Auxin Signaling 2 4 10 - Plant physiology · 64 cellular, tissue, organ and whole plant scales....

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Auxin Signaling 1 2 Ottoline Leyser 3 4 Sainsbury Laboratory 5 University of Cambridge University 6 Bateman Street 7 Cambridge 8 CB2 1LR 9 10 Email: [email protected] 11 12 13 One sentence summary: Auxin triggers diverse responses in plants and this is 14 reflected in quantitative and qualitative diversity in the auxin signaling 15 machinery. 16 17 Funding information: OL’s research is funded by The Gatsby Charitable 18 Foundation, The European Research Council and The UK Biotechnology and 19 Biological Science Research Council. 20 21 22

Plant Physiology Preview. Published on August 17, 2017, as DOI:10.1104/pp.17.00765

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23 Abstract 24 Auxin acts as a general co-ordinator of plant growth and development, 25 transferring information over both long and short ranges. Auxin famously 26 appears to be extraordinarily multi-functional, with different cells responding 27 very differently to changes in auxin levels. There has been considerable progress 28 over recent years in understanding how this complexity is encoded in the 29 cellular auxin response machinery. Of central importance is an elegantly short 30 but versatile signaling pathway through which auxin triggers changes in gene 31 expression. However, it is increasingly clear that this pathway is not sufficient to 32 explain all auxin responses and other auxin signaling systems are emerging. 33 34 Auxin by analogy 35 Apparently, I have been writing reviews about auxin for 20 years (Leyser, 1997), 36 and certainly I have been in very good company. Auxin is a much written about 37 molecule. Entire books are dedicated to it (Estelle et al, 2011). From all these 38 column inches there is a clear consensus that auxin is extremely important, that 39 it is involved in virtually every aspect of plant biology, and that this baffling array 40 of functions makes the task of understanding auxin daunting to say the least. 41 Many very helpful analogies have been developed in an attempt to provide an 42 intellectual framework within which auxin biology can be adequately 43 encapsulated. A major driver for these analogies is to move away from the 44 constraints of auxin as a specific instructive signal triggering specific and 45 universal outcomes (Weyers and Paterson, 2001). This idea is clearly 46 inappropriate as far as auxin is concerned, but nonetheless somehow inveigles 47 its way into the field due to prevalent paradigms in signalling biology in general, 48 and hormone biology in particular. For auxin, it is increasingly clear that the 49 specificity in the system is not in the signal, but in the cells that perceive it. Auxin 50 does not instruct cells to do anything in particular, but rather it influences the 51 behavior of cells according to their pre-existing identity. For example I have 52



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previously suggested that auxin is like the baton wielded by the conductor of an 53 orchestra- “When the auxin baton points your way, it’s your turn to play 54 whatever musical instrument you happen to be holding” (Leyser, 2005). 55 This analogy is of course deficient in many ways. In particular, it brings into 56 sharp relief the second and perhaps more important challenge that must be 57 embraced to understand auxin. Although auxin can trigger very specific changes 58 in cells, this seldom involves step changes in auxin concentration. The question 59 of how auxin works is not the question of what happens when some auxin 60 arrives at a cell. There is always auxin. The absolute and relative amount of auxin 61 at any one location in the plant varies over time and this tunes and retunes the 62 balance within a set of interlocking feedback loops operating at subcellular, 63 cellular, tissue, organ and whole plant scales. Within the orchestral analogy, 64 maybe some of this can be captured by considering the dynamics of the music. 65 The baton is not a play-don’t play switch but can also be used to modulate how 66 loudly to play. But even with this addition, the analogy does not allow sufficiently 67 for feedback, with the baton being modulated by the players. Maybe if there is an 68 unruly player in the orchestra, the baton might become a little more insistent, 69 and certainly an orchestral performance is a collaboration between the 70 conductor and the players, with information flow mediated by the baton and its 71 behavior. The same musical score can be interpreted differently by different 72 conductor-orchestra combinations. Nonetheless in this scenario, there is no 73 doubt who is in charge. It's the conductor. In a plant, there is no central control. 74 Rather all aspects of auxin biology are characterized by emergent self-organizing 75 properties that allow distributed rather than centralized decision making. 76 These considerations have led to another prevalent analogy, or rather a useful 77 comparison (Leyser, 2016). Many of the functions performed by the auxin 78 network in plants are fulfilled by the nervous system in animals. Here a very 79 non-specific signal, an electrical impulse, carries information through the 80 organism modulating diverse outputs depending on the receiving tissue. There is 81 extensive feedback, and in the brain in particular, dynamic self-organisation with 82 competition and reinforcement rewiring neural connections depending on their 83 frequency of use. However, there is also the obvious and glaring difference, 84 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from

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already mentioned above, of central vs distributed processing. This difference is 85 often discussed in the context of the heterotrophic vs autotrophic life styles of 86 animals vs plants. While heterotrophy is supported by locomotion allowing long 87 distance foraging for food, autotrophy on land requires large surface areas for 88 acquisition of dilute resources such as light, carbon dioxide and water. This latter 89 involves large underground surface areas, precluding locomotion. As a 90 consequence plants are unable to escape predation by locomotion and so must 91 be robust to loss of body parts. Central processing- a brain- is poorly suited to 92 this requirement and instead plants typically have no unique parts. 93 Addressing these issues, in their review, Stewart and Nemhauser argue that 94 auxin is a cellular currency “think of it as money. Auxin does not have much 95 intrinsic value—it stores very little energy or raw materials. However, like paper 96 currency, it has great symbolic value, as an easily circulated means of facilitating 97 transactions in the dynamic economy of plant life” (Stewart and Nemhauser, 98 2010). Like auxin, money does everything, but what it does depends on who 99 gives it to whom and under what circumstances. And the economics analogy 100 certainly offers plenty of potential for feedback and complex self-organizing 101 dynamics. 102 The money analogy is also interesting from an evolutionary perspective. Money 103 was invented as a proxy for the things people really need or want, to allow 104 diverse goods and services to be more readily exchanged in more complex and 105 less direct ways than a one on one swap, for example, of eggs for bread. This is 106 potentially an interesting way to think about auxin. It is metabolically close to an 107 amino acid, tryptophan, and amino acid availability via limitations in N supply is 108 an important constraint on plant growth (Elser et al, 2007). Auxin could 109 plausibly have evolved from a mechanism directly linking amino acid availability 110 to growth. In the context of the increasing complexity of multicellular plant form, 111 with division of labor between different cell and tissue types, a direct local link 112 between resource availability and growth does not allow the necessary co-113 ordination and prioritization of growth across the organism. For example, in 114 most seed plants, shoots capture carbon and roots capture mineral nutrients 115 such as nitrate. Growth of the root and shoot systems must therefore be 116 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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prioritized depending on the C:N ratio in the plant, rather than the local 117 availability of either fixed carbon or nitrogen. The requirement to co-ordinate 118 growth, not just regulate it, necessitates dedicated signaling systems that can 119 operate both systemically and locally. As a general description, auxin is one such 120 growth co-ordinator- regulating where, when, how much and what sort of 121 growth should occur. We have previously argued that the apparent diversity of 122 auxin action makes sense in this context (Bennett and Leyser, 2014). An early 123 origin as a general growth co-ordinator could be followed by cooption to 124 modulate wider co-ordinated activities. Once money has been invented it can be 125 used and reused to buy things that did not previously exist. In this review, I will 126 focus on how auxin as a currency is traded at the cellular level, or put rather less 127 fancifully, how cells recognize and use information about changes in the amount 128 of auxin present. 129 130 Auxin and the regulation of transcription 131 The major mechanism by which changes in auxin levels are converted into 132 cellular responses is via changes in transcription. Hundreds of genes change 133 their expression rapidly in response to exogenous auxin supply (Paponov et al, 134 2008). Auxin regulates transcription via an elegantly short signal transduction 135 pathway, which has been extensively reviewed (Chapman and Estelle, 2009; 136 Salehin et al, 2015) and is illustrated in figure 1. In brief, auxin acts as molecular 137 glue bringing together F-box proteins of the TRANSPORT INHIBITOR RESPONSE 138 1/AUXIN SIGNALING F-BOX (TIR1/AFB) family and members of the Aux/IAA 139 transcriptional repressor family (Tan et al, 2007). F-box proteins are the 140 substrate selection subunit of SCF-type ubiquitin protein ligase complexes, 141 named after three of their subunits- Skp1, Cullin and an F-box protein (Smalle 142 and Vierstra, 2004). The F-box itself is a motif at the amino terminal end of F-box 143 proteins through which they interact with Skp1, which also interacts with a 144 dimer of Cullin and RBX1. This dimer transfers activated ubiquitin from an 145 ubiquitin activating enzyme and conjugates it to target proteins. The target 146 protein is brought to the SCF by its interaction with the carboxy-terminal domain 147



