Shining Light on the Function of NPH3/RPT2-like Proteins ... · 33 stomatal opening and...

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Update on Blue Light Signaling 1

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Shining Light on the Function of NPH3/RPT2-like Proteins in Phototropin Signalling 3 4 John M. Christie1*, Noriyuki Suetsugu1,2, Stuart Sullivan1 and Masamitsu Wada3 5 6 1Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life 7 Sciences, Bower Building, University of Glasgow, Glasgow G12 8QQ, UK 8 2Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan 9 3Graduate School of Science and Engineering, Tokyo Metropolitan University, Tokyo 192-0397, 10 Japan 11 12 Corresponding Author: John M. Christie 13 Tel: +44 141 330 239; Email [email protected] 14 15 This work was supported by funding from the UK Biotechnology and Biological Sciences 16 Research Council (BB/M002128/1 to J.M.C) and the Grant-in-Aid for Scientific Research Grant 17 from the Japan Society for the Promotion of Science (15KK0254 to N.S.). 18 19 Summary: NRL proteins coordinate different aspects of phototropin signaling through signaling 20 processes that are conserved in land plants and algae 21 22

Plant Physiology Preview. Published on July 18, 2017, as DOI:10.1104/pp.17.00835

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Introduction 24 Plasma membrane receptors play fundamental roles in shaping plant growth and development. 25 A large proportion of these are autophosphorylating serine/threonine kinases (De Smet et al., 26 2009). Some function as dual-specificity kinases, autophosphorylating additionally on tyrosine 27 residues, one of which being the extensively studied steroid receptor BRASSINOSTEROID-28 INSENSITIVE 1 (BRI1) (Oh et al., 2009). Light regulation of plant growth is also mediated by 29 plasma membrane-bound serine/threonine kinases known as the phototropins (Fankhauser and 30 Christie, 2015). Seed plants contain two phototropins (phot1 and phot2) that have important 31 roles in regulating leaf positioning and expansion, chloroplast photorelocation movement, 32 stomatal opening and phototropism, all of which serve to optimize photosynthetic efficiency 33 (Christie et al., 2015). Phots are members of the AGCVIII kinase family (Rademacher and 34 Offringa, 2012), but are distinct from transmembrane receptor kinases such as BRI1, as they 35 are hydrophilic and bind to the intracellular side of the plasma membrane (Kong et al., 2013) to 36 initiate signaling (Preuten et al., 2015). Although, the ability to associate with the plasma 37 membrane is conserved in algal phots (Sullivan et al., 2016), the mechanism underlying this 38 attachment is still not known, but is thought to involve some form of lipid binding/modification. 39

Kinase inactive versions of phot1 and phot2 are non-functional highlighting the 40 importance of receptor autophosphorylation in phot signaling (Inoue et al., 2008; Inoue et al., 41 2011). Autophosphorylation occurs predominantly on multiple serine residues. At least 21 and 42 29 phosphorylation sites have been identified for Arabidopsis phot1 and phot2, respectively 43 (Christie et al., 2015). Most of these sites are found in the N-terminus of the protein which 44 contains two light-sensing modules known as LIGHT, OXYGEN OR VOLTAGE SENSING 45 (LOV) domains known as LOV1 and LOV2 (Christie et al., 2012). Autophosphorylation of S350, 46 S376 and S410 within the LOV-linker region promotes binding of 14-3-3 regulatory proteins to 47 phot1 (Inoue et al., 2008; Sullivan et al., 2009). However, the biological significance of this 48 interaction is still not known. The occurrence of some these phosphorylation sites is also 49 fluence-rate dependent (Salomon et al., 2003) and is thought to play a role in receptor 50 desensitization (Christie and Murphy, 2013). By contrast, autophosphorylation of two conserved 51 serine residues within the activation loop of the C-terminal kinase domain (S849 and S851 in 52 phot1; S761 or S763 in phot2) are necessary for receptor signaling (Inoue et al., 2008; Inoue et 53 al., 2011). Mutation of these sites to alanine impairs phot1 function in Arabidopsis, whereas 54 phosphomimetic substitutions to aspartate are without effect (Inoue et al., 2008). 55

Despite considerable efforts over the last two decades, the signaling events that follow 56 receptor autophosphorylation remain poorly understood for most phot-mediated responses. Yet, 57



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it is becoming increasingly apparent that members of the NPH3/RPT2-Like family (NRL) are 58 required to elicit several phot responses. Moreover, accumulating evidence suggests that these 59 plant-specific proteins act in concert with different AGCVIII kinases to regulate various aspects 60 of auxin transport and signaling. In this review, we summarize our current understanding of the 61 biochemical properties of the NRL family in Arabidopsis and how these proteins function to 62 coordinate different aspects of phot signaling. We also discuss to what extent these signaling 63 processes are conserved in land plants and algae. 64 65 Structure and Function of Arabidopsis NRL Proteins 66 The NRL family is named after its two founding members NON-PHOTOTROPIC HYPOCOTYL 67 3 (NPH3) and ROOT PHOTOTROPISM 2 (RPT2) (Liscum et al., 2014) which were first 68 identified from genetic screens for Arabidopsis mutants impaired in hypocotyl and root 69 phototropism (Okada and Shimura, 1992; Liscum and Briggs, 1995; Sakai et al., 2000). The 70 primary amino acid structure of NRL proteins can be separated into three main parts based on 71 sequence conservation: a BTB (bric-a-brac, tramtrack and broad complex) domain at the N-72 terminus, followed by an NPH3 domain and a C-terminal coiled coil domain (Liscum et al., 73 2014). In addition to NPH3 and RPT2, Arabidopsis contains a further 31 NPH3/RPT2-like 74 proteins (NRL1 to 31), all of which are defined by the presence of the NPH3 domain (Pedmale 75 et al., 2010). Ten of these members lack the C-terminal coiled coli domain, whereas 2 are 76 devoid of the BTB domain (Pedmale et al., 2010). The reasons for these differences in domain 77 structure are not clear at present because many of these NRL proteins have yet to be ascribed 78 a biological function. 79

