation specific antibody α-pY670 (665–674) recognised 232

AhSYMRK but did not react with its gatekeeper mutants like Y670F, Y670A, Y670E or the 233

catalytically dead mutant K625E attesting to its specificity. But it was intriguing to note a 234

feeble but consistent immunoblot crossreactivity of α-pY670 (665–674) with Y670T which 235

we believe, is due to phosphorylation on gatekeeper Thr (pT670) as suggested by MS 236

analysis (Fig.1B, Supplemental Table S2). 237

We then examined how the nature of the gatekeeper affected the relative levels of 238

phosphorylation in each of the identified phosphorylation sites in AhSYMRK using LFQMS 239

(Ahmed et al., 2014). Only phosphopeptides that were detected in all experimental replicates 240

of the WT and Y670T/F/A mutants were subjected to quantitation (Supplemental Table S2 & 241

S3). Additionally, we quantified Y670E phosphorylation status for these sites only, which 242

was either absent or barely detectable. The pY containing peptides encompassing the 243

activation segment/αEF helix were only detectable in WT and Y670T and have been included 244

in the analysis. Representative data plotted against the functional domains of protein kinases 245

highlighted the sharp contrast in the autophosphorylation profile between AhSYMRK with 246



9

phosphorylatable (Y670/Y670T) and non-phosphorylatable gatekeepers (Y670F/A) (Fig. 247

1C). While autophosphorylation on most sites was relatively unaffected by gatekeeper 248

substitution, in several sites autophosphorylation was selectively suppressed only in Y670F 249

and Y670A. Those sites are located in the β3-αC loop (S631), activation segment (S754, 250



10

T763), αEF helix (T773) and the αF-αG loop (S810). Besides, doubly phosphorylated 251

peptides encompassing the P+1 loop and/or the αEF helix containing pY766/pY771/pY772 252

were conspicuously absent in Y670F/A mutants indicating this region to have a contrasting 253

pY signature with non-phosphorylatable gatekeepers (Supplemental Table S3). As opposed to 254

these sites, where autophosphorylation was compromised in Y670F/A, autophosphorylation 255

in S757 residue in the activation loop showed a sharp increase in Y670F (~48 fold) and 256

Y670A (~37 fold). Interestingly, Y670E polypeptide which was barely active showed ~17 257

fold increase in autophosphorylation in S757 residue. Thus two different autoactivation states 258

with two distinct sets of autophosphorylation targets, is defined in AhSYMRK with 259

phosphorylatable or non-phosphorylatable gatekeepers. 260

261

Non-phosphorylatable gatekeepers in AhSYMRK arrested infection threads in the 262

epidermis. 263

Cross-species complementation tests showed that SYMRKs from eurosids, including 264

nodulating and non-nodulating lineages, can restore symbiosis in symrk null mutants (Gherbi 265

et al., 2008; Markmann et al., 2008). Earlier we have demonstrated complementation of 266

TR25, a symrk null mutant of Medicago truncatula by AhSYMRK (Saha et al., 2014). The 267

same experimental conditions were used to determine the significance of gatekeeper Y670 268

phosphorylation in AhSYMRK in vivo where we transformed TR25 with the native 269

AhSYMRK and its gatekeeper mutants and monitored their ability to restore symbiotic 270

features. Transformed roots inoculated with S.meliloti-mRFP were monitored for their 271

colonization at 2 weeks after infection (WAI). Upon infection with S. meliloti, in both 272

TR25/AhSYMRK and TR25/AhSYMRK-Y670T roots, microcolonies were observed within 273

tightly curled root hairs and IT formation could be restored (Fig. 2A-B). In 274

TR25/AhSYMRK, the ITs were always a continuous tubular structure (Fig. 2A), whereas in 275

TR25/AhSYMRK-Y670T, ITs sometimes developed sac like structures (Fig. 2C) or they 276

revealed misdirected progression at the epidermal–cortical interface (Fig. 2D) but in most 277

cases the ITs were found to progress normally (Fig. 2E). In contrast, in TR25/AhSYMRK-278

Y670F/A, the root hair curls were enlarged with diffused agglomerations (Fig. 2, F and J). In 279

both cases the ITs contained extensive inflated sac like structures and this feature was more 280

prominent in TR25/AhSYMRK-Y670F roots (Fig. 2, F-H and J-L). However the most 281

important distinguishing feature was the arrest of IT progression at the epidermal cortical 282



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interface or subepidermal cortex (Fig. 2, F-H, J and L). The misdirected ITs were noted to 283

migrate parallel to the longitudinal axis of the root instead of ramifying and reaching the 284

dividing cortical cells (Fig. 2, H-I and L-M). ITs were also found to be blocked within the 285

root hair shaft but that was rare (Fig. 2K). Also, as compared to TR25/AhSYMRK and 286

TR25/AhSYMRK-Y670T/A, the number of ITs was at least ~3 times higher in only 287

TR25/AhSYMRK-Y670F (Fig. 2, N-O; Supplemental Fig.S1), which could be due to the 288



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plants’ attempt to compensate for the defect in IT propagation (more prominent in Y670F) by 289

initiation of more ITs as noted before in Lotus (Murray et al., 2007). In contrast to these 290

observations, none of the epidermal features of rhizobial invasion were restored in 291