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of the F-box protein. In the case of TIR1/AFBs this consists of leucine rich 148 repeats including an auxin binding pocket (Tan et al, 2007). The binding of auxin 149 in this pocket is greatly stabilized by the docking of the Aux/IAA protein across 150 the pocket mouth, mediated by a short protein motif in the Aux/IAA known as 151 domain II (Tan et al, 2007). For this reason TIR1/AFB- Aux/IAA pairs can be 152 considered as co-receptors for auxin. The auxin-mediated binding of Aux/IAAs to 153 TIR1/AFBs brings them to the SCF, allowing their ubiquitination and subsequent 154 degradation (Gray et al, 2001; Maraschin et al, 2009). In this way, changes in 155 auxin levels are converted into changes in Aux/IAA levels. 156 There are 29 Aux/IAAs in Arabidopsis (Paponov et al, 2008). Their half-lives and 157 the extent to which their half-lives reduce in response to applied auxin vary 158 greatly (Dreher et al, 2006). An important determinant of these characteristics is 159 the sequence of Domain II. This sequence acts as a degron and is sufficient to 160 confer auxin-triggered destruction on heterologous proteins (Zenser et al, 2001). 161 Aux/IAA half-lives also depend on sequences outside the degron and the AFB 162 with which the Aux/IAA interacts (Moss et al, 2015). There are 6 AFBs in 163 Arabidopsis (Dharmasiri et al, 2005, Prigge et al, 2016). Different TIR1/AFB-164 Aux/IAA pairs have very different affinities for each other, and for different 165 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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auxins, contributing to the wide range of Aux/IAA half-lives and their auxin 166 sensitivities (Calderon Villalobos et al, 2012). Reconstitution of the auxin 167 response pathway in yeast demonstrates the diversity in dynamics that can be 168 achieved through this mechanism, such that the same change in auxin input can 169 result in a wide range of changes in Aux/IAA output (Havens et al, 2012). There 170 is evidence that this variation is functionally significant in planta. For example, in 171 Arabidopsis the Aux/IAA protein IAA14 is involved in the early stages of lateral 172 root development. Stabilized auxin insensitive versions of IAA14 are well known 173 to block lateral root emergence completely. Point mutations in this protein have 174 been engineered to produce variants, which in partnership with TIR1, have 175 approximately 10 and 100x lower affinity for auxin (Guseman et al, 2015). This 176 increases their half-lives in response to auxin addition from approximately 20 177 minutes to more than 2 hours. When these variants are expressed in plants, they 178 delay lateral root emergence in proportion to their half-lives (Guseman et al, 179 2015). 180 Aux/IAA proteins act as transcriptional repressors (Ulmasov et al, 1997). They 181 contain a conserved EAR domain through which they can recruit co-repressors 182 of the TOPLESS (TPL) family to promoters (Tiwari et al, 2004; Szemenyei et al, 183 2008). In turn, TPLs can recruit chromatin remodeling proteins that stabilize 184 transcriptional repression (Szemenyei et al, 2008). The Aux/IAAs do not 185 themselves bind DNA, but they can dimerize with transcription factors of the 186 AUXIN RESPONSE FACTOR (ARF) family. Dimerization occurs through C-187 terminal PB1 domains shared by both protein families (Guilfoyle, 2015). The PB1 188 domain has an acidic and a basic interaction surface through which dimerization 189 can occur. This arrangement can support Aux/IAA oligomerization, like a stack of 190 Lego bricks (Korasick et al, 2014; Nanao et al 2014; Dinesh et al, 2015). Point 191 mutations along one face of IAA19 that allow Aux/IAA dimerization with ARFs, 192 but do not support subsequent oligomerization with additional Aux/IAAs are 193 non-functional in some assays, suggesting that these higher order complexes can 194 contribute to effective transcriptional repression (Korasick et al, 2014). However, 195 transcription can be repressed without such higher order complex formation 196 (Pierre-Jerome et al, 2016). 197 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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ARF proteins can also homodimerize through their N-terminal B3 domains, and 198 it is through this homotypic dimerization that they co-operatively bind DNA 199 (Boer DR, 2014). ARFs bind to specific Auxin Response Elements (ARE) with the 200 consensus sequence TGTCTC in the promoters of auxin regulated genes (Abel 201 and Theologis, 1996; Mironova et al, 2014). A subset of ARFs include a Q rich 202 middle domain between the B3 and PB1 domains and these ARFs can act as 203 transcriptional activators through recruitment of chromatin remodeling 204 enzymes (Ulmasov et al 1999; Wu et al 2015). Oligomerization with Aux/IAAs 205 prevents this activation. Auxin modulates the level of expression from ARF-206 bound promoters by triggering Aux/IAA degradation. 207 Since the ability of Aux/IAAs to modulate transcription is entirely dependent on 208 ARFs, the presence of different ARF complements in different cells can also 209 contribute to auxin signaling specificity (Bargmann et al., 2013; Rademacher et al, 210 2012). There are 23 different ARFs in Arabidopsis and evidence for differential 211 affinities between specific ARFs and Aux/IAAs (Vernoux et al, 2011). Different 212 homo and hetero oligomerizations of Aux/IAAs at the promoter may add an 213 additional mechanism for auxin response diversity (Knox et al, 2003; Bargmann 214 et al., 2013; Rademacher et al, 2012). For palindromic AREs, there is also 215 evidence for different affinities between different dimerized ARFs and ARE-216 containing promoters, based on the spacing of the ARE palindrome (Boer et al, 217 2014). Interestingly many ARFs lack the Q rich region (Ulmasov et al, 1999). 218 They bind the same AREs and in some cases there is good evidence that they act 219 as transcriptional repressors (Ulmasov et al, 1999). It is likely that these 220 repressor ARFs compete with activator ARFs for occupancy of the same 221 promoters (Vert et al, 2008). The complement of repressive ARFs in a cell 222 therefore provides an additional mechanism by which different cells might 223 respond differently to auxin. It is also possible that these various alternative 224 protein-DNA and protein-protein interactions at the promoters of auxin-225 regulated genes are further influenced by protein-protein interactions off the 226 promoter. For example off-promoter Aux/IAA oligomerizations could sequester 227 specific Aux/IAAs preventing their interactions with ARFs. 228



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This system allows extremely rapid changes in transcription in response to auxin. 229 Changes in transcript abundance can be detected within 3-5 minutes of auxin 230 treatments (McClure et al, 1989; Abel and Theologis, 1996). The half-life of many 231 Aux/IAAs is very short even in the absence of exogenously applied auxin (Abel et 232 al, 1994) and the genes encoding Aux/IAA proteins are themselves rapidly up-233 regulated in response to auxin (Abel and Theologis, 1996). Thus cells 234 continuously make and degrade Aux/IAAs with the flux of Aux/IAAs through this 235 cycle modulated by auxin, potentially re-equilibrating the system at different 236 steady states depending on the auxin concentration. Consistent with this 237 behavior, auxin signaling is particularly sensitive to mutation in apparently 238 generic parts of the protein degradation and protein synthesis machinery (Del 239 Pozo et al, 2002; Gray et al, 2003; Hellmann et al, 2003; Chuang et al, 2004; 240 Stirnberg et al, 2012). This powerfully illustrates the mismatch between auxin 241 signaling and the classical on-off switch paradigm. Auxin modulates 242 transcription through retuning the equilibrium in a highly dynamic, feedback-243 regulated network. The system is capable of acting as a bistable switch, but it has 244 a much wider range of possible behaviors, and even stable high and low 245 expression states are dependent on flux through the Aux/IAA synthesis-246 degradation cycle (Bridge et al, 2012). 247 Another important feature of this system is that auxin acts by degrading a non-248 DNA binding inhibitor of transcription. From an evolutionary perspective this 249 immediately suggests the hypothesis that the ability of auxin to regulate 250 transcription could have been added on to an existing system of transcriptional 251 regulation. A completely auxin-independent system, consisting only of activator 252 and repressor ARFs competing for the same promoters, with some mechanism 253 for changing their relative abundance could provide a way to modulate 254 transcription from multiple genes, for example tuning growth in response to 255 environmental factors. Adding in Aux/IAA-mediated transcriptional repression 256 and auxin-triggered Aux/IAA degradation would make these genes auxin 257 responsive in the presence of activator ARFs. Some evidence to support this 258 order of events in the evolution of auxin signaling comes from recent work on 259 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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basal land plant species- the liverwort, Marchantia polymorpha, and the moss, 260 Physcomitrella patens. 261 The Marchantia genome has only three ARFs, one Aux/IAA and one TIR1/AFB. 262 Evidence to date supports the idea that this system works in the same way as in 263 angiosperms, described above (Kato et al, 2015; Flores-Sandoval et al, 2015). 264 The ARFs fall into three distinct clades covering both activator and repressor 265 ARFs, all three of which are represented in angiosperm genomes (Kato et al, 266 2015). This three-clade structure is therefore the likely ancestral state for land 267 plants. Analysis of gain of function and reduced function mutants in these 268 components has identified diverse auxin-regulated aspects of growth and 269 development such as cell expansion in dorsal epidermal tissues of the 270 Marchantia thallus (Kato et al, 2015; Flores-Sandoval et al, 2015). 271 In Physcomitrella patens there are 16 ARFs, distributed across the three clades 272 described above, and 3 Aux/IAAs (Prigge et al, 2010). Recently a Physcomitrella 273 line completely lacking all these Aux/IAAs has been generated (Lavy et al, 2016). 274 These plants lack any detectable transcriptional response to auxin and 275 phenotypically resemble moss plants treated with high levels of auxin. The 276 analysis of this line arguably provides some support for the idea that auxin 277 signaling evolved as a refinement of a system based on environmental control of 278 the ratio of repressive and activating ARFs. First, over expression of a repressive 279 ARF in the triple Aux/IAA mutant background suppresses its constitutive high 280 auxin phenotype, and indeed confers a phenotype similar to that conditioned by 281 expression of stablized auxin resistant Aux/IAA protein variants (Lavy et al, 282 2016). This suggests that repressive and activating ARFs do indeed compete for 283 access to the same promoters, and shifting the ratios between them can 284 coordinately regulate transcription from these promoters. 285 Second, examination of the auxin-Aux/IAA-ARF-regulated transcriptome in moss 286 shows that the gene set down-regulated by auxin and loss of Aux/IAAs is 287 enriched for genes involved in light responses, photosynthesis and carbon 288 fixation; while the up-regulated gene set is enriched for genes involved in 289 transcription and biosynthesis (Lavy et al, 2016). This correlates with the ability 290