Functions for 10 out of the 33 Arabidopsis NRL proteins have been identified so far. 80 Phylogenetic analysis has shown that NRL proteins can be classified into 7 distinct clades in 81 land plants (Suetsugu et al., 2016). However, in angiosperms such as Arabidopsis only 6 of 82 these clades are present (Fig. 1). NRL proteins from 3 of these clade classifications (Suetsugu 83 et al., 2016) are known to interact with the phots. These include NPH3 (Motchoulski and 84 Liscum, 1999), RPT2 (Inada et al., 2004), NRL PROTEIN FOR CHLOROPLAST MOVEMENT 1 85 (NCH1/NRL31) (Suetsugu et al., 2016) and NRL2 (Sullivan et al., 2009). NRL2 was identified as 86 a phot1-interacting protein through yeast-two hybrid screening (Sullivan et al., 2009). However, 87 its functional role in phot signaling remains undetermined. NPH3 and RPT2 are required for 88 several auxin-mediated growth processes including phototropism, leaf positioning and leaf 89 expansion (Christie et al., 2015). A central role for coordinating auxin distribution has also been 90 linked to other members of the NRL family which function independently from the phots. For 91



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instance, DEFECTIVELY ORGANIZED TRIBUTARIES 3 (DOT3/NRL23) is associated with 92 vascular development and leaf vein patterning (Petricka et al., 2008), whereas NRL proteins 93 (NRL6, NRL7, NRL20, NRL21, and NRL30) known as NAKED PINS IN YUCCA (NPY) (Fig. 1) 94 function redundantly to regulate auxin movements required for organogenesis and root 95 gravitropism in concert with AGCVIII kinases other than the phots (Cheng et al., 2008; Li et al., 96 2011). NRL8 (otherwise known as SETH6) is involved in pollen tube growth (Lalanne et al., 97 2004) which also requires AGC kinases activity (Zhang et al., 2008). Consequently, NRL 98 proteins are proposed to function as AGC kinase modules that regulate various aspects of auxin 99 trafficking and signaling. However, as discussed later, new evidence on the function of NRL 100



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proteins in phot signaling has begun to break down this paradigm that these proteins are solely 101 mediators of auxin-dependent processes. 102 103 NRL-dependent and –independent Phot Responses 104 Phots regulate a range of physiological responses in Arabidopsis. These are listed in Table 1 105 and can be separated into two categories depending on the involvement of NRL proteins (NRL 106 dependent and NRL independent). Phototropism (Motchoulski and Liscum, 1999; Sakai et al., 107 2000), petiole positioning and leaf expansion (Inoue et al., 2008) and chloroplast accumulation 108 (Suetsugu et al., 2016) are examples of NRL-dependent responses, whereas chloroplast 109 avoidance movement (Kong and Wada, 2014) and stomatal opening are NRL-independent 110 (Inoue and Kinoshita, 2017). While several of these responses can be described as NRL 111 independent, it is worth remembering that functions for 23 members of the NRL family are still 112 lacking. Whether these processes are truly devoid of NRL involvement awaits further genetic 113 characterization of these remaining family members. In the following sections, we summarize 114 progress made to date in uncovering the role of NRL proteins in phot signaling. 115 116 NPH3 and its Role in Phototropism 117 A central role for NPH3 in phototropism has been firmly established for some time now. 118 Arabidopsis mutants lacking NPH3 fail to exhibit phototropism under a variety of different light 119 conditions (Liscum et al., 2014; Fankhauser and Christie, 2015). A detailed discussion of 120 phototropism is beyond the scope of this review and readers are directed to other articles that 121 provide a comprehensive overview of the different types of photophysiological responses 122 involved (Sakai and Haga, 2012; Christie and Murphy, 2013). While the biochemical function of 123 NPH3 remains poorly understood, it appears to be instrumental for establishing lateral auxin 124 gradients required for this differential growth response (Haga et al., 2015). NPH3 is localized to 125 the plasma membrane and has been shown to interact directly with phot1 via its C-terminal 126 region (Motchoulski and Liscum, 1999). Like the phots, NPH3 contains no obvious 127 transmembrane spanning domain, so how it associates with the plasma membrane is still not 128 known. However, truncation and transient expression analysis of NPH3-GFP in stomatal guard 129 cells of Vicia faba suggests that the C-terminus, including the coiled coil domain, is important for 130 localization to the plasma membrane (Inoue et al., 2008). 131

Recent in vivo co-immunoprecipitation analysis indicates that phot1-NPH3 interactions at 132 the plasma membrane are transiently disrupted upon irradiation (Haga et al., 2015). Light not 133 only impacts the ability of NPH3 to interact with phot1, but also leads to dynamic changes in its 134



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subcellular localization. Expression of YFP-NPH3 under the control of the constitutive 135 Cauliflower Mosaic Virus 35S promoter restores hypocotyl phototropism in the nph3 mutant 136 (Haga et al., 2015). YFP-NPH3 is localized to the plasma membrane in darkness, but is rapidly 137 (within minutes) internalized into micro-domain aggregates upon phot1 activation by blue light 138 (Haga et al., 2015). The appearance of these micro-domains is diminished in periods of 139 prolonged irradiation or when seedlings are returned to darkness suggesting that their formation 140 is reversible (Haga et al., 2015). The biological significance and the role of these micro-domains 141 in phot signaling is currently unknown. However, biochemical fractionation experiments indicate 142 that these NPH3 aggregates accumulate in the cytosol (Haga et al., 2015). These findings 143 agree with observations that cytoskeleton inhibitors or inhibitors of vesicle trafficking fail to affect 144 NPH3 micro-domain formation (Haga et al., 2015). 145

The above phot1-driven changes in NPH3 localization correlate well with alterations in 146 NPH3 phosphorylation status. NPH3 is phosphorylated in darkness and becomes rapidly (within 147 minutes) dephosphorylated following phot1 activation (Pedmale and Liscum, 2007). This de-148 phosphorylation process is tissue, and most likely cell autonomous (Sullivan et al., 2016) and 149 does not appear to be initiated by phot2 (Inada et al., 2004; Pedmale and Liscum, 2007; 150 Tsuchida-Mayama et al., 2008; Haga et al., 2015). As found for YFP-NPH3 micro-domain 151 formation, NPH3 de-phosphorylation is recoverable either in darkness (Pedmale and Liscum, 152 2007) or over periods of prolonged irradiation (Haga et al., 2015). The kinetics for NPH3 de-153 phosphorylation and re-phosphorylation correlate closely with the timescale described for the 154 changes in YFP-NPH3 localization (Haga et al., 2015). This has led to the proposal that 155 phosphorylation of NPH3 is necessary for it to form an active signaling complex with phot1 at 156 the plasma membrane (Fig. 2). Phot1-NPH3 interactions are disrupted following NPH3 de-157 phosphorylation and its release from the plasma membrane (Haga et al., 2015) leading to a 158 cessation of receptor signaling. Thus, reassembly of this complex would be necessary to re-159 establish and sustain phototropic signaling especially under continuous irradiation (Fig. 2). 160