TR25/AhSYMRK-Y670E roots which is consistent with the drastic loss of catalytic activity 292

in Y670E (Fig. 2P). In summary, with non-phosphorylatable gatekeepers in AhSYMRK the 293

epidermal/cortical barrier was insurmountable by ITs. This is a direct demonstration of the 294

physiological consequences of the differential autophosphorylation profile of AhSYMRK 295

with a phosphorylatable and a non-phosphorylatable gatekeeper. 296

297

Non-phosphorylatable gatekeepers in AhSYMRK uncoupled epidermal and cortical 298

events in RNS 299

Our next objective was to monitor the gatekeeper substitution mutants of SYMRK for their 300

ability to restore nodule organogenesis and rhizobial colonisation in the cortex. By 6 WAI, 301

nodules were visible with all the mutants and their number was reproducibly higher (~2 to 3 302

times) with all the gatekeeper substituted mutants (Supplemental Fig. S2; Supplemental Table 303

S4). In TR25/AhSYMRK and TR25/AhSYMRK-Y670T cortical ramification of ITs was 304

restored, and the symbionts were released in the central infected zone of the developed 305

nodule (n=40) (Fig. 3, A-B and J-K). However some infected nodules in TR25/AhSYMRK-306

Y670T were distinct by having a small infection patch/pocket at the apex, a feature almost 307

never observed in nodules developed in TR25/AhSYMRK roots (Fig. 3B). In at least 20% 308

TR25/AhSYMRK-Y670T nodules the misdirected ITs remained restricted in apical 309

pockets leaving the nodules without a central infected zone (Fig. 3A inset, Fig. 3, C and 310

L). As opposed to TR25/AhSYMRK-Y670T, in TR25/AhSYMRK-Y670F/A nodules there 311

was absolutely no ramification of ITs in the nodule interior (n=60) (Fig. 3, D-I and L). As a 312

result, the nodules were always empty and the symbionts were strictly restricted to extensive 313

infection patches on the apex. Moreover, the nodules developed in TR25/AhSYMRK-314

Y670F/A showed improper vasculature (Fig. 3, E and H), which is in accordance with the 315

adverse effect on nodule organogenesis by epidermal arrest of rhizobial invasion as 316

demonstrated in both Medicago and Lotus (Yano et al., 2009; Guan et al., 2013). This effect 317

was not ephemeral as the symbionts were detained in the infection pockets without any signs 318

of IT propagation to the cortex even 8WAI and the nodule development never progressed 319

further. Additionally TR25/AhSYMRK-(573–883)-Y670F could profusely generate 320

spontaneous nodules and these nodules developed with proper vasculature (Supplemental 321



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Fig. S3), as demonstrated earlier in TR25/AhSYMRK-(573–883) (Saha et al., 2014; Saha and 322

DasGupta, 2015). This confirms that the restricted autoactivation of AhSYMRK-Y670F can 323

generate all the signals necessary for proper nodule organogenesis and the improper 324

vasculature noted in TR25/AhSYMRK-Y670F/A were indeed due to inhibitory signals 325

generated by epidermal arrest of symbionts. Also the increase of nodule number with 326

gatekeeper mutants is likely to be a downstream effect of the absence of mature nodules 327

where absence of suppression may have led to a recurrent initiation of new foci of cell 328

divisions as proposed previously in Medicago (Kuppusamy et al., 2004). These results again 329



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show a correlation between the RNS features and the differential autophosphorylation profile 330

of SYMRK with a phosphorylatable and a non-phosphorylatable gatekeeper. 331

332

AhSYMRK with non-phosphorylatable gatekeepers fails to upregulate expression of 333

genes required for epidermal-cortical coordination in RNS 334

335

Several factors have been evidenced in the literature to have a role in epidermal–cortical 336

coordination in RNS (Popp and Ott, 2011). For example, TFs like CYCLOPS (Singh et al., 337

2014) and NIN (Soyano et al., 2013; Vernié et al., 2015), a nodule-specific remorin 338

MtSYMREM1 (Lefebvre et al., 2010), the plasma membrane-resident ankyrin protein 339

Vapyrin (Murray et al., 2011), the U-box containing E3 ubiquitin-ligase LIN (Kuppusamy et 340

al., 2004) and the non-coding RNA ENOD40 (Crespi et al., 1994). In CYCLOPS mutant of 341

Medicago (TE7), several nodules remain small (primordia) with ITs arrested at the nodule 342

apex similar to what has been observed in presence of AhSYMRK with the non-343

phosphorylatable gatekeepers (Fig. 3, D-I) (Benaben et al., 1995). LjCYCLOPS 344

transactivates the NIN gene, a bifunctional membrane bound transcriptional coactivator 345

(Singh et al., 2014). In both Medicago and Lotus, NIN is essential for IT initiation in the 346

epidermis and nodule organogenesis in the cortex (Yoro et al., 2014; Fournier et al., 2015). 347

MtSYMREM1 interacts with SYMRK and NFRs to mediate their assembly in membrane 348

rafts and its downregulation leads to IT arrest in epidermal cells (Lefebvre et al., 2010). Both 349

Vapyrin and LIN mutants in Medicago show impaired growth of ITs that are blocked in the 350

epidermis (Kuppusamy et al., 2004; Murray et al., 2011). Finally, ENOD40, an early Nod-351

factor-induced gene has a role in both infection and nodule primordia initiation as 352

demonstrated in Medicago (Crespi et al., 1994). Overall all these genes appear to have a role 353

in proper invasion of ITs into the dividing cells of the nodule primordia in the cortex. 354

We compared the expression of these genes in TR25/AhSYMRK-Y670T/F/A/E roots at 355

6WAI. In TR25/AhSYMRK-Y670E, expression of the above symbiotic genes was barely 356

detectable which is in accordance with absence of any symbiotic response of these roots in 357

presence of rhizobia (Fig. 4). Expression of LIN and MtENOD40 was relatively unaffected in 358