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of auxin to suppress the production of the chloroplast-rich chloronemal moss 291 filaments and promote the production of relatively chloroplast-poor caulonemal 292 filaments, which extend the moss colony. Auxin can therefore be seen as 293 switching the moss colony from prioritizing energy and carbon capture to 294 prioritizing growth and expansion. This might be associated with differences in 295 the C:N ratio, and could ancestrally have been driven, for example, by light 296 regulation of ARFs, perhaps modulated in some way by N availability. Consistent 297 with this speculative idea, like auxin, high light prioritizes caulonemal over 298 chloronemal growth (Thelander et al, 2005). However, unlike light, auxin is 299 potentially mobile in the plant and hence can co-ordinate growth systemically. 300 As described above, an early origin as a general growth co-ordinator could be 301 followed by cooption to modulate and co-ordinated a wider range of activities 302 across the plant body, consistent with the lethality often observed in higher plant 303 auxin signaling mutants, for example lacking multiple members of the TIR1/AFB 304 family (Dharmasiri et al, 2005). 305 In this context the recent discovery of an additional ARF-dependent auxin 306 sensing mechanism is of particular interest. ETTIN is a non-canonical ARF that 307 lacks the PB1 Aux/IAA interaction domain. Its best characterized role is in 308 regulating patterning in the developing gynoecium (Sessions et al, 1997; 309 Nemhauser et al, 2000). Here ETTIN dimerises with the basic helix-loop-helix 310 transcription factor INDEHISCENT (IND) to regulate transcription of key target 311 genes (Simonini et al, 2016). This dimerization is affected by auxin binding, and 312 this correlates with auxin-dependent changes in the association of ETTIN with 313 the promoters of target genes, and auxin-dependent changes in the expression of 314 these targets (Simonini et al, 2016). This ability of auxin to modulate the 315 interaction between ETTIN and partner transcription factors extends beyond 316 IND, and indeed could be quite widerspread (Simonini et al, 2016). It will be 317 interesting to explore the evolutionary origin of this mechanism for auxin-318 regulated transcription based on a non-canonical ARF. 319 Is that all there is? 320



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The TIR1/AFB-Aux/IAA-ARF signaling system provides plenty of scope for 321 diversity in auxin response, and the dramatic phenotypes of mutants 322 compromised in this pathway attest to its importance in the co-ordination of 323 plant growth and development. 324 This begs the question as to whether this is primary auxin detection system in 325 plants. Several arguments have been put forward in support of the existence of 326 additional auxin response systems. However, many of these can easily be 327 accommodated by the TIR1/AFB-Aux/IAA-ARF system. One argument that there 328 are multiple systems comes from the very different auxin sensitivities of 329 different auxin responses, both with respect to their dose-response kinetics and 330 their specificity for different auxins. For example, a much-studied classical 331 response to auxin is its ability to drive cell elongation in hypocotyls, epicotyls 332 and coleoptiles, all of which must elongate rapidly during early seedling 333 establishment after seed germination. This response is complex. In pea, the 334 natural auxin indole-3-acetic acid (IAA) has a biphasic dose response curve with 335 maxima in the 1µM and 1mM ranges (Yamagami et al, 2004). Meanwhile, the 336 dose response curve for the synthetic auxin 1-naphthaleneacetic acid (NAA) has 337 only one maximum in the 10µM range (Yamagami et al, 2004). Of these response 338 maxima, only the high affinity IAA response is strongly sensitive to Ca2+ 339 availability, while the others are not (Yamagami et al, 2004). This kind of 340 diversity has been used to argue for two distinct perception mechanisms with 341 different affinities for IAA and NAA. However the diversity in auxin sensitivity of 342 TIR1/AFB-Aux/IAA pairs could account for these phenomena given the wide 343 range of Kms described for different auxins and different AFB-Aux/IAA pairs 344 (Calderon Villalobos et al, 2012). The basis for the differences in Ca2+ sensitivity 345 are less straightforward to accommodate through the AFB-Aux/IAA system. 346 While the downstream effectors driving these elongation responses are a matter 347 for debate, there is substantial evidence supporting a role for various ion fluxes 348 across the plasma membrane (Ruck et al, 1993). Because the activity of diverse 349 membrane transporters is regulated post-transcriptionally, this is a second 350 argument that has fueled speculation about additional response pathways, and 351 specifically non-transcriptional auxin effects. For example, auxin-induced 352 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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elongation is associated with stimulation of the plasma membrane proton 353 pumping ATPase (PM H+ ATPase), thereby acidifying the apoplast (Hager, 2003; 354 Takahashi et al, 2012). According to the acid growth hypothesis, this in turn 355 affects cell wall extensibility leading to turgor-driven elongation (Kutschera, 356 1994). This response is quite slow, and so could reasonably result from the very 357 rapid changes in gene expression triggered by auxin (Badescu and Napier, 2005). 358 Indeed, recent data support this idea. In particular, there is mounting evidence 359 that auxin stimulates the activity of the PM H+ ATPase by up-regulating the 360 transcription of members of the SMALL AUXIN UP-REGULATED RNA (SAUR) gene 361 family, via the canonical TIR1/AFB-Aux/IAA-ARF pathway (Chae et al, 2012; 362 Spartz et al, 2012). 363 As their name suggests, the SAUR genes were originally identified because many 364 of them are rapidly up-regulated in response to auxin (Abel and Theologis, 1996). 365 The promoters of the auxin-upregulated SAUR family members include the 366 classical ARE ARF binding motif and changes in SAUR transcript abundance can 367 be detected within 5 minutes of auxin application (Abel and Theologis, 1996; 368 McClure et al, 1989). SAUR genes are plant-specific and typically present as 369 multi-gene families, making genetic analysis difficult. However, the use of 370 artificial microRNAs to target multiple SAURs simultaneously, together with 371 gain-of-function studies have demonstrated that in Arabidopsis the SAUR19-372 SAUR24 sub-family are positive regulators of cell expansion in diverse tissues 373 including the hypocotyl (Spartz et al, 2012). 374 This work has been greatly helped by the discovery that fusion proteins between 375 these SAURs and a wide range of tags result in the stabilization of the proteins, 376 providing over-expression lines (Spartz et al, 2012). Arabidopsis lines over-377 expressing tagged SAUR19 have long hypocotyls due to increased cell expansion. 378 This phenotype is associated with reduced apoplastic pH, which is significantly 379 attenuated in PM H+ ATPase mutant backgrounds (Spartz et al, 2014). Consistent 380 with these results, the SAUR19 over-accumulating lines show constitutive 381 activity of the PM H+ ATPase, associated with increased phosphorylation of Thr- 382 947 within the pump’s C-terminal auto-inhibitory domain. Phosphorylation at 383 this site is known to activate the PM H+ ATPase by driving recruitment of a 14-3-384