The identity of the kinase(s) responsible for phosphorylating NPH3 is still not known. 161 Moreover, studies have yet to examine whether NPH3 is a substrate for phot1 kinase activity. 162 However, pharmacological studies have implicated a role for a type 1 protein phosphatase 163 (Pedmale and Liscum, 2007). To date, 18 phosphorylation sites have been identified within 164 NPH3 through global phosphoproteomic approaches (Heazlewood et al., 2008). The 165 contribution of some of these sites to phototropic signaling has been investigated through 166 structure-function analysis. S212, S222 and S236 downstream of the BTB domain are 167 phosphorylated in darkness and become dephosphorylated following phot1 activation 168



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(Tsuchida-Mayama et al., 2008). Collective mutation of these sites to alanine or deletion of this 169 region (Δ212-238) does not adversely affect the ability of NPH3 to mediate hypocotyl 170 phototropism in Arabidopsis (Tsuchida-Mayama et al., 2008). Phosphorylation sites other than 171 S212, S222 and S236 are therefore clearly important (Haga et al., 2015). Identifying these sites 172 and dissecting how changes in their phosphorylation status impact NPH3 function presents a 173 formidable challenge for future research. However, recent work has now demonstrated that the 174 second founding member of the NRL family, RPT2 has a role in modulating the phosphorylation 175 status and localization dynamics of NPH3 in Arabidopsis. 176 177 Contribution of RPT2 to Phot Signaling 178 RPT2 was originally identified from a genetic screen for Arabidopsis mutants impaired in root 179 phototropism (Okada and Shimura, 1992; Sakai et al., 2000) and has been shown to interact 180 directly with both NPH3 (Inada et al., 2004) and phot1 (Inada et al., 2004; Sullivan et al., 2009). 181 The transposon-insertion mutant rpt2-2 lacks RPT2 protein (Inada et al., 2004) and is impaired 182 in hypocotyl phototropism at blue light intensities ≥ 0.17 μmol m-2 s-1 (Haga et al., 2015). By 183 contrast, the phototropic response of rpt2-2 mutants is indistinguishable from wild-type 184



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seedlings at blue light intensities ≤ 0.017 μmol m-2 s-1 (Haga et al., 2015). A requirement for 185 RPT2 in regulating phototropism to higher light correlates well with its expression profile. 186 Expression of RPT2 is barely detectable in etiolated seedlings, but increases in response to red 187 and blue light (Inada et al., 2004; Tsuchida-Mayama et al., 2008; Haga et al., 2015) in a fluence 188 rate-dependent manner (Sakai et al., 2000). As indicated above, reconstitution of a phot1-NPH3 189 complex is considered necessary to sustain effective phototropic signaling under continuous 190 irradiation (Fig. 2). The presence of RPT2 is necessary to facilitate this process at high light 191 intensities (Haga et al., 2015). Based on these findings, RPT2 is proposed to contribute to 192 photosensory adaption and promote efficient phototropism under brighter light conditions (Fig. 193 2). 194

Mutants deficient in either NPH3 or RPT2 exhibit leaf positioning and leaf expansion 195 phenotypes that resemble those of the phot1 phot2 double mutant (Inoue et al., 2008; Harada et 196 al., 2013). These findings demonstrate that NPH3 and RPT2 have roles in phot signaling 197 besides phototropism. Leaf positioning and leaf expansion both require differential growth and 198 most likely arise from alterations in auxin distribution. The severity of rpt2 phenotype for these 199 responses (Harada et al., 2013) is dramatically reduced under moderate light conditions when 200 crossed with the phot1 single mutant. This phenotype of the phot1 rpt2 double mutant has 201 uncovered a level of complexity regarding the contribution of RPT2 to phot signaling. RPT2 acts 202 positively in conjunction with phot1 to mediate leaf positioning and leaf expansion. In contrast, 203 RPT2 is not required for phot2 signaling. Instead, RPT2 appears to have some role in 204 suppressing the ability of phot1 to inhibit phot2 signaling for these responses. In this model (Fig. 205 3), both phot1 and phot2 signaling pathways would be impaired in the rpt2 mutant. The phot1 206 pathway would be inactive since its signaling is dependent on RPT2, whereas phot2 signaling is 207 impaired owing to the suppressive action of phot1. Likewise, both phot1 and phot2 signaling 208 pathways would be inactive in a phot2 rpt2 double mutant. However, phot2 signaling for leaf 209 positioning and leaf expansion would still viable in this model for the phot1 rpt2 double mutant 210 consistent with the phenotype observed, since the inhibitory action of phot1 is removed (Fig. 3). 211

Additional evidence suggests that this complex interplay between phot1 and phot2 212 signaling may occur for other phot responses. The rpt2-1 mutant shows impaired hypocotyl 213 phototropism under low and high fluence rates of unilateral blue light (Inada et al., 2004). 214 Phototropic responsiveness was restored at higher fluence rates in the phot1-101 rpt2-1 double 215 mutant indicative of functional phot2 signaling. Similarities can be drawn between these results 216 and those of observed for the leaf positioning and leaf expansion phenotypes of the phot1 rpt2 217 mutant (Harada et al., 2013). However, some caution should be exercised when comparing 218