TR25/AhSYMRK-Y670T/F/A indicating their expression to be upstream or parallel to the 359

pathway that leads to overcoming of the epidermal/cortical barrier. Vapyrin is the only factor 360

that was almost equally affected in TR25/AhSYMRK-Y670T/F/A. Therefore Vapyrin does 361

not appear to be connected with the sharp contrast between TR25/AhSYMRK-Y670F/A and 362



15

TR25/AhSYMRK-Y670T with respect to loss of cortical colonisation. On the other hand, 363

misdirected IT progression in the epidermis is a common feature that distinguishes 364

TR25/AhSYMRK-Y670T/F/A from its WT counterpart, and this feature may be associated 365

with low expression of Vapyrin. In TR25/AhSYMRK-Y670F/A, expression was significantly 366

lower for MtNIN (~6-9 fold), MtSYMREM1 (~4 fold) and IPD3 (~2 fold) as compared to 367

TR25/AhSYMRK-Y670T, indicating these genes to be directly involved in synchronising the 368

epidermal and cortical events. This attests the role of these factors in coupling the epidermal 369

and cortical events as suggested previously and designates them to function downstream to 370

SYMRK for the same. 371

372

Discussion: 373

374

Here we demonstrate gatekeeper Tyr autophosphorylation as a hallmark of a distinct 375

autoactivated state of AhSYMRK that generates vital phospho-cues for progress in symbiosis. 376

AhSYMRK with non-phosphorylatable gatekeepers like Phe and Ala conspicuously 377

upregulate or suppress autophosphorylation in specific sites (Fig. 1C), notably in the 378

activation segment/αEF and β3-αC loop, and in addition failed to support a coordinated 379

epidermal and cortical response during establishment of RNS (Fig. 2 and Fig.3). 380

The role of SYMRK in coordinating the epidermal and cortical responses was first noted 381

in symrk-3 snf-1 double mutants of Lotus where ITs were occasionally noted to be 382

misdirected and swollen and unable to reach the nodule primordia (Madsen et al., 2010). 383

Another example is symrk-14 in Lotus with a P386L substitution in the extracellular GDPC 384

motif of SYMRK that prevents its ectodomain shedding (Kosuta et al., 2011; Antolin-Llovera 385

et al., 2014). Substitution in the GDPC motif does not affect IT formation or nodule 386



16

organogenesis but restricts ITs to the epidermis. Our investigations reveal SYMRK with non-387

phosphorylatable gatekeepers to have a similar phenotypic output in Medicago (Fig. 2 and 388

Fig. 3). Additionally we show that the state of autoactivation differs with a non-389

phosphorylatable gatekeeper where autophosphorylation on selective targets on activation 390

segment/αEF and β3-αC loop are significantly affected or abolished (Fig. 1). The 391

phenotypic overlap of symrk14 mutant of Lotus and our observations on TR25/AhSYMRK-392

Y670F/A in Medicago suggest SYMRK to have distinct autoactivation states based on the 393

nature of its extracellular domains. SYMRK activity with its intact ectodomain triggers 394

cortical cell division and the epidermal infection thread formation. Then ectodomain 395

shedding switches SYMRK to another autoactivation state that enables gatekeeper 396

phosphorylation and full-scale phosphorylation of activation segment/αEF and β3-αC loop of 397

the receptor. Together, ectodomain shedding and gatekeeper phosphorylation could be a 398

coupled switch that maintains a synchrony between epidermal and cortical events for 399

precisely timing the crossing over of the epidermal-cortical barrier for endocytic 400

accommodation of symbionts in the primordia. It remains to be seen whether and how the 401

extracellular GDPC motif allosterically connects with the gatekeeper residue in the kinase 402

domain to deliver the outputs required for a successful coordination of epidermal and cortical 403

symbiotic features. 404

Several other mutants have indicated the epidermal-cortical interface to be an important 405

checkpoint during the progress of RNS (Popp and Ott, 2011; Rival et al., 2012; Hayashi et 406

al., 2014). Premature arrest of ITs in the epidermis and restriction of symbionts in infection 407

patches in the nodule apex was observed in ccamk-14 (Liao et al., 2012), nap-1, pir-1(Yokota 408

et al., 2009), and nena (Groth et al., 2010) of Lotus. In Medicago, similar phenotypes were 409

observed in lyk3 (Smit et al., 2007), TE7 (Benaben et al., 1995), api (Teillet et al., 2008) and 410

lin-1 mutants (Kuppusamy et al., 2004). The spreading of misdirected ITs in the epidermis as 411

noted predominantly with gatekeeper substituted SYMRKs in Medicago (TR25/AhSYMRK-412

Y670F/A, Fig 2), was previously noted in the vag-1 and suner1-1 mutants of Lotus (Suzaki 413

et al., 2014; Yoon et al., 2014). The significance of CCaMK/DMI3 in epidermal-cortical 414

crosstalk is illustrated in both Lotus and Medicago (Rival et al., 2012; Hayashi et al., 2014). 415

Epidermal expression of CCaMK supported IT progression in the epidermis but its cortical 416

expression was essential for allowing the ITs to cross the epidermal/cortical barrier and 417

triggering cortical cell division for nodule organogenesis. The Ca2+-responsive domains of 418

CCaMK were indispensable for epidermal infections but dispensable for nodule 419



17

organogenesis and cortical infection processes (Gleason et al., 2006; Shimoda et al., 2012; 420

Hayashi et al., 2014). NIN is also a central player in coordinating epidermal/cortical 421

responses in both Lotus and Medicago (Soyano et al., 2013; Vernié et al., 2015). 422