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3 protein, which binds to the domain, alleviating its inhibitory influence 385 (Fuglsang et al, 1999; Kanczewska et al, 2005). Fluorescent tags demonstrate 386 that SAUR19 can localize to the plasma membrane (Spartz et al, 2012). 387 Furthermore SAUR19, and other SAUR family members, interact directly with 388 type 2C protein phosphatase D (PP2C-D), inhibiting its activity, and this PP2C-D 389 interacts with and inhibits the activity of the PM H+ ATPase (Spartz et al, 2014; 390 Sun et al, 2016). These results support a clear chain of events through which 391 auxin regulates PM H+ ATPase activity via transcriptional up-regulation of 392 SAUR19, which directly inhibits PP2C-D activity, leading to the accumulation of 393 active Thr-947 phosphorylated PM H+ ATPase, apoplast acidification, cell wall 394 loosening and growth. In support of this model Arabidopsis SAUR19 and SAUR9 395 can inhibit tomato PP2C-Ds and over-expression of Arabidopsis SAUR19 in 396 tomato bypasses the requirement for auxin addition to trigger increased cell wall 397 extensibility and elongation in excised hypocotyl segments (Spartz et al, 2017). 398 Consistent with these results, acid growth in Arabidopsis hypocotyls is 399 dependent on the TIR1/AFB-Aux/IAA-ARF signaling system (Fendrych et al, 400 2016). 401 These results provide direct evidence that the TIR1/AFB-Aux/IAA-ARF 402 transcriptional pathway for auxin response regulates PM H+ ATPase activity and 403 that this contributes to the ability of auxin to promote elongation. As mentioned 404 above, the response times for acidification and growth in these tissues are in the 405 order of 10-30 minutes, concordant with this idea. However, in other situations 406 much more rapid changes in ion fluxes and growth are observed. 407 A particularly convincing example comes from high spatiotemporal resolution 408 analyses of root responses to auxin. Addition of physiologically relevant 409 concentrations of auxin to Arabidopsis roots results in a dose-dependent influx 410 of Ca2+ across the plasma membrane, increasing cytosolic Ca2+ concentrations 411 (Monshausen et al, 2011). This response occurs within 10 seconds and is 412 accompanied by apoplastic alkalinization, which can be measured as a change in 413 root surface pH. Pretreatment with the Ca2+ channel blocker, La3+, inhibits both 414 the Ca2+ and pH responses, suggesting that the pH changes are dependent on the 415 increase in cytosolic Ca2+. 416



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Such rapid changes in ion fluxes have been detected previously, in guard cells 417 and particularly in protoplast systems where their physiological significance has 418 remained unclear (Ruck et al, 1993; Blatt and Thiel, 1994). The high level of 419 spatiotemporal resolution now possible in growing roots, coupled with the 420 power of Arabidopsis genetics, has provided robust evidence linking these fluxes 421 to growth. Both the rapid auxin-induced cytosolic Ca2+ elevation and the 422 apoplastic alkalinization have been shown to depend on a cyclic nucleotide-gated 423 channel, CNGC14 (Shih et al, 2015). Both responses are completely abolished in 424 cngc14 loss of function mutants (Shih et al, 2015). Members of this family are 425 known to transport Ca2+ and although this protein accumulates only to very low 426 levels in root tips, it can be detected at the plasma membrane in at least some 427 cell types (Shih et al, 2015). Crucially, auxin-induced root growth inhibition is 428 significantly delayed in cngc14 roots (Shih et al, 2015). In wild-type roots, a 429 significant reduction in elongation rate across the elongation zone can be 430 detected within 1 minute of auxin addition. In cngc14 mutants it is not until 7 431 minutes after auxin application that the rate of root growth slows significantly. 432 These data suggest that auxin stimulates the activity of CNGC14 triggering Ca2+ 433 influx, which in turn results in cell wall alkalinization, inhibiting cell elongation. 434 This idea is supported by analysis of the root gravity response, bypassing the 435 possibility of any artifacts associated with the use of applied auxin (Shih et al, 436 2015). The ability of roots to reorient their growth in response to changes in the 437 gravity vector is dependent on the asymmetric redistribution of auxin at the root 438 tip. Auxin transported toward the tip in the central stele is recirculated back up 439 the root through the lateral root cap and root epidermis (Luschnig et al, 1998; 440 Müller et al, 1998; Swarup et al, 2005). This pattern of auxin transport is 441 mediated by polarly localized transporters of the PIN family (Blilou et al, 2005). 442 In the columella root cap, auxin arriving through central tissues is transported 443 laterally by PIN3, where it enters the peripheral shootward transport system. 444 Tight control over the flow of auxin through these tissues is achieved by rapid 445 removal from the apoplast mediated by the AUX/LAX family of auxin importers 446 (Swarup et al, 2005). Upon gravistimulation detected in the columella root cap, 447 PIN3 is polarized in the root cap cells, directing auxin disproportionately to the 448



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lower root surface, resulting in asymmetric distribution of auxin across the root 449 and consequent asymmetric growth (Friml et al, 2002; Harrison and Mason, 450 2003). 451 Current methods for live imaging of auxin concentrations are not sufficiently 452 sensitive to detect directly this auxin asymmetry rapidly after gravistimulation 453 (Band et al, 2012). The best available method at present is based on the auxin-454 triggered degradation of a fluorescent reporter protein fused to a relatively long 455 half-life Aux/IAA degron (Vernoux et al, 2011). A long half-life degron is required 456 to allow sufficient accumulation of the fluorescent protein for detection, but 457 comes at the expense of temporal resolution. Using a parameterized model for 458 degradation of this protein in response to auxin, it has been estimated that 459 asymmetry is established at 5 minutes after gravistimulation (Band et al, 2012). 460 This is broadly consistent with the asymmetric distribution of Ca2+, which was 461 detected within 3-6 minutes of gravistimulation, with higher levels on the lower 462 surface of the root than the upper surface (Shih et al, 2015). Similarly, when 463 auxin is applied locally at the root tip, a wave of elevated cytosolic Ca2+ is 464 detected, moving shootward at a rate 150-600 µm/minute, consistent with 465 typical rates of polar auxin transport (Shih et al, 2015). That this wave is auxin-466 mediated is supported by the fact that it is dependent on the auxin influx carrier, 467 AUX1. In the case of gravistimulation, the pH at the upper surface reduces and at 468 the lower surface increases with similar kinetics. These rapid changes in ion flux 469 correlate with differential growth, which can be detected after 4 minutes. In the 470 cgnc14 mutant, all three of these effects are delayed by approximately 6 minutes 471 (Shih et al, 2015). 472 These data provide compelling evidence for a mode of auxin action too rapid for 473 the transcriptional pathway. A ten second response timeframe does not seem 474 plausible for even the extremely rapid changes in gene expression elicited by 475 auxin. Consistent with this idea, the ion flux changes are unaffected in a mutant 476 lacking three of TIR1/AFB auxin receptors (Shih et al, 2015), which is severely 477 compromised in the transcriptional response system (Dharmasiri et al, 2015). In 478 this context it is important to note that gravitropic root growth is only very 479 mildly affected in cgnc14 mutant roots, but is strongly compromised in mutants 480



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defective in the transcriptional response system. This suggests that, while the 481 CNG14-dependent response contributes to the very rapid initiation of root 482 reorientation, the transcriptional system is required for longer timeframe, 483 sustained reorientation responses. 484 The non-transcriptional detection of auxin extends further the timeframes over 485 which cells can directly sense changes in auxin concentrations from seconds to 486 many hours. The importance of these diverse response times is beautifully 487 illustrated at the root tip. Here, there is good evidence that a tip-high gradient of 488 auxin patterns root development (Sabatini et al, 1999; Galinha et al, 2007; 489 Mähönen et al, 2014), but also fine tunes growth rates, as in the example of 490 gravitropism (Luschnig et al, 1998; Müller et al, 1998; Swarup et al, 2005). A 491 cluster of initial cells form a stem cell niche at the root tip, where the auxin 492 concentration is high (Sabatini et al, 1999). These cells give rise to a rapidly 493 dividing population of cells that make up the division zone. On exiting the cell 494 cycle, the cells expand rapidly forming an elongation zone, after which they 495 mature and differentiate, for example as root hairs in the differentiation zone. 496 There is good evidence that the rate of progress of cells through these stages is 497 dependent on the tip-high auxin concentration gradient mentioned above, but 498 interpreted indirectly through the auxin-regulated expression of a set of 499 transcription factors of the PLETHORA family (Galinha et al, 2007; Mähönen et al, 500 2014). These proteins are expressed in response to the high auxin 501 concentrations of the root tip. They are very stable, persisting through cell 502 divisions. As a result, a stable gradient of PLETHORA forms, buffered against 503 rapid changes in auxin concentration, for example due to gravi-stimulated auxin 504 redistribution at the root tip (Mähönen et al, 2014). Meanwhile, as described 505 above, these transient fluctuations in auxin level can be interpreted over very 506 short timescales by calcium spiking, and over intermediate timescales by rapid 507 primary transcriptional changes, supporting dynamic responses in root growth 508 rate and direction. Thus multiple direct and indirect auxin sensing systems 509 operating over different timescales deliver robust multi-scale growth co-510 ordination. 511 A polarizing issue 512