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these findings given the difference in ecotypes used, as well as the apparent leakiness of the 219 rpt2-1 mutant (Haga et al., 2015). 220 221 Phytochrome Kinase Substrate Proteins 222 NPH3 and RPT2 are not the only mediators of phototropism, leaf positioning and leaf expansion 223 in Arabidopsis. PHYTOCHROME KINASE SUBSRTATE proteins (PKS1-4) also play a role in 224 establishing these processes. PKS1 was originally identified as a kinase substrate for 225 phytochrome A (phyA) (Fankhauser et al., 1999). Whether phyA is bona fide protein kinase is 226 still debated although recent work has offered renewed support for its role as a protein kinase in 227 regulating photomorphogenesis (Shin et al., 2016). While PKS proteins are required for 228 phytochrome signaling (Lariguet et al., 2003; Schepens et al., 2008), some of the phenotypes 229 associated with pks mutants resemble those of nph3, rpt2 and phot-deficient mutants. For 230 instance, the pks1pks2pks4 triple mutant exhibits reduced phototropic curvature (Lariguet et al., 231 2006; Kami et al., 2014). PKS1 and PKS2 also act in concert with NPH3 to establish leaf 232 positioning and leaf expansion (de Carbonnel et al., 2010). Their role in phot signaling appears 233 to be restricted to these processes since pks mutants are not impaired in blue light-induced 234 stomatal opening and chloroplast photorelocation movement (de Carbonnel et al., 2010). 235 Consistent with their involvement in phot signaling, PKS proteins are known to localize to the 236 plasma membrane where they are known to associate with phot1, phot2 and NPH3 (Lariguet et 237 al., 2006; de Carbonnel et al., 2010; Demarsy et al., 2012) Furthermore, studies have shown 238 that PKS4 is a substrate target for phot1 kinase activity (Demarsy et al., 2012). Together, these 239 data clearly demonstrate that PKS proteins are integral components of the phot signaling 240



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pathways associated with NPH3 and RPT2. Resolving the biochemical functions of these 241 proteins and how they integrate with NPH3 and RPT2 will be important to fully understand how 242 phots initiate signaling from the plasma membrane. Like NPH3, PKS proteins are suggested to 243 modulate auxin transport or signaling (de Carbonnel et al., 2010; Kami et al., 2014). Yet, their 244 mechanism of action in this regard remains to be elucidated. 245 246 NCH1 and RPT2 are Mediators of Chloroplast Accumulation Movement 247 Phot-induced chloroplast accumulation movement has recently been shown to involve the co-248 action of two NRL proteins. At low blue light intensities, phot1 and phot2 overlap in function to 249 direct chloroplast relocation to the upper and lower cell surface to maximize light capture for 250 photosynthesis (Sakai et al., 2001). Chloroplast avoidance movement is mediated solely by 251 phot2 (Kagawa et al., 2001) and serves to prevent photodamage of the photosynthetic 252 apparatus in excess light (Kasahara et al., 2002). Chloroplast movement is achieved by the 253 formation of chloroplast actin (cp-actin) filaments that polymerize on the leading edge of the 254 chloroplast (Kadota et al., 2009). Polymerization of cp-actin requires the action of 255 CHLOROPLAST UNUSUAL POSITIONING 1 (CHUP1) (Oikawa et al., 2003) and KINESIN-256 LIKE PROTEIN FOR ACTIN-BASED CHLOROPLAST MOVEMENT (KAC) proteins (Suetsugu 257 et al., 2010). PLASTID MOVEMENT IMPAIRED 1 (PMI1) is also required to stabilize cp-actin 258 filaments (Suetsugu et al., 2015). Consequently, cp-actin formation and thus chloroplast 259 accumulation and avoidance movement are impaired in chup1, pmi1 and kac1 kac2 double 260 mutants. 261

How light perception by phots is coupled to the activity of CHUP1, PMI1 and KAC 262 proteins is not known. At least for chloroplast accumulation movement, the NRL proteins NCH1 263 (NRL31) and RPT2 have been shown to function as key mediators of this response (Suetsugu 264 et al., 2016). NCH1 and RPT2 reside with the same clade of the NRL family tree in land plants 265 (Fig. 1). Both nch1 and rpt2 mutants exhibit a weaker chloroplast accumulation response 266 compared to wild-type plants (Suetsugu et al., 2016). However, this process is completely 267 abolished in the rpt2 nch1 double mutant indicating that NCH1 functions redundantly with RPT2 268 to mediate chloroplast accumulation movement (Suetsugu et al., 2016). Moreover, chloroplast 269 avoidance movement is unaltered in the rpt2 nch1 double mutant demonstrating that NCH1 and 270 RPT2 are only necessary for the accumulation response. While these findings have uncovered 271 a new function for NRL proteins in phot signaling, they also demonstrate that RPT2 plays a 272 central role in establishing several different phot responses. RPT2 could possibly mediate 273 additional aspects of phot signaling in conjunction with other members of the NRL family. 274



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Further genetic analysis of the NRL family in combination with the rpt2 mutant will be required to 275 shed light on this possibility. 276

The discovery of NCH1 and its role in chloroplast accumulation movement has now 277 changed our view on how different NRL proteins contribute to phot and AGCVIII kinase 278 signaling. Chloroplast photorelocation movement is cell autonomous and occurs independently 279 of gene expression (Kong and Wada, 2016; Wada, 2016). Thus, auxin trafficking and auxin-280 mediated transcription are not required for this processes in contrast to multi-cellular responses 281 like phototropism, leaf positioning and leaf expansion. These findings are the first to 282 demonstrate that NRL proteins can function with AGCVIII kinases to elicit responses 283 independently of auxin. 284 285 Biochemical Function of NRL Proteins 286 Molecular genetic analysis in Arabidopsis has been successful in identifying physiological 287 functions for almost a third of the NRL family. Nevertheless, it is still not clear how these 288 proteins operate at the biochemical level. The majority of NRL proteins contain a BTB domain 289 which can function as a substrate adaptor to recruit specific proteins for ubiquitination and 290 degradation (Hua and Vierstra, 2011). Indeed, NPH3 has been reported to interact with CULLIN 291 3a (CUL3a) when co-expressed in insect cells and may form part of CUL3 RING E3 UBIQUITIN 292 LIGASE (CRL3) complex that directs ubiquitination of signaling targets (Roberts et al., 2011). 293 Biochemical and mass spectrometry analysis has shown that phot1 becomes ubiquitinated by a 294 CRLNPH3 complex following blue light activation (Deng et al., 2014). CRL3NPH3-mediated poly-295 ubiquitination of phot1 is associated with its degradation in response to prolonged irradiation, 296 whereas mono-ubiquitination is proposed to stimulate rapid trafficking of phot1 from the plasma 297 membrane in response to low light intensities (Roberts et al., 2011). Whether this light-activated 298 change in subcellular localization plays a role in phot1 signaling is still open to question (Liscum, 299 2016). Recent approaches aimed at tethering phot1 to the plasma membrane by myristoylation 300 or farnesylation suggest this not to be the case, as incorporation of these modifications severely 301 diminishes the light-induced internalization of phot1 without impacting its functionality in 302 Arabidopsis (Preuten et al., 2015). So far, no other targets besides phot1 have been identified 303 for the CRL3NPH3 complex. Yet, it is worth noting that phot1-driven changes in subcellular 304 trafficking of the auxin efflux carrier PIN2 are dependent on NPH3 (Wan et al., 2012). Since 305 dynamic adjustments in PIN2 distribution and turnover have been linked to ubiquitination of K63 306 (Leitner et al., 2012), it is tempting to speculate that auxin transporters could be CRL3NPH3 307