Overexpressing NIN in either the epidermis or the cortex auto-activates cortical cell division 423

but unlike epidermal NIN, cortical NIN expression can promote the formation of nodule like-424

structures independent of Cre1 (Vernié et al., 2015). Since SYMRK functions at the upstream 425

end of the SYM pathway, the phenotypic overlap of TR25/AhSYMRK-Y670F/A with the 426

above mutants indicate SYMRK with its phospho-cues to be important for guiding the proper 427

progression of the ITs. Additionally, expression of MtNIN, MtSYMREM1 and IPD3 were 428

significantly affected in TR25/AhSYMRK-Y670F/A as compared to TR25/AhSYMRK-429

Y670T (Fig. 4), indicating these factors to have important roles in enabling the ITs to 430

surmount the epidermal-cortical barrier. All these genes are therefore involved in the network 431

that guide and guard the epidermal–cortical barrier. 432

433 The sites where autophosphorylation was affected with a non-phosphorylatable gatekeeper 434

(Y670F/A), are all conserved in SYMRKs from other species (Fig.1C, Supplemental Fig. S4) 435

indicating the strategic importance of gatekeeper phosphorylation and suggesting the 436

underlying mechanism of full-scale autoactivation of SYMRKs to be conserved. Even in 437

other RLKs the same sites or regions are known to be autophosphorylated suggesting the 438

autoactivating principles to be conserved beyond SYMRK (Supplemental Fig. S4). The 439

residue S757, where autophosphorylation sharply increased in absence of a phosphorylatable 440

gatekeeper (Fig. 1C), is also highly conserved in SYMRKs suggesting its importance in 441

symbiotic signaling. Phosphorylation on the invariant Thr (T763 in AhSYMRK/ T760 in 442

LjSYMRK) in the activation loop was shown earlier to be important for SYMRK activity 443

(Yoshida and Parniske, 2005; Samaddar et al., 2013). Since T763 autophosphorylation is 444

drastically downregulated in Y670F/A, it could be that the autoactivation with a non-445

phosphorylatable gatekeeper, is actually independent of T763 phosphorylation in the 446

activation segment. Such activation loop phosphorylation independent activation is 447

demonstrated in certain RTKs and RLKs (Dardick et al., 2012; Plaza-Menacho et al., 2014). 448

It remains to be understood as to how gatekeeper Tyr phosphorylation in the hinge region is 449

involved with autophosphorylation in the distal and dynamic elements like the activation 450

segment/αEF helix and β3-αC loop (Fig. 1C). However, the importance of hinge motions for 451

kinase activation and allosteric communication between the activation loop and hinge has 452

been suggested for some animal kinases (Hari et al., 2013; Sours et al., 2014). In the majority 453



18

of RTKs, an inhibitory network of hydrogen bonds involving the gatekeeper residue is 454

disengaged upon activation loop phosphorylation to activate the kinase (Chen et al., 2007). In 455

ERK2, flexibility of the activation loop and its accessibility to autophosphorylation could be 456

controlled over long distances by the nature of the gatekeeper through an intramolecular 457

pathway of connectivity through interacting side chains (Emrick et al., 2006). Similar 458

mechanism has been hypothesized for Arabidopsis MPK6, where gatekeeper Tyr 459

substitutions lead to constitutive activity and independence from upstream MAPK activation 460

(Berriri et al., 2012). In tune to these examples, our results indicate SYMRK to adopt such 461

long-range allosteric interaction networks whereby it transmits the identity of the gatekeeper 462

to distant locations within the core kinase domain for full-scale autoactivation of the kinase. 463

Consistent with this proposition, we have already demonstrated that conformations of 464

SYMRK distinctly differ based on whether it had Tyr or Phe as the gatekeeper (Paul et al., 465

2014). We hypothesize the phosphorylated or non-phosphorylated state of the gatekeeper Tyr 466

to determine the autophosphorylation trajectory in SYMRK as described for the FGFR family 467

of animal kinases and thereby define distinct autoactivation states (Furdui et al., 2006). 468

Futher experimentation is required for determining the state of phosphorylation of SYMRK 469

with the initiation and progress of symbiosis to understand how well the in vitro 470

phosphorylation studies reflect the trajectory of its autophosphorylation in planta. Such 471

understanding would clarify the role of differential phosphoclusters of SYMRK in serving as 472

platform for ‘docking’ of effector proteins to transmit downstream signaling. 473

In conclusion, a phosphorylatable gatekeeper residue determines a distinct autoactivation 474

state of SYMRK that differentially autophosphorylates and generates phospho-cues for 475

coupling the epidermal and cortical responses of RNS. Since a gatekeeper tyrosine is 476

common in RLKs, a conserved mechanism of activation associated with gatekeeper 477

phosphorylation could be of common occurrence in RLKs. 478

479

480

Materials and Methods 481

Plant and Rhizobial strains 482

Medicago TR25 seeds, Agrobacterium rhizogenes strain MSU440 and pBHR-mRFP-483

S.meliloti 2011 strain were used. 484

485

Constructs 486



19

pET28a-AhSYMRK-kd(573-883)(Samaddar et al., 2013) and its point mutations generated 487

with the QuikChangeSite-Directed mutagenesis kit (Stratagene) were used to express the 488

His6-polypeptides in E. coli strain BL21 (DE3). The full length AhSYMRK and its gatekeeper 489

mutants AhSYMRK-Y670T/F/A/E were recombined into pK7FWG2 using LR-Clonase (Life 490

Technologies) thereby generating 35S::AhSYMRK-GFP and its corresponding tyrosine 491

residue mutants e.g. 35S::AhSYMRK-Y670T/F/A/E-GFP. (for details, see Supplemental 492