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The existence of a non-transcriptional auxin signaling system is also supported 513 by several theoretical considerations. Transcriptional regulation has only a 514 limited ability to account for the apparent importance of auxin in polarity and 515 polarization. There is a considerable body of evidence that auxin is intimately 516 involved in the regulation of polarity. The mechanisms by which auxin 517 contributes to cellular and tissue level polarity are poorly understood and 518 consequently they are currently a very active area of research. In some cases, it 519 seems likely that auxin acts to allow proteins to respond to polarizing cues 520 provided by other systems. For example auxin, acting through its transcriptional 521 pathway, influences polar PIN accumulation and activity (Hazak et al, 2010). 522 However, there is also evidence that auxin can contribute to the polarizing cue 523 itself. 524 Here again, in some cases, the canonical TIR1/AFB-Aux/IAA-ARF pathway can 525 account for auxin-mediated polarization phenomena. For example, organ 526 primordia at the shoot apical meristem are formed at sites of locally high auxin 527 (Reinhardt et al, 2003; Heisler et al, 2005). Auxin accumulates at these maxima 528 through the action of specific members of the PIN-FORMED (PIN) family of auxin 529 efflux carrier. In the meristem epidermis, these PINs are polarized towards the 530 neighboring cell inferred from auxin response reporters to have the highest 531 auxin concentration, in a so-called “up the gradient” pattern (Reinhardt et al, 532 2003; Heisler et al, 2005; Jönsson et al, 2006; Smith et al, 2006). One mechanism 533 that has been proposed to account for this polarization is based on the ability of 534 cells to detect differences in physical forces across the cell wall (Heisler et al, 535 2010). If auxin promotes cell expansion in the meristem epidermis, then the 536 increased expansion of cells with higher auxin levels than their neighbors will 537 create tensile stresses in the cell wall adjacent to the expanding cell. If PIN 538 proteins are delivered or retained in the plasma membrane in proportion to 539 adjacent cell wall stresses, then this could drive up-the-gradient PIN polarization, 540 as observed. In this way, nuclear auxin signaling, working via auxin-regulated 541 gene expression, could regulate polarization of neighboring cells. 542 There is now strong evidence to suggest that this non-cell-autonomous 543 polarization depends on the TIR1/AFB-Aux/IAA-ARF system (Bhatia et al, 2016). 544 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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The ARF, MONOPTEROS (MP), is a central player in patterning organ emergence 545 at the shoot apical meristem. Meristems deficient in MP are barren, producing no 546 organs, nor can they be induced to produce organs by local auxin application 547 (Reinhardt et al, 2000). When small clones of wild-type MP were induced in such 548 an mp mutant background, PIN1 polarized towards the clones and organ-like 549 outgrowths were initiated at these sites (Bhatia et al, 2016). This strongly 550 suggests auxin signaling via the TIR1/AFB-Aux/IAA-ARF system can act as a 551 polarizing cue for neighboring cells in the shoot apical meristem. This could act 552 via the wall stress mechanism described above, but any directional signal from 553 the MP-expressing cells could contribute to orienting PINs in neighboring cells. 554 However, there are other examples of auxin-regulated cell polarization that are 555 more difficult to explain using only nuclear auxin signaling. Cellular polarization 556 fundamentally requires symmetry breaking, and within a cell it is difficult to see 557 how this could be accomplished by changes in transcription alone. During organ 558 formation at the shoot apical meristem, the role of auxin is non-cell autonomous, 559 with asymmetry established in the polarizing cell by auxin signaling in its 560 neighbors. There are situations where this type of explanation is more difficult to 561 reconcile with the observed phenomena. 562 A good example is the positioning of Arabidopsis root hairs. As described above, 563 various assays suggest that there is a tip-high gradient of auxin that patterns the 564 Arabidopsis root, regulating the transition of cells between the division, 565 elongation and differentiation zones. This gradient also appears to play a role in 566 positioning root hairs. Root epidermal cells elongate highly anisotropically in the 567 elongation zone. In trichoblast cell files, upon exit from the elongation zone, root 568 hairs develop as tip-growing projections from the epidermal cells (Nakamura et 569 al, 2012). The hairs are positioned close to, but a little way back from, the 570 rootward end of the trichoblast. The site of root hair development is predicted by 571 accumulation of a patch of the type I Rho of Plants (ROP) GTPase protein on the 572 plasma membrane (Molendijk et al, 2001; Jones et al, 2002). This patch acts as an 573 organizing center for the cytoskeletal changes associated with root hair 574 development. 575 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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The positioning of the ROP patch and therefore the root hair along the 576 trichobalst can be shifted by manipulation of the auxin gradient along the root 577 (Figure 2) (Fischer et al, 2006; Ikeda et al, 2009). For example, when this 578 gradient is flattened as in the aux1 ethylene-insensitive2 (ein2) gnomeb (gneb) 579 triple mutant, root hairs emerge at variable positions along the trichoblast cells. 580 Although the hairs can emerge at any position, there is a bias toward either the 581 rootward or the shootward end of the cell. Correct, rootward positioning can be 582 restored by application of auxin rootward of the differentiation zone (Fischer et 583 al, 2006). Strikingly, root hair positioning can be biased to the shootward end by 584 application of auxin shootward of the differentiating hair (Figure 2). These data 585 support the hypothesis that an auxin gradient contributes to the positioning of 586 the root hair, and consistent with this idea, mutants with defects in root tip auxin 587 biosynthesis have a shootward shift in root hair positioning (Ikeda et al, 2009). 588 Manipulation of ROP activity can also affect the position of root hair emergence. 589 For example, over-expression of ROPs, or expression of a constitutively active 590 form, can trigger the development of multiple root hairs per cell (Jones et al, 591 2002). Combined, this phenomenology, and particularly the wide range of root 592 hair positions observed in response to auxin and ROP manipulation, is difficult to 593 explain with a system in which polarization is driven non-cell autonomously 594 from neighboring cells. 595 An attractive hypothesis has been proposed to explain these data. At its core is 596 the ability of a gradient to stabilize a self-organizing Turing pattern. Turing 597 patterns emerge from a regulatory architecture involving a slow diffusing 598 activator that promotes its own activity, combined with a faster diffusing 599 inhibitor of this activity (Turing, 1952). Type I ROPs could act in a Turing system 600 since upon activation they can be S-acylated and recruited into lipid rafts (Sorek 601 et al, 2007). Thus in their inactive form they may diffuse much more rapidly than 602 in their active state. With the assumption of autocatalytic activation, this can 603 create patches of active ROPs on the membrane (Payne and Grierson, 2009). 604 However, to position the patch at a specific site along the cell, additional 605 information is needed and this is hypothesized to derive from the auxin gradient. 606 If local auxin concentration tunes, for example, the rate of autocatalytic 607 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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activation of ROPs, then the site(s) of ROP nucleation can depend on local auxin 608 concentration (Payne and Grierson, 2009). Consistent with this idea, there is 609 some evidence that auxin can rapidly activate ROPs in a dose-dependent manner 610 (Tao et al, 2002; Xu et al, 2010). This can be detected using antibodies specific to 611 the active form of ROPs. Active ROPs are known to regulate cytoskeletal 612 organization, for example via RIC1 and RIC4 (Yalofsky et al, 2008), which could 613 coordinate the events necessary for root hair emergence. 614 This model is compelling because of its impressive ability to generate the 615 patterns of root hair emergence observed as a result of various genetic and 616 pharmacological manipulations by mechanistically plausible model parameter 617 changes. The idea that symmetry breaking to generate a root hair relies on a self-618 organising Turing-like patterning system for ROPs has an evidence-base, 619 particularly with respect to polarization events in slime mold and animal cells 620 (Otsuji et al, 2007; Jilkine et al, 2007), as well as from more general 621 considerations of the requirements for self-organising polarity. The role of auxin 622 is simply to bias this system, effectively providing a quantitative positional cue. 623 In particular, the model involves sensing an intracellular, tip-high auxin gradient 624 in each trichoblast. Such a gradient is predicted to be fed by the macroscopic tip-625 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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high auxin gradient, but patterned substantially by the polar shootward 626 localization of PIN2 efflux carriers in each trichoblast cell (Grieneisen et al, 2007). 627 The active efflux of auxin from the shootward end of these cells is predicted to 628 deplete the adjacent cytoplasm of auxin, establishing a diffusion-limited auxin 629 gradient along the cell. Under this hypothesis, the aux1 ein2 gneb triple mutant 630 could reduce the steepness of the intracellular gradient by reducing cellular 631 auxin supply and uptake (Figure 2). Unfortunately, it is not currently possible to 632 measure intracellular gradients so these ideas cannot be directly tested. 633 If root hair position is indeed determined by this mechanism, auxin’s role is 634 effectively to convert an inherent apical-basal polarity axis, reflected in PIN2 635 polarity, into a new lateral growth axis for root hair emergence. However, 636 intracellular auxin gradients have also been proposed as a mechanism to 637 regulate polar PIN protein distribution itself, raising the possibility of feedback 638 between PIN-generated auxin gradients, and PIN polarity. This idea is 639 particularly interesting in the context of auxin transport canalization. Auxin 640 transport canalization is a hypothesis proposed by Tsvi Sachs to account for a 641 variety of observations associated with the regulation of vascular strand 642 patterning by auxin (Sachs et al, 1968; Sachs et al, 1969; Sachs et al, 1981). 643 Vascular strands develop between auxin sources, such as young expanding 644 leaves, and auxin sinks, such as existing vascular strands, which include files of 645 cells with highly polar rootward auxin transport. Vascular strand development is 646 preceded by the emergence of files of cells expressing highly polar PIN 647 transporters connecting the auxin source to the sink (Scarpella et al, 2006; Sauer 648 et al, 2006; Sawchuk et al, 2006). This can be explained if an initial passive flux of 649 auxin between the source and the sink is up-regulated and polarized in the 650 direction of the sink by the accumulation of PIN proteins at the plasma 651 membrane in proportion to net auxin flux across the membrane (Mitchison, 652 1980; Sachs et al, 1981; Rolland-Lagan and Prusinkiewicz, 2005). Although this 653 idea can account for a wide range of observations, the mechanism by which PIN 654 proteins can be allocated in proportion to flux (so-called “with the flux” 655 polarization), are entirely obscure (Bennett et al, 2014). One mechanism that has 656 been proposed to account for this is the allocation of PIN proteins to membranes 657 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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dependent on intracellular auxin gradients (Kramer, 2009). Modeling has 658 demonstrated that if cells with an intracellular auxin gradient greater than 1% 659 allocate PINs to the plasma membrane adjacent to the lowest cytoplasmic auxin 660 concentration, this can contribute to the positive feedback necessary to drive 661 canalization of auxin transport between an auxin source and a sink. Integral to 662 this feedback is the amplification of the intracellular gradient by PIN polarization. 663 Alternative or additional explanations for flux-correlated PIN allocation involve 664 positive feedback between PIN accumulation and PIN activity, modified by 665 extracellular auxin concentration (Cieslak et al, 2015). This requires an 666 extracellular auxin sensor of some kind, as well as the ability of PIN proteins to 667 act, in effect, as auxin sensors for example if PIN activity inhibits their removal 668 from the plasma membrane. Interestingly, this kind of dual-sensing system can 669 generate either with-the-flux type patterns of PIN accumulation or up-the-670 gradient type patterns depending on whether extracellular auxin decreases or 671 increases local PIN accumulation (Cieslak et al, 2015). 672 An additional mechanism has been reported that can generate either up-the-673 gradient or with-the-flux type patterns of PIN polarization. This involves an 674 auxin-biased spontaneous polarization mechanism similar to that described 675 above for ROPs, but operating at the whole cell level to create a single axis of 676 polarity across the cell, rather than a small patch (Abley et al, 2013). If this axis is 677 oriented by extracellular auxin, even a very shallow auxin gradient can create co-678 ordinated cell polarity across a tissue oriented from high extracellular auxin, as 679 might be expected at an auxin source, to low extracellular auxin as might be 680 expected at an auxin sink. Since polarization depends on extracellular auxin, 681 orientation of PINs toward cells with high intracellular auxin, as in up-the-682 gradient polarization patterns, can be achieved if these cells express high levels 683 of auxin importers and therefore have low extracellular auxin. This is consistent 684 with the observation that up-the-gradient PIN polarization is correlated with, 685 and in some cases dependent on, expression of auxin importers of the Aux/LAX 686 family (Abley et al, 2016). Unfortunately, as for intracellular auxin gradients, 687 there is currently no way to measure extracellular auxin concentration at the 688 level of resolution necessary to assess correlations with PIN accumulation. 689 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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Together, these considerations suggest that additional auxin sensing 690 mechanisms beyond transcription are necessary to explain the full range of 691 auxin activities. These could include an intracellular sensor that can detect 692 intracellular gradients, and/or an extracellular auxin sensor. In both cases, these 693 could act to bias self-organising polarization systems, such as ROP partitioning. 694 There is some evidence that auxin can regulate ROP activity, and thus ROP 695 partitioning (Tao et al, 2002; Xu et al, 2010). The detection systems involved are 696 poorly understood but a small family of plasma membrane-localized receptor 697 kinases have been implicated (Xu et al, 2015). Similarly, the relationship 698 between these hypothetical auxin detection systems and the rapid auxin-induced 699 Calcium transients described above is also unclear. 700 Other auxin receptors 701 Given the evidence for auxin signaling beyond the TIR1/AFB-Aux/IAA-ARF 702 system, including non-transcriptional effects, there should be additional auxin 703 receptors/sensors. Indeed several have been proposed, with varying degrees of 704 support and varying levels if evidence for their functional significance. 705 Prominent among them is Auxin Binding Protein 1 (ABP1), which has been a 706 constant and controversial feature on the auxin signaling landscape throughout 707 the full 20 years I have been writing reviews about auxin. As its name suggests, 708 ABP1 was originally identified biochemically through its ability to bind auxin 709 (Löbler M, Klämbt D, 1985a; Löbler M, Klämbt D, 1985b). A substantial body of 710 data on the biochemistry of ABP1 has accumulated since, including its crystal 711 structure (Woo et al, 2002). ABP1 binds the natural auxin, indole-3-acetic acid 712 (IAA) with a Kd of 5-10 µM (Napier, 1995). It has a much higher affinity, in the 713 region of 100nM, for the synthetic auxin NAA. Binding of NAA to ABP1 is highly 714 pH sensitive, with an optimum of 5.0-5.5, with very little binding at pH7. The cell 715 biology of ABP1 has also been studied quite intensively because the majority of 716 the protein is retained in the endoplasmic reticulum, where the pH is such that 717 auxin binding is predicted to be weak (Klode et al, 2011; Napier, 1997). Although 718 there is considerable speculation about the role of ER-localised auxin in nuclear 719 and cytoplasmic auxin homeostasis (Friml and Jones, 2010), there is currently no 720 evidence that auxin signals from the ER. However, some ABP1 appears to escape 721



