A hallmark of plants is their adaptability of size and form in response to widely fluctuating environments. The metabolism and redistribution of the phytohormone auxin play pivotal roles in establishing active auxin gradients and resulting cellular differentiation. In Arabidopsis thaliana, cotyledons and leaves synthesize indole-3-acetic acid (IAA) from tryptophan through indole-3-pyruvic acid (3-IPA) in response to vegetational shade. This newly synthesized auxin moves to the hypocotyl where it induces elongation of hypocotyl cells. Here we show that loss of function of VAS2 (IAA-amido synthetase Gretchen Hagen 3 (GH3).17) leads to increases in free IAA at the expense of IAA-Glu (IAA-glutamate) in the hypocotyl epidermis. This active IAA elicits shade- and high temperature-induced hypocotyl elongation largely independently of 3-IPA-mediated IAA biosynthesis in cotyledons. Our results reveal an unexpected capacity of local auxin metabolism to modulate the homeostasis and spatial distribution of free auxin in specialized organs such as hypocotyls in response to shade and high temperature.

Howard Hughes Medical Institute and Plant Biology Laboratory The Salk Institute for Biological Studies La Jolla California 92037 USA

Howard Hughes Medical Institute and The Jack H Skirball Center for Chemical Biology and Proteomics The Salk Institute for Biological Studies La Jolla California 92037 USA Czech Republic

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany ASCR Šlechtielů 11 783 71 Olomouc Czech Republic

Plant Biology Laboratory The Salk Institute for Biological Studies La Jolla California 92037 USA

The Jack H Skirball Center for Chemical Biology and Proteomics The Salk Institute for Biological Studies La Jolla California 92037 USA

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences SE 901 83 Umeå Sweden

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Nat Plants. 2016 Apr 05;2:16044. doi: 10.1038/nplants.2016.44. PubMed

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Franklin KA. Shade avoidance. New Phytol. 2008;179:930–944. PubMed

Casal JJ. Shade avoidance. Arabidopsis Book. 2012;10:e0157. PubMed PMC

Li L, et al. Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 2012;26:785–790. PubMed PMC

Tao Y, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 2008;133:164–176. PubMed PMC

de Wit M, Lorrain S, Fankhauser C. Auxin-mediated plant architectural changes in response to shade and high temperature. Physiol Plant. 2014;151:13–24. PubMed

Stepanova AN, et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–191. PubMed

Sun J, Qi L, Li Y, Chu J, Li C. PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. 2012;8:e1002594. PubMed PMC

Keuskamp DH, Pollmann S, Voesenek LA, Peeters AJ, Pierik R. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc Natl Acad Sci USA. 2010;107:22740–22744. PubMed PMC

Franklin KA, et al. Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA. 2011;108:20231–20235. PubMed PMC

Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M. The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol. 2009;151:168–179. PubMed PMC

Procko C, Crenshaw CM, Ljung K, Noel JP, Chory J. Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa. Plant Physiol. 2014;165:1285–1301. PubMed PMC

Petrasek J, Friml J. Auxin transport routes in plant development. Development. 2009;136:2675–2688. PubMed

Zheng Z, et al. Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nature Chem Biol. 2013;9:244–246. PubMed PMC

Hagen G, Kleinschmidt A, Guilfoyle T. Auxin-regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta. 1984;162:147–153. PubMed

Staswick PE, et al. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 2005;17:616–627. PubMed PMC

Westfall CS, Herrmann J, Chen Q, Wang S, Jez JM. Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal Behav. 2010;5:1607–1612. PubMed PMC

Ludwig-Muller J. Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot. 2011;62:1757–1773. PubMed

Korasick DA, Enders TA, Strader LC. Auxin biosynthesis and storage forms. J Exp Bot. 2013;64:2541–2555. PubMed PMC

Morant M, et al. Metabolomic, transcriptional, hormonal, and signaling crosstalk in superroot2. Mol Plant. 2010;3:192–211. PubMed PMC

Paponov IA, et al. Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant. 2008;1:321–337. PubMed

Terol J, Domingo C, Talon M. The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene. 2006;371:279–290. PubMed

Novak O, et al. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 2012;72:523–536. PubMed

Ljung K. Auxin metabolism and homeostasis during plant development. Development. 2013;140:943–950. PubMed

Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot. 2005;95:707–735. PubMed PMC

Rampey RA, et al. A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 2004;135:978–988. PubMed PMC

LeClere S, Tellez R, Rampey RA, Matsuda SP, Bartel B. Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem. 2002;277:20446–20452. PubMed

Sauer M, Robert S, Kleine-Vehn J. Auxin: simply complicated. J Exp Bot. 2013;64:2565–2577. PubMed

Kim JY, et al. Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J Biol Chem. 2010;285:23309–23317. PubMed PMC

Pencik A, et al. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell. 2013;25:3858–3870. PubMed PMC

Khan S, Stone JM. Arabidopsis thaliana GH3.9 influences primary root growth. Planta. 2007;226:21–34. PubMed

Westfall CS, et al. Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science. 2012;336:1708–1711. PubMed

Yuan H, et al. Genome-wide analysis of the GH3 family in apple (Malus × domestica) BMC Genomics. 2013;14:297. PubMed PMC

Fu J, Yu H, Li X, Xiao J, Wang S. Rice GH3 gene family: regulators of growth and development. Plant Signal Behav. 2011;6:570–574. PubMed PMC

Khan S, Stone JM. Arabidopsis thaliana GH3.9 in auxin and jasmonate cross talk. Plant Signal Behav. 2007;2:483–485. PubMed PMC

Mittag J, Gabrielyan A, Ludwig-Muller J. Knockout of GH3 genes in the moss Physcomitrella patens leads to increased IAA levels at elevated temperature and in darkness. Plant Physiol Biochem. 2015;97:339–349. PubMed

Jagadeeswaran G, et al. Arabidopsis GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J. 2007;51:234–246. PubMed

Takase T, Nakazawa M, Ishikawa A, Manabe K, Matsui M. DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation. Plant Cell Physiol. 2003;44:1071–1080. PubMed

Nakazawa M, et al. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J. 2001;25:213–221. PubMed

Santner A, Calderon-Villalobos LI, Estelle M. Plant hormones are versatile chemical regulators of plant growth. Nature Chem Biol. 2009;5:301–307. PubMed

Nemhauser JL, Hong F, Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006;126:467–475. PubMed

Zhao Y. Auxin biosynthesis. Arabidopsis Book. 2014;12:e0173. PubMed PMC

van Berkel K, de Boer RJ, Scheres B, ten Tusscher K. Polar auxin transport: models and mechanisms. Development. 2013;140:2253–2268. PubMed

Blilou I, et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005;433:39–44. PubMed

Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature. 2007;449:1008–1013. PubMed

Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B. Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA. 2013;110:1107–1112. PubMed PMC

Mravec J, et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009;459:1136–1140. PubMed

Barbez E, et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 2012;485:119–122. PubMed

Morgan DC, O’Brien T, Smith H. Rapid photomodulation of stem extension in light-grown Sinapis alba L.: studies on kinetics, site of perception and photoreceptor. Planta. 1980;150:95–101. PubMed

Preuten T, Hohm T, Bergmann S, Fankhauser C. Defining the site of light perception and initiation of phototropism in Arabidopsis. Curr Biol. 2013;23:1934–1938. PubMed

Yamamoto Y, et al. Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol. 2014;55:1206–1215. PubMed PMC

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