Methods S1). 493

494

Kinase Assay, Phosphoamino acid analysis, Immunoprecipitation. Kinase 495

autophosphorylation assays, immunoblotting, immunoprecipitation and phosphostaining 496

were performed as described previously (DasGupta, 1994; Samaddar et al., 2013; Paul et al., 497

2014). 498

LFQMS. The recombinant proteins were subjected to the kinase reaction with unlabeled 499

ATP until phosphorylation was complete, followed by sample preparation and LC/MS/MS 500

analysis as described in Supplemental Methods S1. 501

Phenotypic analysis. Generation of composite M. truncatula plants and scoring nodulation, 502

phenotypic analysis and confocal microscopy were performed as described previously (Saha 503

et al., 2014). 504

For detailed description of methods pertaining to construct generation, qRT-PCR, primers 505

used see Supplemental Methods S1. 506

507

Acknowledgments 508

We thank Giles Oldroyd & Christian Rogers for TR25 seeds, Ton Bisseling & Erik Limpens 509

for S. meliloti harboring pBHR-mRFP, Douglas R. Cook for Agrobacterium strain MSU440. 510

511

512

513

514

515

516

517



20

FIGURE LEGENDS: 518

Figure 1.Gatekeeper Y670 defines a distinct autoactivation state for AhSYMRK. 519

A) AhSYMRK is autophosphorylated on gatekeeper Y670. Product ion spectrum of a doubly 520 charged peptide ion at m/z 1103.5044 with the phosphosite assigned to be Y670 in the 521 sequence 664-DQQILVYPFMSNGSLQNR-681. B) Autophosphorylation of gatekeeper 522 mutants (From topmost panel). Intrinsic phosphorylation detected by ProQ Diamond staining, 523 in vitro AhSYMRK autophosphorylation activity detected by [32P]-γ-ATP (autorad), 524 phosphorylation was detected by anti-phosphothreonine (α-pThr), anti-phosphotyrosine (α-525 pTyr) and modification specific (α-pY670: 665-674) antibodies, protein abundance visualized 526 by Coomassie Brilliant Blue staining (CBB). The catalytically inactive K625E mutant is used 527 as reference. C) Gatekeeper mutations significantly affect the autophosphorylation profile of 528 AhSYMRK. A MS-based quantitation of specific phosphopeptides from recombinant 529 AhSYMRK gatekeeper Y670 mutant proteins relative to WT (wild type, defined as 1). 530 Phosphosites have been arranged N to C-terminus and clustered under the typical secondary 531 structural features of the kinase domain (Taylor and Kornev, 2011). Gatekeeper Y670/T670, 532 S674, S677 (Supplemental Table S2 & S3) have not been included due to different ionization 533 efficiencies of these phosphopeptides. Phosphosites significantly affected due to Y670 534 substitutions have been marked with *. Activation loop (AL, red), P+1 loop (blue), αEF helix 535 (orange), P+1 loop/ αEF (brown). 536

Figure 2. Effect of the gatekeeper mutation on progression of ITs. 537 TR25 roots were transformed with 35S::AhSYMRK-GFP and gatekeeper mutants 538 35S::AhSYMRK-Y670T/F/A/E-GFP. Progress of IT was observed 2 WAI with S. meliloti-539 mRFP and are shown as merged images of bright field and mRFP fluorescence. 540 IT progress in TR25/AhSYMRK (A), TR25/ AhSYMRK-Y670T (B-E), TR25/ AhSYMRK-541 Y670F (F-I), TR25/ AhSYMRK-Y670A (J-M). No S.meliloti colonization was observed in 542 roots of TR25/AhSYMRK-Y670E (P). S.meliloti colonization in AhSYMRK-Y670F (N) and 543 AhSYMRK-Y670A (O) roots. Scale bar: 200μm (N-O), 100μm (A, F, I-J and P), 50 μm (D-544 E, G and M), 20μm (H and K-L) and 10μm (B-C). 545 546 Figure 3. Effect of the gatekeeper mutation on nodule development and symbiont 547 colonization. 548 TR25 roots were transformed with 35S::AhSYMRK-GFP and gatekeeper mutants 549 35S::AhSYMRK-Y670T/F/A-GFP. Nodule development and S.meliloti colonization was 550 observed 6 WAI. 551 Nodule developed in TR25/AhSYMRK-Y670T (A-C), TR25/ AhSYMRK-Y670F (D-F), 552 TR25/ AhSYMRK-Y670A (G-I) and TR25/ AhSYMRK (J-K). Nodulated roots (A,D, G and 553 J) with insets showing enlarged view of nodules. Rhizobial accumulation at the nodule apex 554 indicated by arrow. Longitudinal sections revealing S.meliloti colonized in nodule interior (B, 555 K). Infection pocket (B) and extensive infection patches in nodule apex (C, E and H). 556 Magnified view of infection pocket showing sub-epidermal rhizobial colonisation (F and I). 557 Vascular bundles indicated by arrowhead. 558



21

(L) Percentage of S. meliloti colonization in the nodule interior or apex in TR25 plants 559 transformed with indicated gatekeeper mutants. 560 Images shown as merged images of bright-field and red (S. meliloti expressing mRFP) (A-C, 561 D-E, G-H and J-K), bright-field (bottom left) and merged (bottom right) images of GFP and 562 mRFP fluorescence (inset of A, D, G and J) or merged images of red and blue (Calcofluor, 563 cell wall stain) fluorescence (F, I). 564 Scale bar: 2mm (A, D, G and J), 500µm (inset of A, D, G and J), 100µm (B-C, E, H and K) 565 and 5 µm (F, I). 566 567 Figure 4.Effect of gatekeeper substitution on the expression of IPD3, NIN, SYMREM1, 568 Vapyrin, LIN and ENOD40. 569 Expression of the mentioned genes in TR25/AhSYMRK-Y670T/F/A/E at 6WAI were 570 measured relative to those in TR25/AhSYMRK roots. The expression level in 571 TR25/AhSYMRK was set to 1. In all cases, MtACTIN2 was used as the reference gene. 572 Histograms represent means of 3 biological replicates ± SEM. Asterisks above bars indicate 573 significant differences (P<0.05). 574