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targets. That said, there is currently no published evidence indicating that NPH3 can physically 308 interact with auxin transport proteins. 309

NPH3 is not the only NRL protein to exhibit features of a CRL3 substrate adaptor. NCH1 310 (NRL31) was previously identified as AtSR1 INTERACTING PROTEIN 1 (SR1IP1) (Zhang et 311 al., 2014). SR1IP1 and CUL3a interact when transiently co-expressed in Nicotiana 312 benthamiana. SR1IP1 is responsible for ubiquitination and subsequent degradation of the 313 Arabidopsis Ca2+/calmodulin-binding transcription factor SIGNAL RESPONSIVE 1 (AtSR1), 314 which functions to suppress plant defense responses to bacterial pathogens. Consequently, 315 sr1ip1 mutants are more susceptible to Pseudomonas infection indicating that SR1IP1 serves 316 as a positive regulator of plant immunity (Zhang et al., 2014). By contrast, virus-induced gene 317 silencing of SR1IP1 orthologues in Nicotiana benthamiana reduces susceptibility to Phytopthora 318 infestans infection suggesting that SR1IP1 can also act as a negative regulator of plant defense 319 (Yang et al., 2016). Clearly more work is needed to elucidate the role of SR1IP1 (NCH1) in plant 320 immunity and how this function integrates with its role in regulating chloroplast accumulation 321 movement (Suetsugu et al., 2016). Chloroplasts can aid the transport of pro-defence signals to 322 the nucleus via highly dynamic connections known as stromules (Caplan et al., 2015). It will 323 therefore be of interest to examine whether NRL proteins such as NCH1 are involved, especially 324 since light is known to impact stromule formation (Gray et al., 2012; Brunkard et al., 2015). 325 326 327 Evolutionary Conservation of Phot Signaling 328 Phots are restricted to the green plant lineage from photosynthetic algae to flowering plants 329 (Fig. 3), but are absent from red algae (Li et al., 2015). In contrast to land plants, green algae 330 typically contain one phot (Huang et al., 2002; Prochnik et al., 2010; Sullivan et al., 2016), 331 although two phots have been identified in Zygnematales including Mougeotia scalaris both of 332 which might function to mediate chloroplast photorelocation movement in this alga (Suetsugu et 333 al., 2005; Li et al., 2015). Several functions have been ascribed to phot from Chlamydomonas 334 reinhardtii. These include light-regulation of various aspects of the sexual lifecycle (Huang et al., 335 2002; Huang and Beck, 2003; Ermilova et al., 2004), the control of eyespot development and 336 phototactic behavior (Trippens et al., 2012), and transcriptional regulation of enzymes involved 337 in chlorophyll and carotenoid biosynthesis (Im et al., 2006). More recently, Chlamydomonas 338 phot has been shown to be pivotal for modulating the abundance of key molecular effectors 339 required for photoprotection of the photosynthetic machinery. As a result, the phot-deficient 340



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mutants of Chlamydomonas displays reduced fitness under excessive light conditions 341 (Petroutsos et al., 2016). 342

Despite its divergent functions, Chlamydomonas phot can successfully restore 343 phototropism, chloroplast photorelocation movement and stomatal opening when expressed in 344 the phot1 phot2 double mutant of Arabidopsis (Onodera et al., 2005). These findings suggest 345 that the mode of action between plant and algal phots is highly conserved. However, recent 346 studies centered on phot from the marine picoalga Ostreococcus tauri are not consistent with 347 this conclusion. While Ostreococcus phot is capable of mediating chloroplast accumulation 348 movement, stomatal opening, as well as leaf positioning and leaf expansion when expressed in 349 the phot1 phot2 double mutant of Arabidopsis, it fails to restore phototropism and chloroplast 350 avoidance movement (Sullivan et al., 2016). At least for phototropism, this lack of functionality 351 correlates with the inability of Ostreococcus phot to complex with NPH3 (Sullivan et al., 2016). 352 These findings fall more in line with what is known regarding the evolutionary conservation of 353 NPH3 and other NRL proteins involved in phot signaling. NPH3, RPT2 and NCH1 are prevalent 354 in land plants including liverworts and mosses (Suetsugu et al., 2016), but have not been 355 identified in green algae (Fig. 4). The presence of these NRLs in land plants would coincide with 356 their cooption to modulate multi-cellular (e.g. phototropism), as well as cell-autonomous (e.g. 357 chloroplast movement, stomatal opening) responses. 358

Chloroplast photorelocation movement is prevalent in both land plants and green algae. 359 The liverwort Marchantia polymorpha contains 7 NRL proteins; one protein for each of the 7 360 NRL clades (Suetsugu et al., 2016). The ortholog of NCH1 is essential for chloroplast 361 accumulation movement in Marchantia, but not for the avoidance response indicating that the 362 signaling events underlying chloroplast photorelocation movements are conserved in land plants 363 (Suetsugu et al., 2016). In contrast to Arabidopsis, Marchantia contains one representative 364 ortholog for the NPH3 clade and one for the NCH1/RPT2 clade suggesting that the divergence 365 of these NRL proteins occurred early in land plant evolution (Suetsugu et al., 2016). PKS 366 proteins by comparison appear to have evolved later than NPH3 and NCH1/RPT2 in the land 367 plant lineage (Fig. 4). CHUP1, KAC, PMI1 and NRL proteins are present in Streptophytes 368 (including land plants and charophytes) and are essential factors for driving chloroplast 369 photorelocation movement (Suetsugu and Wada, 2016). However, no orthologs of these genes 370 have been found in chlorophytes (including Chlamydomonas and Ostreococcus). Thus, NRL-371 mediated chloroplast movement may have been acquired during evolution of the streptophyte 372 lineage. Yet, the charophyte alga Klebsormidium flaccidum (charophyte) does contain two NRL-373 like proteins (Suetsugu et al., 2016). It is possible that these proteins mediate chloroplast 374