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ER retention and is secreted, where the pH matches better the auxin binding 722 maximum (Jones and Herman, 1993; Napier, 1997). 723 The analysis of protoplast auxin responses provides some evidence that ABP1 724 might function as an extracellular auxin receptor (Ruck et al, 1993; Steffens et al, 725 2001; Napier, 2005). For example, protoplasts derived from Pea epicotyl 726 epidermal cells swell slightly in response to IAA addition. Measured 90 minutes 727 after auxin treatment, this response is biphasic with maxima at around 1 and 10 728 µM. The dose response curve for NAA has only a single maximum at around 1 µM. 729 When these assays are performed in the presence of antibodies against ABP1, 730 the response to NAA is completely abolished, and the response to IAA is 731 simplified, with a single peak retained at 1µM (Yamagami et al, 2004; Napier, 732 2005). One interpretation of these results is that auxin can induce protoplast 733 swelling by two different mechanisms, one of which is ABP1 dependent. 734 However, while these responses are intriguing, their physiological significance is 735 unclear. Robust in planta analysis requires genetic resources, and it is here that 736 the ABP1 story becomes most problematic. Various methods have been used to 737 assess the effects of modulating ABP1 activity in planta. These include 738 conventional anti-sense expression, as well as over-expression of both the native 739 protein and a mutant version lacking the ER retention sequence (Jones et al, 740 1998; Braun et al, 2008; Tromas et al, 2009; Robert et al, 2010). In addition, lines 741 over expressing the anti-ABP1 antibody have also been widely used, again either 742 ER-retained or secreted (Venis et al, 1992; Leblanc et al, 1999; Braun et al, 2008; 743 Tromas et al, 2009; Robert et al, 2010). These approaches come with caveats 744 because, for example, antibodies might have off-target effects, and over 745 expression is prone to neomorphism artifacts. The use of these lines has been a 746 mainstay of ABP1 research because of initial suggestions that its stable loss of 747 function resulted in early embryonic lethality, precluding the use of clean null 748 mutants for analyzing the post-embryonic roles of ABP1 (Chen et al, 2001). To 749 circumvent this problem, TILLING was used to isolate weaker alleles, including 750 the abp1-5 allele, which carries a point mutation in the auxin binding pocket 751 (Robert et al, 2010, Xu et al, 2010). This was predicted to prevent auxin binding 752 without markedly altering other ABP1 properties. 753 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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A number of auxin response defects have been reported for these ABP1-754 perturbed lines. Most have focused on cellular-level responses, such as inhibition 755 of endocytosis (Robert et al, 2010; Chen et al, 2012) and microtubule 756 reorientation (Chen et al, 2014). These phenotypes have been linked to ROP 757 activity, which as described above may be auxin regulated. ROPs, auxin and 758 ABP1 have also all been implicated in pavement cell morphogenesis in the leaf 759 (Xu et al, 2010). 760 However, the interpretation of these results has been called into question by the 761 identification of new null mutant alleles in the ABP1 gene (Gao et al, 2015). These 762 mutations have no obvious phenotypic differences compared to wild-type plants. 763 Meanwhile, the lethality attributed to loss of ABP1 in the originally analysed line 764 results from mutation in a closely linked gene (Michalko et al, 2015). Thus, 765 rather than being an essential gene, ABP1 is apparently completely dispensable 766 for normal plant growth and development under lab conditions. Compounding 767 the problem, an isolate of the abp1-5 allele was found to include thousands of 768 polymorphisms compared to the parental genetic background, as well as a 769 chromosomal segment derived from a different background, consistent with 770 errors in the back-crossing regime that followed the isolation of this allele 771 (Enders et al, 2015). As a result, the phenotypic differences between this line and 772 its wild-type previously attributed to the abp1-5 allele may in fact result from 773 other mutations in the background. Together, these results require a major re-774 examination of the evidence supporting a functionally significant role for ABP1, 775 including in endocytosis, cytoskeletal arrangement and ROP modulation. Clean 776 null mutants are now available, and assessment of these auxin responses in the 777 new mutant background will establish whether or not they require ABP1. 778 ABP1 is highly conserved across the plant kingdom, although interestingly it is 779 apparently missing from the Marchantia polymorpha genome (Kato et al, 2015). 780 Nonetheless, this suggests that it confers a significant selective advantage, 781 despite the fact that it is not required for the auxin-regulated processes so far 782 examined, and to the extent to which they have been examined in abp1 null 783 mutants. It may be that either fully parallel systems and/or different auxin 784 response systems regulate the same processes, resulting in functional 785 www.plantphysiol.orgon April 26, 2020 - Published by Downloaded from