575

SUPPLEMENTAL DATA 576

Supplemental Figure S1. ITs in TR25/AhSYMRK and TR25/AhSYMRK-Y670T/F/A roots 577

2 WAI with S. meliloti. 578

Supplemental Figure S2. Nodules developed in TR25/AhSYMRK and TR25/AhSYMRK-579

Y670T/F/A roots 6 WAI with S. meliloti. 580

Supplemental Figure S3. Spontaneous nodule formation by overexpression of AhSYMRK-581

(573–883) Y670F. 582

Supplemental Figure S4. Conservation of phosphorylation sites in SYMRKs and other 583

RLKs. 584

Supplemental Table S1. Phosphorylation on gatekeeper Y670 of wild type AhSYMRK-kd 585

identified by LC/MS/MS. 586

Supplemental Table S2. List of phosphorylation sites detected for AhSYMRK-kd and its 587

gatekeeper mutants, identified by LC-MS/MS. 588

Supplemental Table S3. List of phosphopeptides of AhSYMRK-kd and its gatekeeper 589

mutants quantitated by LFQMS (represented in Fig. 1C) 590



22

Supplemental Table S4. Restoration of RNS in TR25 by overexpression of AhSYMRK and 591

AhSYMRK-Y670T/F/A/E 592

Supplemental Methods S1. Methods in detail. 593

594 595 596 597 598

599



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http://scholar.google.com/scholar?as_q=A molecular brake in the kinase hinge region regulates the activity of receptor tyrosine kinases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28enod%5BTitle%5D%29 AND 40%5BVolume%5D AND Crespi M%2C Jurkevitch E%2C Poiret M%2C d%27Aubenton%2DCarafa Y%2C Petrovics G%2C Kondorosi E%2C Kondorosi A%5BAuthor%5D&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Dardick C, Schwessinger B, Ronald P (2012) Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr Opin Plant Biol 15: 358-366

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http://scholar.google.com/scholar?as_q=Characterization of a calcium-dependent protein kinase from Arachis hypogea (groundnut) seeds&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=DasGupta&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proceedings of the National Academy of Sciences%5BTitle%5D%29 AND 103%5BVolume%5D AND 18101%5BPagination%5D AND Emrick MA%2C Lee T%2C Starkey PJ%2C Mumby MC%2C Resing KA%2C Ahn NG%5BAuthor%5D&dopt=abstract


CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development.Nature 417: 962-966


Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG (2015) Remodeling of theInfection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host LegumeRoot Hair. Plant Physiol 167: 1233-1242


Furdui CM, Lew ED, Schlessinger J, Anderson KS (2006) Autophosphorylation of FGFR1 Kinase Is Mediated by a Sequential andPrecisely Ordered Reaction. Molecular cell 21: 711-717


Gage DJ (2004) Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes.Microbiology and Molecular Biology Reviews 68: 280-300


Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M, BoguszD (2008) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, andFrankiabacteria. Proc Natl Acad Sci U S A 105: 4928-4932


Gleason C, Chaudhuri S, Yang T, Munoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by acalcium-activated kinase lacking autoinhibition. Nature 441: 1149-1152


Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M (2010) NENA, aLotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia butdispensable for cortical endosymbiotic development. Plant Cell 22: 2509-2526


Guan D, Stacey N, Liu C, Wen J, Mysore KS, Torres-Jerez I, Vernie T, Tadege M, Zhou C, Wang ZY, Udvardi MK, Oldroyd GE,Murray JD (2013) Rhizobial infection is associated with the development of peripheral vasculature in nodules of Medicagotruncatula. Plant Physiol 162: 107-115


Hari SB, Merritt EA, Maly DJ (2013) Sequence determinants of a specific inactive protein kinase conformation. Chemistry & biology20: 806-815


Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, Hayashi M (2014) Rhizobial infection does not require corticalexpression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking. The Plant Journal 77: 146-159


Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszynski A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, VintherM, Andersen SU, Krusell L, Thirup S, Jensen KJ, Ronson CW, Blaise M, Radutoiu S, Stougaard J (2015) Receptor-mediatedexopolysaccharide perception controls bacterial infection. Nature 523: 308-312


Klaus-Heisen D, Nurisso A, Pietraszewska-Bogiel A, Mbengue M, Camut S, Timmers T, Pichereaux C, Rossignol M, Gadella TW,Imberty A (2011) Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. Journal of Biological Chemistry 286: 11202-11210



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http://search.crossref.org/?page=1&rows=2&q=Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966

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http://scholar.google.com/scholar?as_q=A receptor kinase gene regulating symbiotic nodule development&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A receptor kinase gene regulating symbiotic nodule development&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Endre&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 167%5BVolume%5D AND 1233%5BPagination%5D AND Fournier J%2C Teillet A%2C Chabaud M%2C Ivanov S%2C Genre A%2C Limpens E%2C de Carvalho%2DNiebel F%2C Barker DG%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG (2015) Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair. Plant Physiol 167: 1233-1242

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http://scholar.google.com/scholar?as_q=Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fournier&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Molecular cell%5BTitle%5D%29 AND 21%5BVolume%5D AND 711%5BPagination%5D AND Furdui CM%2C Lew ED%2C Schlessinger J%2C Anderson KS%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Furdui CM, Lew ED, Schlessinger J, Anderson KS (2006) Autophosphorylation of FGFR1 Kinase Is Mediated by a Sequential and Precisely Ordered Reaction. Molecular cell 21: 711-717