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photorelocation in this organism. Clearly, more work is needed to determine how light-induced 375 chloroplast movement is achieved in photosynthetic algae. 376 377 Conclusions and Future Perspectives 378 Molecular genetic analysis in Arabidopsis has been instrumental in shedding light on the 379 biological functions of NRL family members. Work so far has coordinated their mode of action 380 with AGCVIII kinases and auxin signaling. Studies have now shown that NRL proteins can 381 mediate signaling independently of auxin, at least in the case of chloroplast accumulation 382 movement. A major challenge for future research will be to elucidate how NRL proteins function 383 at the biochemical level and how changes in their localization and phosphorylation status can 384 impact their activity. At least 24 out of the 33 NRL members are known to be phosphorylated 385 (Heazlewood et al., 2008). Unlike NPH3 and NCH1, RPT2 does not exhibit E3 ubiquitin ligase 386 activity in vitro (Roberts et al., 2011). Nor does its plasma membrane localization change in 387 response to blue light treatment (Haga et al., 2015). Hence, the biochemical and localization 388 properties for specific NRL family members are clearly different. Resolving the biochemical 389 functions of NPH3 and RPT2 and their role in phot signaling will be essential if we are to 390



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understand how lateral auxin gradients are established to promote responses such as 391 phototropism, leaf positioning and leaf expansion. NRL2 is known to interact with phot1 392 (Sullivan et al., 2009), but its biological role in phot signaling awaits additional molecular and 393 genetic characterization. Further functional dissection of the Arabidopsis NRL family will be a 394 demanding task given the large size of this protein family and the redundancy between 395 members. The reduced size and complexity of the NRL family in Marchantia now provides a 396 tractable alternative to assigning functions to each of 7 NRL clade classifications found in land 397 plants. 398



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399 Figure Legends 400 Figure 1. Bayesian phylogenetic tree of the NRL protein family in Arabidopsis. The Bayesian 401 phylogenetic tree of NRL proteins. The tree was modified from that in Suetsugu et al. (Suetsugu 402 et al., 2016) with Archaeopteryx software. Six of the seven major clades of land plant NRL 403 proteins are color coded. RPT2/NCH1, NPH3 and NPY reside in different clades. 404 405 Figure 2. Role of NPH3 and RPT2 in mediating phototropic signaling in Arabidopsis. The model 406 was modified from Haga et al. (Haga et al., 2015) where phot1 and NPH3 form a plasma 407 membrane (PM) complex in darkness. Phot1-NPH3 interactions are diminished upon phot1 408 activation and dephosphorylation of NPH3. However, efficient signaling under continuous blue 409 light conditions requires reconstitution of a phot1-NPH3 complex which involves RPT2 at higher 410 blue light intensities. 411 412 Figure 3. Functional complexity for RPT2 in controlling phot-mediated leaf positioning in 413 Arabidopsis. The model was adapted from Harada et al. (Harada et al., 2013). Sold black 414 lines/arrows illustrate the signaling pathways operational in wild-type plants and mutant 415 backgrounds. Non-operational pathways in each of the genotypes are greyed out for clarity. 416 417 Figure 4. Schematic representation depicting the evolution of phot signaling components in the 418 green plant lineage. The topology of the lineages is derived from Bowman et al. (Bowman et al., 419 2007). Arrows indicate the lineages in which orthologs of PHOT, NRL and PKS proteins were 420 identified from genomic and/or transcriptomic data. Stomata evolved after hornwort 421 diversification. 422 423 424 425 426 427 428 429 430 431 432



18

Phot Response NRL-dependent NRL-independent References Phototropism Requires NPH3 and

RPT2 (Motchoulski and

Liscum, 1999; Sakai et al., 2000)

Petiole positioning Requires NPH3 and RPT2

(Inoue et al., 2008; Harada et al., 2013)

Leaf expansion Requires NPH3 and RPT2

(Inoue et al., 2008; Harada et al., 2013)

Chloroplast accumulation

Requires RPT2 and NCH1 (NRL31)

(Suetsugu et al., 2016)

Chloroplast avoidance Does not require NPH3, RPT2 or NCH1

(NRL31)


Nuclear avoidance Does not require NPH3

(Higa et al., 2014)

Stomatal opening Does not require NPH3, RPT2 or NCH1

(NRL31)


Destabilization of Lhcb mRNA

Requires NPH3 (Folta and Kaufman, 2003)

Inhibition of hypocotyl elongation

Does not require NPH3

(Folta and Spalding, 2001)

Circadian control of PSII photosynthetic

efficiency

Does not require NPH3

(Litthauer et al., 2015)

Table 1. NRL-dependent and -independent phot-mediated responses in Arabidopsis. 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449



19

450



ADVANCES

• Phototropin (phot) blue-light receptors regulate phototropism, choloroplast accumulation movement, leaf positioning and leaf flattening in Arabidopsis through the coordinated action of specific NRL family members.

• NPH3 is essential for establishing lateral auxin gradients underpinning phototropic curvatures and possibly leaf positioning and expansion.

• RPT2 modulates phototropic responsiveness through alterations in the localization and phosphorylation status of NPH3.

• NCH1 and RPT2 function redundantly to mediate chloroplast accumulation movement independently of auxin.

• NPH3 and NCH1 exhibit biochemical features of CRL3 substrate adaptors.

• Functional divergence of phot-NRL signaling has occurred during land plant evolution.



OUTSTANDING QUESTIONS

• How do NPH3 and RPT2 coordinate auxin fluxes for phototropism?

• How do the dynamic changes in NPH3 localization and phosphorylation contribute to its action?

• Do NRL proteins besides NPH3 and NCH1 exhibit E3 ubiquitin ligase activity and what are their substrates?

• How do PKS proteins integrate with NPH3 and RPT2 to mediate phot signaling?

• How do NCH1 and RPT2 drive cp-actin polymerization required for chloroplast accumulation movement?