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redundancy. This is the case for auxin-regulated root growth described above. 786 Here, the very earliest stages of gravitropic bending depend on auxin-stimulated 787 Ca2+ influx, mediated independently of the TIR1/AFB-Aux/IAA-ARF system. 788 However, the slightly later effects of the TIR1/AFB-Aux/IAA-ARF system on 789 gravitropism all but mask the loss of the non-transcriptional pathway at a 790 macroscopic level. For this response, however, auxin-stimulated Ca2+ influx has 791 been assessed in an abp1 null mutant background and found to be normal (Shih 792 et al, 2015). 793 It is noteworthy that for many of the cell biological responses reported as being 794 ABP1-dependent, associated whole plant level phenotypes have not been 795 examined in much detail and where they have, relatively modest effects are 796 typically reported, despite strong effects reported for the cellular level (Robert et 797 al, 2010; Chen et al, 2014; Baskin, 2015). This is consistent with the idea that 798 these cell biological responses are either not very important at the organismal 799 level, or there is sufficient redundancy in their regulation to mask any 800 morphological effects of ABP1 manipulation. There are, however, some examples 801 of strong morphological effects from perturbed ABP1 levels, including standard 802 ABP1 antisense expression (Braun et al, 2008; Tromas et al, 2009). These 803 experiments involve inducible antisense expression, raising the possibility that 804 sudden changes in ABP1 levels have more significant effects than stable loss of 805 function. This could be consistent with one or more redundant compensating 806 systems requiring time to re-equilibrate in response to ABP1 loss. 807 Whatever the role of ABP1 it is clear that it is not sufficient to explain the known 808 and/or strongly suspected non-transcriptional effects of auxin, for example on 809 root Ca2+ spiking. There must therefore be other auxin perception systems. 810 There are certainly additional biochemically identified auxin binding proteins, 811 although there is very limited evidence that they play any role in auxin responses 812 (Napier and Venis, 1995). Perhaps the best-supported auxin receptor mediating 813 an at least partially non-transcriptional auxin response is the Arabidopsis S-814 Phase Kinase-Associated Protein 2A (SKP2A). SKP2A is an F-box protein with 815 structural similarities to the TIR1 family (Jurado et al, 2008; Jurado et al, 2010). 816 It regulates cell cycle progression by promoting degradation of cell cycle 817



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transcriptional regulators including E2FC and DPB (del Pozo et al, 2006). Auxin 818 has been shown to trigger these degradative events, as well as triggering 819 degradation of SKP2A itself (Jurado, 2010). Structural modeling against TIR1 820 suggested that auxin could bind directly to SKP2A, and this was experimentally 821 validated. Furthermore, mutation of the predicted auxin binding site 822 compromised auxin binding as well as auxin-induced destabilization of SKP2A 823 and interaction with DPB. These data directly link auxin to cell cycle progression 824 and the functional significance of this link is supported by the auxin resistant 825 root growth phenotype of plants in over-expressing SPK2A that is unable to bind 826 auxin. 827 Summary and perspectives 828 Auxin can be considered as a general co-ordinator of growth and development, 829 used and reused throughout the life cycle of plants to mediate communication 830 between cells and tissues at short and long ranges. How this information is 831 decoded at the receiving tissues is unsurprisingly complex. Relevant information 832 is present in the absolute as well as spatially and temporally relative levels of 833 auxin. The appropriate response to all this information depends on myriad other 834 factors, requiring an extensive and highly tunable information processing system 835 in every cell. The TIR1/AFB-Aux/IAA-ARF system provides impressive power to 836 deliver the necessary response properties, but there is mounting evidence that it 837 cannot and does not account for all auxin responses. Additional auxin binding 838 activities, for example mediated by ETTIN and SKP2A, have been linked to 839 specific downstream responses; and specific auxin responses unlikely to be 840 mediated by known auxin reception systems have been identified, such as root 841 Ca2+ transients and root hair positioning. Evolutionary approaches are a 842 promising route for the characterization of these auxin responses, and 843 integration of computational modeling continues to make important 844 contributions. However, limitations in currently available in vivo auxin detection 845 systems are a major constraint on progress. 846 847



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848 849 Figure legend 850 Figure 1: The main pathway for regulation of transcription by auxin 851 Auxin-inducible genes have auxin response elements (AREs) in their promoters, 852 which are bound by dimers of the Auxin Response Factor (ARF) protein family. 853 Gene expression is prevented by recruitment of Aux/IAA transcriptional 854 repressors to these promoters via their interaction with the ARFs. Aux/IAAs 855 recruit TOPLESS family (TPL) co-repressors, which in turn recruit chromatin 856 modifying enzymes (not shown) that stabilize the repressed state. The steps in 857 the auxin response pathway are indicated by the numbered arrows. (1) Auxin 858 acts as a molecular glue bringing together Aux/IAAs and F-box proteins of the 859 TIR1/AFB family. (2) These F-box proteins are part of an SCF-type E3 ubiquitin 860 protein ligase complex that transfers activated ubiquitin (Ub) from an E1/E2 861 enzyme system. (3) Polyubiquitination of the Aux/IAAs results in their 862 degradation. (4) This releases repression at ARE-containing promoters. 863 864 Figure 2: Hypothetical intracellular auxin gradients and root hair position 865 (A) Epidermal cells in trichoblast cell files of the Arabidopsis root produce a root 866 hair toward the rootward end of the cell. This is patterned by a root-tip-high 867 auxin gradient, which is predicted to feed a tip-high intracellular auxin gradient 868 in trichoblasts (blue shading), reinforced by shootward localization of the PIN2 869 auxin exporter (orange line). (B) Triple mutation in aux1 ein2 and gneb flattens 870 the tip-high auxin gradient and presumably also the intracellular auxin gradient. 871 This is associated with shifts in root hair placement. (C) Application of auxin to 872 aux1 ein2 gneb mutants shootward of the root hair differentiation zone shifts the 873 root hair position to the shootward end of the cell, presumably associated with 874 an inverted intracellular auxin gradient. (D) Application of auxin to aux1 ein2 875 gneb mutants rootward of the root hair differentiation zone restores a more wild-876 type root hair position, presumably associated with restoration of the tip-high 877 intracellular auxin gradient. 878 879 880



30

881 882



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http://www.ncbi.nlm.nih.gov/pubmed?term=Heisler MG%2C Ohno C%2C Das P%2C Sieber P%2C Reddy GV%2C Long JA%2C Meyerowitz EM %282005%29 Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem%2E Curr Biol 15%3A 1899%2D1911&dopt=abstract

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Heilser MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jonsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarityand microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoSBiol 8: e1000516


Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, del Pozo C, Reinhardt D, Estelle M. (2003) Arabidopsis AXR6 encodesCUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22: 3314-3325


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Jones MA, Shen J-J, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase Is a Positive Regulator of Both Root HairInitiation and Tip Growth. Plant Cell 14: 763-776


Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis.Proc Natl Acad Sci U S A 103: 1633-1638


Jurado S, Abraham Z, Manzano C, Lopez-Torrejo G, Pacios LF, Del Pozo JC (2010) The Arabidopsis Cell Cycle F-Box Protein SKP2ABinds to Auxin. Plant Cell 22: 3891-3904


Jurado S, Diaz-Trivino S, Abraham Z, Manzano C, Gutierrez C, del Pozo C (2008) SKP2A, an F-box protein that regulates cell division,is degraded via the ubiquitin pathway. Plant J 53: 828-841


Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud JL, Boutry M (2005) Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer. Proc Natl Acad Sci USA 102: 11675-11680


Kato H, Ishizaki K, Kouno M, Shirakawa M, Bowman JL, Nishihama R, Kohchi T (2015) Auxin-mediated transcriptional system with aminimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLoS Genetics 11: e1005084