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http://search.crossref.org/?page=1&rows=2&q=Gage DJ (2004) Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes. Microbiology and Molecular Biology Reviews 68: 280-300

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci U S A%5BTitle%5D%29 AND 105%5BVolume%5D AND 4928%5BPagination%5D AND Gherbi H%2C Markmann K%2C Svistoonoff S%2C Estevan J%2C Autran D%2C Giczey G%2C Auguy F%2C Peret B%2C Laplaze L%2C Franche C%2C Parniske M%2C Bogusz D%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gleason&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28NENA%5BTitle%5D%29 AND 13%5BVolume%5D AND is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development%2E Plant Cell 22%3A 2509%5BPagination%5D AND Groth M%2C Takeda N%2C Perry J%2C Uchida H%2C Draxl S%2C Brachmann A%2C Sato S%2C Tabata S%2C Kawaguchi M%2C Wang TL%2C Parniske M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22: 2509-2526

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http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Groth&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Chemistry %26 biology%5BTitle%5D%29 AND 20%5BVolume%5D AND 806%5BPagination%5D AND Hari SB%2C Merritt EA%2C Maly DJ%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28The Plant Journal%5BTitle%5D%29 AND 77%5BVolume%5D AND 146%5BPagination%5D AND Hayashi T%2C Shimoda Y%2C Sato S%2C Tabata S%2C Imaizumi%2DAnraku H%2C Hayashi M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Hayashi T, Shimoda Y, Sato S, Tabata S, Imaizumi-Anraku H, Hayashi M (2014) Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking. The Plant Journal 77: 146-159

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hayashi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hayashi&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature%5BTitle%5D%29 AND 523%5BVolume%5D AND 308%5BPagination%5D AND Kawaharada Y%2C Kelly S%2C Nielsen MW%2C Hjuler CT%2C Gysel K%2C Muszynski A%2C Carlson RW%2C Thygesen MB%2C Sandal N%2C Asmussen MH%2C Vinther M%2C Andersen SU%2C Krusell L%2C Thirup S%2C Jensen KJ%2C Ronson CW%2C Blaise M%2C Radutoiu S%2C Stougaard J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszynski A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH, Vinther M, Andersen SU, Krusell L, Thirup S, Jensen KJ, Ronson CW, Blaise M, Radutoiu S, Stougaard J (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523: 308-312

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http://scholar.google.com/scholar?as_q=Receptor-mediated exopolysaccharide perception controls bacterial infection&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Receptor-mediated exopolysaccharide perception controls bacterial infection&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kawaharada&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Journal of Biological Chemistry%5BTitle%5D%29 AND 286%5BVolume%5D AND 11202%5BPagination%5D AND Klaus%2DHeisen D%2C Nurisso A%2C Pietraszewska%2DBogiel A%2C Mbengue M%2C Camut S%2C Timmers T%2C Pichereaux C%2C Rossignol M%2C Gadella TW%2C Imberty A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Klaus-Heisen D, Nurisso A, Pietraszewska-Bogiel A, Mbengue M, Camut S, Timmers T, Pichereaux C, Rossignol M, Gadella TW, Imberty A (2011) Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. Journal of Biological Chemistry 286: 11202-11210

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http://scholar.google.com/scholar?as_q=Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Klaus-Heisen&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1


Kosuta S, Held M, Hossain MS, Morieri G, Macgillivary A, Johansen C, Antolin-Llovera M, Parniske M, Oldroyd GE, Downie AJ,Karas B, Szczyglowski K (2011) Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J 67:929-940


Kuppusamy KT, Endre G, Prabhu R, Penmetsa RV, Veereshlingam H, Cook DR, Dickstein R, VandenBosch KA (2004) LIN, aMedicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol 136: 3682-3691


Lefebvre B, Timmers T, Mbengue M, Moreau S, Herve C, Toth K, Bittencourt-Silvestre J, Klaus D, Deslandes L, Godiard L, MurrayJD, Udvardi MK, Raffaele S, Mongrand S, Cullimore J, Gamas P, Niebel A, Ott T (2010) A remorin protein interacts with symbioticreceptors and regulates bacterial infection. Proc Natl Acad Sci U S A 107: 2343-2348


Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C,Debelle F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science303: 1361-1364


Liao J, Singh S, Hossain MS, Andersen SU, Ross L, Bonetta D, Zhou Y, Sato S, Tabata S, Stougaard J (2012) Negative regulation ofCCaMK is essential for symbiotic infection. The Plant Journal 72: 572-584


Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nodfactor-induced infection. Science 302: 630-633


Lin W, Li B, Lu D, Chen S, Zhu N, He P, Shan L (2014) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediatesArabidopsis innate immunity. Proceedings of the National Academy of Sciences 111: 3632-3637


Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J(2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640


Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) Themolecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 10


Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution ofintracellular root symbioses with bacteria. PLoS Biol 6: e68


Messinese E, Mun JH, Yeun LH, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ane JM (2007) Anovel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula.Mol Plant Microbe Interact 20: 912-921


Miri M, Janakirama P, Held M, Ross L, Szczyglowski K (2015) Into the Root: How Cytokinin Controls Rhizobial Infection. Trends inplant science


Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent proteinkinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 101:4701-4705

Pubmed: Author and Title www.plantphysiol.orgon March 19, 2020 - Published by Downloaded from Copyright © 2016 American Society of Plant Biologists. All rights reserved.