• What is the function of the phot1-interacting protein NRL2?



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Motchoulski A, Liscum E (1999) Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science286: 961-964


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Petroutsos D, Tokutsu R, Maruyama S, Flori S, Greiner A, Magneschi L, Cusant L, Kottke T, Mittag M, Hegemann P, Finazzi G,Minagawa J (2016) A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature 537: 563-566


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Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, ChapmanJ, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E,Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS (2010) Genomic analysis of organismal complexity in the multicellular greenalga Volvox carteri. Science 329: 223-226


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Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2. A signal transducer of the phototropic response in Arabidopsis. Plant Cell 12:225-236


Salomon M, Knieb E, von Zeppelin T, Rudiger W (2003) Mapping of low- and high-fluence autophosphorylation sites in phototropin1. Biochemistry 42: 4217-4225


Schepens I, Boccalandro HE, Kami C, Casal JJ, Fankhauser C (2008) PHYTOCHROME KINASE SUBSTRATE4 modulatesphytochrome-mediated control of hypocotyl growth orientation. Plant Physiol 147: 661-671


Shin AY, Han YJ, Baek A, Ahn T, Kim SY, Nguyen TS, Son M, Lee KW, Shen Y, Song PS, Kim JI (2016) Evidence that phytochromefunctions as a protein kinase in plant light signalling. Nat Commun 7: 11545


Suetsugu N, Higa T, Kong SG, Wada M (2015) PLASTID MOVEMENT IMPAIRED1 and PLASTID MOVEMENT IMPAIRED1-RELATED1Mediate Photorelocation Movements of Both Chloroplasts and Nuclei. Plant Physiol 169: 1155-1167


Suetsugu N, Mittmann F, Wagner G, Hughes J, Wada M (2005) A chimeric photoreceptor gene, NEOCHROME, has arisen twiceduring plant evolution. Proc Natl Acad Sci U S A 102: 13705-13709

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Suetsugu N, Takemiya A, Kong SG, Higa T, Komatsu A, Shimazaki K, Kohchi T, Wada M (2016) RPT2/NCH1 subfamily of NPH3-likeproteins is essential for the chloroplast accumulation response in land plants. Proc Natl Acad Sci U S A 113: 10424-10429


Suetsugu N, Wada M (2016) Evolution of the Cp-Actin-based Motility System of Chloroplasts in Green Plants. Front Plant Sci 7: 561Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-basedchloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107: 8860-8865


Sullivan S, Petersen J, Blackwood L, Papanatsiou M, Christie JM (2016) Functional characterization of Ostreococcus tauriphototropin. New Phytol 209: 612-623


Sullivan S, Takemiya A, Kharshiing E, Cloix C, Shimazaki KI, Christie JM (2016) Functional characterization of Arabidopsisphototropin 1 in the hypocotyl apex. Plant J 88: 907-920


Sullivan S, Thomson CE, Kaiserli E, Christie JM (2009) Interaction specificity of Arabidopsis 14-3-3 proteins with phototropinreceptor kinases. FEBS Lett 583: 2187-2193


Trippens J, Greiner A, Schellwat J, Neukam M, Rottmann T, Lu Y, Kateriya S, Hegemann P, Kreimer G (2012) Phototropin influenceon eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell 24: 4687-4702


Tsuchida-Mayama T, Nakano M, Uehara Y, Sano M, Fujisawa N, Okada K, Sakai T (2008) Mapping of the phosphorylation sites onthe phototropic signal transducer, NPH3. Plant Science: 626-633


Wada M (2016) Chloroplast and nuclear photorelocation movements. Proc Jpn Acad Ser B Phys Biol Sci 92: 387-411Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluska F, Lin J (2012) The signal transducer NPH3 integratesthe phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24: 551-565


Yang L, McLellan H, Naqvi S, He Q, Boevink PC, Armstrong M, Giuliani LM, Zhang W, Tian Z, Zhan J, Gilroy EM, Birch PR (2016)Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor. PlantPhysiol 171: 645-657


Zhang D, Wengier D, Shuai B, Gui CP, Muschietti J, McCormick S, Tang WH (2008) The pollen receptor kinase LePRK2 mediatesgrowth-promoting signals and positively regulates pollen germination and tube growth. Plant Physiol 148: 1368-1379


Zhang L, Du L, Shen C, Yang Y, Poovaiah BW (2014) Regulation of plant immunity through ubiquitin-mediated modulation of Ca(2+)-calmodulin-AtSR1/CAMTA3 signaling. Plant J 78: 269-281




http://scholar.google.com/scholar?as_q=A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution&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 chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suetsugu&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Suetsugu N%2C Takemiya A%2C Kong SG%2C Higa T%2C Komatsu A%2C Shimazaki K%2C Kohchi T%2C Wada M %282016%29 RPT2%2FNCH1 subfamily of NPH3%2Dlike proteins is essential for the chloroplast accumulation response in land plants%2E Proc Natl Acad Sci U S A 113%3A 10424%2D10429&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Suetsugu N, Takemiya A, Kong SG, Higa T, Komatsu A, Shimazaki K, Kohchi T, Wada M (2016) RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants. Proc Natl Acad Sci U S A 113: 10424-10429


http://scholar.google.com/scholar?as_q=RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants&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=RPT2/NCH1 subfamily of NPH3-like proteins is essential for the chloroplast accumulation response in land plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suetsugu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Suetsugu N%2C Wada M %282016%29 Evolution of the Cp%2DActin%2Dbased Motility System of Chloroplasts in Green Plants%2E Front Plant Sci 7%3A 561&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Suetsugu N, Wada M (2016) Evolution of the Cp-Actin-based Motility System of Chloroplasts in Green Plants. Front Plant Sci 7: 561


http://scholar.google.com/scholar?as_q=Evolution of the Cp-Actin-based Motility System of Chloroplasts in Green Plants.&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=Evolution of the Cp-Actin-based Motility System of Chloroplasts in Green Plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suetsugu&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Suetsugu N%2C Yamada N%2C Kagawa T%2C Yonekura H%2C Uyeda TQ%2C Kadota A%2C Wada M %282010%29 Two kinesin%2Dlike proteins mediate actin%2Dbased chloroplast movement in Arabidopsis thaliana%2E Proc Natl Acad Sci U S A 107%3A 8860%2D8865&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107: 8860-8865


http://scholar.google.com/scholar?as_q=Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana&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=Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Suetsugu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sullivan S%2C Petersen J%2C Blackwood L%2C Papanatsiou M%2C Christie JM %282016%29 Functional characterization of Ostreococcus tauri phototropin%2E New Phytol 209%3A 612%2D623&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sullivan S, Petersen J, Blackwood L, Papanatsiou M, Christie JM (2016) Functional characterization of Ostreococcus tauri phototropin. New Phytol 209: 612-623