Klode M, Dahlke RI, Sauter M, Steffens B (2011) Expression and subcellular localization of Arabidopsis thaliana auxin-binding protein 1(ABP1). J Plant Growth Regul 30: 416-424


http://www.ncbi.nlm.nih.gov/pubmed?term=Heilser MG%2C Hamant O%2C Krupinski P%2C Uyttewaal M%2C Ohno C%2C Jonsson H%2C Traas J%2C Meyerowitz EM %282010%29 Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport%2E PLoS Biol 8%3A e1000516&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hellmann H%2C Hobbie L%2C Chapman A%2C Dharmasiri S%2C Dharmasiri N%2C del Pozo C%2C Reinhardt D%2C Estelle M%2E %282003%29 Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis%2E EMBO J 22%3A 3314%2D3325&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M (2009) Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 11: 731-738

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jilkine A%2C Maree A%2C Edelstein%2DKeshet L %282007%29 Mathematical Model for Spatial Segregation of the Rho%2DFamily GTPases Based on Inhibitory Crosstalk%2E Bull Math Biol 69%3A 1943%2D1978&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Jilkine A, Maree A, Edelstein-Keshet L (2007) Mathematical Model for Spatial Segregation of the Rho-Family GTPases Based on Inhibitory Crosstalk. Bull Math Biol 69: 1943-1978

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jones AM%2C Im KH%2C Savka MA%2C Wu MJ%2C DeWitt NG%2C Shillito R%2C Binns AN %281998%29 Auxin%2Ddependent cell expansion mediated by overexpressed auxin%2Dbinding protein 1%2E Science 282%3A 1114%2D1117&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kanczewska J%2C Marco S%2C Vandermeeren C%2C Maudoux O%2C Rigaud JL%2C Boutry M %282005%29 Activation of the plant plasma membrane H%2B%2DATPase by phosphorylation and binding of 14%2D3%2D3 proteins converts a dimer into a hexamer%2E Proc Natl Acad Sci USA 102%3A 11675%2D11680&dopt=abstract

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http://scholar.google.com/scholar?as_q=Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kanczewska&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kato H%2C Ishizaki K%2C Kouno M%2C Shirakawa M%2C Bowman JL%2C Nishihama R%2C Kohchi T %282015%29 Auxin%2Dmediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha%2E PLoS Genetics 11%3A e1005084&dopt=abstract

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Prigge MJ, Greenham K, Zhang Y, Santner A, Castillejo C, Mutka AM, O'Malley RC, Ecker JR, Kunkel BN, Estelle M (2016) TheArabidopsis Auxin Receptor F-Box Proteins AFB4 and AFB5 Are Required for Response to the Synthetic Auxin Picloram. G3 6: 1383-1390


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http://www.ncbi.nlm.nih.gov/pubmed?term=Napier RM %281997%29 Trafficking of the auxin%2Dbinding protein%2E Trends Plant Sci 2%3A 251%2D255&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Robert S%2C Kleine%2DVehn J%2C Barbez E%2C Sauer M%2C Paciorek T%2C Baster P%2C Vanneste S%2C Zhang J%2C Simon S%2C Covanova M%2C Hayashi K%2C Dhonukshe P%2C Yanf Z%2C Bednarek SY%2C Jones AM%2C Luschnig C%2C Aniento F%2C Zazimalova E%2C Friml J %282010%29 ABP1 mediates auxin inhibition of clathrin%2Ddependent endocytosis in Arabidopsis%2E Cell 143%3A 111%2D121&dopt=abstract

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Sauer M, Balla J, Luschnig C, Wisniewska J, Reinöhl V, Friml J, Benková E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependentfeedback regulation of PIN polarity. Genes Dev 20: 2902-2911


Sawchuk MG, Edgar A, Scarpella E (2013). Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet 9:e1003294


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Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC (1997) ETTIN patterns the Arabidopsis floral meristem andreproductive organs. Development 124: 4481-4491


Simonini S, Deb J, Moubayidin L, Stephenson P, Valluru M, Freire-Rios A, Sorefan K, Weijers D, Friml J, Østergaard L (2016) Anoncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes Dev 30: 2286-2296


Shih HW, DePew CL, Miller ND, Monshausen GB (2015) The Cyclic Nucleotide-Gated Channel CNGC14 Regulates Root Gravitropismin Arabidopsis thaliana. Curr Biol 25: 3119-25


Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Ann Rev Plant Biol 55: 555-590Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


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http://www.ncbi.nlm.nih.gov/pubmed?term=Smalle J%2C Vierstra RD %282004%29 The ubiquitin 26S proteasome proteolytic pathway%2E Ann Rev Plant Biol 55%3A 555%2D590&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Smith R%2C Guyomarc%27h S%2C Mandel T%2C Reinhardt D%2C Kuhlemeier C%2C Prusinkiewicz P %282006%29 A plausible model of phyllotaxis%2E Proc Natl Acad Sci USA 103%3A 1301%2D1306&dopt=abstract

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http://scholar.google.com/scholar?as_q=Antibodies to a peptide from the maize auxin-binding protein have auxin agonist activity&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Venis&as_ylo=1992&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Vernoux T%2C Brunoud G%2C Farcot E%2C Morin V%2C Van den Daele H%2C Legrand J%2C Oliva M%2C Das P%2C Larrieu A%2C Wells D%2C Gu�don Y%2C Armitage L%2C Picard F%2C Guyomarch S%2C Cellier C%2C Parry G%2C Koumproglou R%2C Doonan JH%2C Estelle M%2C Godin C%2C Kepinski S%2C Bennett M%2C De Veylder L%2C Traas J %282011%29 The auxin signalling network translates dynamic input into robust patterning at the shoot apex%2E Mol Syst Biol 7%3A 508&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Weyers JDB%2C Paterson NW %282001%29 Plant hormones and the control of physiological processes%2E New Phytol 152%3A 375%2D407&dopt=abstract

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Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rhoGTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143: 99-110


Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusova H, Wang W, Jones AM, Friml J, Patterson SE,Bleecker AB, Yang Z (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025-1028


Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RACGTPases. Plant Physiol 147: 1527-1543


Yamagami M, Haga K, Napier RM, Iino M (2004) Two distinct signaling pathways participate in auxin-induced swelling of pea epidermalprotoplasts. Plant Physiol 134: 735-747


Zenser N, Ellsmore A, Leasure C, Callis J (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci USA 98:11795-11800



http://www.ncbi.nlm.nih.gov/pubmed?term=Wu M%2DF%2C Yamaguchi N%2C Xiao J%2C Bargmann B%2C Estelle M%2C Sang Y%2C Wagner D %282015%29 Auxin%2Dregulated chromatin switch directs acquisition of flower primordium founder fate%2E eLife 4%3A e09269&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Xu T%2C Wen M%2C Nagawa S%2C Fu Y%2C Chen JG%2C Wu MJ%2C Perrot%2DRechenmann C%2C Friml J%2C Jones AM%2C Yang Z %282010%29 Cell surface%2D and rho GTPase%2Dbased auxin signaling controls cellular interdigitation in Arabidopsis%2E Cell 143%3A 99%2D110&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143: 99-110

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

http://scholar.google.com/scholar?as_q=Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis&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=Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Xu T%2C Dai N%2C Chen J%2C Nagawa S%2C Cao M%2C Li H%2C Zhou Z%2C Chen X%2C De Rycke R%2C Rakusova H%2C Wang W%2C Jones AM%2C Friml J%2C Patterson SE%2C Bleecker AB%2C Yang Z %282014%29%2E Cell surface ABP1%2DTMK auxin%2Dsensing complex activates ROP GTPase signaling%2E Science 343%3A1025%2D1028&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusova H, Wang W, Jones AM, Friml J, Patterson SE, Bleecker AB, Yang Z (2014). Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025-1028

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

http://scholar.google.com/scholar?as_q=Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase 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=Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Xu&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yalovsky S%2C Bloch D%2C Sorek N%2C Kost B %282008%29 Regulation of membrane trafficking%2C cytoskeleton dynamics%2C and cell polarity by ROP%2FRAC GTPases%2E Plant Physiol 147%3A 1527%2D1543&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol 147: 1527-1543

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

http://scholar.google.com/scholar?as_q=Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases&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 membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yalovsky&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Yamagami M%2C Haga K%2C Napier RM%2C Iino M %282004%29 Two distinct signaling pathways participate in auxin%2Dinduced swelling of pea epidermal protoplasts%2E Plant Physiol 134%3A 735%2D747&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yamagami M, Haga K, Napier RM, Iino M (2004) Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts. Plant Physiol 134: 735-747

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

http://scholar.google.com/scholar?as_q=Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts&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 distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yamagami&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zenser N%2C Ellsmore A%2C Leasure C%2C Callis J %282001%29 Auxin modulates the degradation rate of Aux%2FIAA proteins%2E Proc Natl Acad Sci USA 98%3A 11795%2D11800&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zenser N, Ellsmore A, Leasure C, Callis J (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci USA 98: 11795-11800

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

http://scholar.google.com/scholar?as_q=Auxin modulates the degradation rate of Aux/IAA proteins&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=Auxin modulates the degradation rate of Aux/IAA proteins&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zenser&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1


Auxin Signaling 2 4 10 - Plant physiology · 64 cellular, tissue, organ and whole plant scales....

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