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http://search.crossref.org/?page=1&rows=2&q=Kuppusamy KT, Endre G, Prabhu R, Penmetsa RV, Veereshlingam H, Cook DR, Dickstein R, VandenBosch KA (2004) LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol 136: 3682-3691

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kuppusamy&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://search.crossref.org/?page=1&rows=2&q=Lefebvre B, Timmers T, Mbengue M, Moreau S, Herve C, Toth K, Bittencourt-Silvestre J, Klaus D, Deslandes L, Godiard L, Murray JD, Udvardi MK, Raffaele S, Mongrand S, Cullimore J, Gamas P, Niebel A, Ott T (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci U S A 107: 2343-2348

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http://search.crossref.org/?page=1&rows=2&q=Lin W, Li B, Lu D, Chen S, Zhu N, He P, Shan L (2014) Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proceedings of the National Academy of Sciences 111: 3632-3637

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http://search.crossref.org/?page=1&rows=2&q=Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640

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http://search.crossref.org/?page=1&rows=2&q=Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 10

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http://search.crossref.org/?page=1&rows=2&q=Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6: e68

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http://search.crossref.org/?page=1&rows=2&q=Messinese E, Mun JH, Yeun LH, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ane JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921

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http://scholar.google.com/scholar?as_q=A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Messinese&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Into the Root%3A How Cytokinin Controls Rhizobial Infection%2E%5BTitle%5D%29 AND Miri M%2C Janakirama P%2C Held M%2C Ross L%2C Szczyglowski K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Miri M, Janakirama P, Held M, Ross L, Szczyglowski K (2015) Into the Root: How Cytokinin Controls Rhizobial Infection. Trends in plant science

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Miri&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Into the Root: How Cytokinin Controls Rhizobial Infection.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Into the Root: How Cytokinin Controls Rhizobial Infection.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Miri&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci U S A%5BTitle%5D%29 AND 101%5BVolume%5D AND 4701%5BPagination%5D AND Mitra RM%2C Gleason CA%2C Edwards A%2C Hadfield J%2C Downie JA%2C Oldroyd GE%2C Long SR%5BAuthor%5D&dopt=abstract


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Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat RevMicrobiol 11: 252-263


Paul A, Samaddar S, Bhattacharya A, Banerjee A, Das A, Chakrabarti S, DasGupta M (2014) Gatekeeper tyrosine phosphorylation isautoinhibitory for Symbiosis Receptor Kinase. FEBS Lett 588: 2881-2889


Plaza-Menacho I, Barnouin K, Goodman K, Martínez-Torres RJ, Borg A, Murray-Rust J, Mouilleron S, Knowles P, McDonald NQ(2014) Oncogenic RET kinase domain mutations perturb the autophosphorylation trajectory by enhancing substrate presentationin trans. Molecular cell 53: 738-751


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http://search.crossref.org/?page=1&rows=2&q=Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 101: 4701-4705

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Mitra&hl=en&c2coff=1

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40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J60: 168-180


Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, Radutoiu S, Held M, Hossain MS, Szczyglowski K, Morieri G, Oldroyd GE,Downie JA, Nielsen MW, Rusek AM, Sato S, Tabata S, James EK, Oyaizu H, Sandal N, Stougaard J (2009) Rearrangement of actincytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21: 267-284


Yoon HJ, Hossain MS, Held M, Hou H, Kehl M, Tromas A, Sato S, Tabata S, Andersen SU, Stougaard J, Ross L, Szczyglowski K(2014) Lotus japonicus SUNERGOS1 encodes a predicted subunit A of a DNA topoisomerase VI that is required for noduledifferentiation and accommodation of rhizobial infection. Plant J 78: 811-821


Yoro E, Suzaki T, Toyokura K, Miyazawa H, Fukaki H, Kawaguchi M (2014) A positive regulator of nodule organogenesis, NODULEINCEPTION, acts as a negative regulator of rhizobial infection in Lotus japonicus. Plant physiology 165: 747-758


Yoshida S, Parniske M (2005) Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J BiolChem 280: 9203-9209



http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 60%5BVolume%5D AND 168%5BPagination%5D AND Yano K%2C Shibata S%2C Chen WL%2C Sato S%2C Kaneko T%2C Jurkiewicz A%2C Sandal N%2C Banba M%2C Imaizumi%2DAnraku H%2C Kojima T%2C Ohtomo R%2C Szczyglowski K%2C Stougaard J%2C Tabata S%2C Hayashi M%2C Kouchi H%2C Umehara Y%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yano&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Lotus japonicus SUNERGOS1 encodes a predicted subunit A of a DNA topoisomerase VI that is required for nodule differentiation and accommodation of rhizobial infection&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Lotus japonicus SUNERGOS1 encodes a predicted subunit A of a DNA topoisomerase VI that is required for nodule differentiation and accommodation of rhizobial infection&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoon&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant physiology%5BTitle%5D%29 AND 165%5BVolume%5D AND 747%5BPagination%5D AND Yoro E%2C Suzaki T%2C Toyokura K%2C Miyazawa H%2C Fukaki H%2C Kawaguchi M%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=A positive regulator of nodule organogenesis, NODULE INCEPTION, acts as a negative regulator of rhizobial infection in Lotus japonicus&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A positive regulator of nodule organogenesis, NODULE INCEPTION, acts as a negative regulator of rhizobial infection in Lotus japonicus&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoro&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 280%5BVolume%5D AND 9203%5BPagination%5D AND Yoshida S%2C Parniske M%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshida&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1


1 Running head: Gatekeeper phosphorylated SYMRK …...6 161 region. Unlike the nfr mutants that lack...

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Transcript of 1 Running head: Gatekeeper phosphorylated SYMRK …...6 161 region. Unlike the nfr mutants that lack...