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

http://scholar.google.com/scholar?as_q=Functional characterization of Ostreococcus tauri phototropin&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=Functional characterization of Ostreococcus tauri phototropin&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sullivan&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sullivan S%2C Takemiya A%2C Kharshiing E%2C Cloix C%2C Shimazaki KI%2C Christie JM %282016%29 Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex%2E Plant J 88%3A 907%2D920&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sullivan S, Takemiya A, Kharshiing E, Cloix C, Shimazaki KI, Christie JM (2016) Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex. Plant J 88: 907-920


http://scholar.google.com/scholar?as_q=Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex&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=Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sullivan&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sullivan S%2C Thomson CE%2C Kaiserli E%2C Christie JM %282009%29 Interaction specificity of Arabidopsis 14%2D3%2D3 proteins with phototropin receptor kinases%2E FEBS Lett 583%3A 2187%2D2193&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Sullivan S, Thomson CE, Kaiserli E, Christie JM (2009) Interaction specificity of Arabidopsis 14-3-3 proteins with phototropin receptor kinases. FEBS Lett 583: 2187-2193


http://scholar.google.com/scholar?as_q=Interaction specificity of Arabidopsis 14-3-3 proteins with phototropin receptor kinases&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=Interaction specificity of Arabidopsis 14-3-3 proteins with phototropin receptor kinases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sullivan&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Trippens J%2C Greiner A%2C Schellwat J%2C Neukam M%2C Rottmann T%2C Lu Y%2C Kateriya S%2C Hegemann P%2C Kreimer G %282012%29 Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii%2E Plant Cell 24%3A 4687%2D4702&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Trippens J, Greiner A, Schellwat J, Neukam M, Rottmann T, Lu Y, Kateriya S, Hegemann P, Kreimer G (2012) Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell 24: 4687-4702

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

http://scholar.google.com/scholar?as_q=Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii&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=Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Trippens&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tsuchida%2DMayama T%2C Nakano M%2C Uehara Y%2C Sano M%2C Fujisawa N%2C Okada K%2C Sakai T %282008%29 Mapping of the phosphorylation sites on the phototropic signal transducer%2C NPH3%2E Plant Science%3A 626%2D633&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Tsuchida-Mayama T, Nakano M, Uehara Y, Sano M, Fujisawa N, Okada K, Sakai T (2008) Mapping of the phosphorylation sites on the phototropic signal transducer, NPH3. Plant Science: 626-633

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tsuchida-Mayama&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wada M %282016%29 Chloroplast and nuclear photorelocation movements%2E Proc Jpn Acad Ser B Phys Biol Sci 92%3A 387%2D411&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wada M (2016) Chloroplast and nuclear photorelocation movements. Proc Jpn Acad Ser B Phys Biol Sci 92: 387-411

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

http://scholar.google.com/scholar?as_q=Chloroplast and nuclear photorelocation movements&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=Chloroplast and nuclear photorelocation movements&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wada&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Wan Y%2C Jasik J%2C Wang L%2C Hao H%2C Volkmann D%2C Menzel D%2C Mancuso S%2C Baluska F%2C Lin J %282012%29 The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2%2Dbased polar auxin transport in Arabidopsis root phototropism%2E Plant Cell 24%3A 551%2D565&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluska F, Lin J (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24: 551-565

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

http://scholar.google.com/scholar?as_q=The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism&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=The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Wan&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yang L%2C McLellan H%2C Naqvi S%2C He Q%2C Boevink PC%2C Armstrong M%2C Giuliani LM%2C Zhang W%2C Tian Z%2C Zhan J%2C Gilroy EM%2C Birch PR %282016%29 Potato NPH3%2FRPT2%2DLike Protein StNRL1%2C Targeted by a Phytophthora infestans RXLR Effector%2C Is a Susceptibility Factor%2E Plant Physiol 171%3A 645%2D657&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yang L, McLellan H, Naqvi S, He Q, Boevink PC, Armstrong M, Giuliani LM, Zhang W, Tian Z, Zhan J, Gilroy EM, Birch PR (2016) Potato NPH3/RPT2-Like Protein StNRL1, Targeted by a Phytophthora infestans RXLR Effector, Is a Susceptibility Factor. Plant Physiol 171: 645-657

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


http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yang&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang D%2C Wengier D%2C Shuai B%2C Gui CP%2C Muschietti J%2C McCormick S%2C Tang WH %282008%29 The pollen receptor kinase LePRK2 mediates growth%2Dpromoting signals and positively regulates pollen germination and tube growth%2E Plant Physiol 148%3A 1368%2D1379&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang D, Wengier D, Shuai B, Gui CP, Muschietti J, McCormick S, Tang WH (2008) The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth. Plant Physiol 148: 1368-1379

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

http://scholar.google.com/scholar?as_q=The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth&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=The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang L%2C Du L%2C Shen C%2C Yang Y%2C Poovaiah BW %282014%29 Regulation of plant immunity through ubiquitin%2Dmediated modulation of Ca%282%2B%29 %2Dcalmodulin%2DAtSR1%2FCAMTA3 signaling%2E Plant J 78%3A 269%2D281&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang L, Du L, Shen C, Yang Y, Poovaiah BW (2014) Regulation of plant immunity through ubiquitin-mediated modulation of Ca(2+) -calmodulin-AtSR1/CAMTA3 signaling. Plant J 78: 269-281

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

http://scholar.google.com/scholar?as_q=Regulation of plant immunity through ubiquitin-mediated modulation of Ca(2+) -calmodulin-AtSR1/CAMTA3 signaling&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=Regulation of plant immunity through ubiquitin-mediated modulation of Ca(2+) -calmodulin-AtSR1/CAMTA3 signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1


Shining Light on the Function of NPH3/RPT2-like Proteins ... · 33 stomatal opening and...

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