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      Out of Shape During Stress: A Key Role for Auxin

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          Abstract

          In most abiotic stress conditions, including salinity and water deficit, the developmental plasticity of the plant root is regulated by the phytohormone auxin. Changes in auxin concentration are often attributed to changes in shoot-derived long-distance auxin flow. However, recent evidence suggests important contributions by short-distance auxin transport from local storage and local auxin biosynthesis, conjugation, and oxidation during abiotic stress. We discuss here current knowledge on long-distance auxin transport in stress responses, and subsequently debate how short-distance auxin transport and indole-3-acetic acid (IAA) metabolism play a role in influencing eventual auxin accumulation and signaling patterns. Our analysis stresses the importance of considering all these components together and highlights the use of mathematical modeling for predictions of plant physiological responses.

          Highlights

          Recent findings in active auxin transport over organelle membranes and the influence of apoplastic and cytosolic pH on passive auxin flow into the cell highlight the importance of short-distance auxin transport for local auxin maxima in roots exposed to stress.

          Based on previously published gene expression data, we have identified stress-induced expression patterns of IAA biosynthesis and conjugation genes in the root that could be relevant for IAA accumulation patterns. These results underscore the importance of incorporating IAA homeostasis into models predicting auxin levels and flow.

          Recent advances in mathematical models involving auxin-related processes highlight the value of combining in planta and in silico experiments when unraveling complex hormonal changes in plants.

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          Most cited references61

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          TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.

          Plants have evolved a tremendous ability to respond to environmental changes by adapting their growth and development. The interaction between hormonal and developmental signals is a critical mechanism in the generation of this enormous plasticity. A good example is the response to the hormone ethylene that depends on tissue type, developmental stage, and environmental conditions. By characterizing the Arabidopsis wei8 mutant, we have found that a small family of genes mediates tissue-specific responses to ethylene. Biochemical studies revealed that WEI8 encodes a long-anticipated tryptophan aminotransferase, TAA1, in the essential, yet genetically uncharacterized, indole-3-pyruvic acid (IPA) branch of the auxin biosynthetic pathway. Analysis of TAA1 and its paralogues revealed a link between local auxin production, tissue-specific ethylene effects, and organ development. Thus, the IPA route of auxin production is key to generating robust auxin gradients in response to environmental and developmental cues.
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            Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid.

            Substantial evidence indicates that amino acid conjugates of indole-3-acetic acid (IAA) function in auxin homeostasis, yet the plant enzymes involved in their biosynthesis have not been identified. We tested whether several Arabidopsis thaliana enzymes that are related to the auxin-induced soybean (Glycine max) GH3 gene product synthesize IAA-amino acid conjugates. In vitro reactions with six recombinant GH3 enzymes produced IAA conjugates with several amino acids, based on thin layer chromatography. The identity of the Ala, Asp, Phe, and Trp conjugates was verified by gas chromatography-mass spectrometry. Insertional mutations in GH3.1, GH3.2, GH3.5, and GH3.17 resulted in modestly increased sensitivity to IAA in seedling root. Overexpression of GH3.6 in the activation-tagged mutant dfl1-D did not significantly alter IAA level but resulted in 3.2- and 4.5-fold more IAA-Asp than in wild-type seedlings and mature leaves, respectively. In addition to IAA, dfl1-D was less sensitive to indole-3-butyric acid and naphthaleneacetic acid, consistent with the fact that GH3.6 was active on each of these auxins. By contrast, GH3.6 and the other five enzymes tested were inactive on halogenated auxins, and dfl1-D was not resistant to these. This evidence establishes that several GH3 genes encode IAA-amido synthetases, which help to maintain auxin homeostasis by conjugating excess IAA to amino acids.
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              Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.

              Plants grown at high densities perceive a decrease in the red to far-red (R:FR) ratio of incoming light, resulting from absorption of red light by canopy leaves and reflection of far-red light from neighboring plants. These changes in light quality trigger a series of responses known collectively as the shade avoidance syndrome. During shade avoidance, stems elongate at the expense of leaf and storage organ expansion, branching is inhibited, and flowering is accelerated. We identified several loci in Arabidopsis, mutations in which lead to plants defective in multiple shade avoidance responses. Here we describe TAA1, an aminotransferase, and show that TAA1 catalyzes the formation of indole-3-pyruvic acid (IPA) from L-tryptophan (L-Trp), the first step in a previously proposed, but uncharacterized, auxin biosynthetic pathway. This pathway is rapidly deployed to synthesize auxin at the high levels required to initiate the multiple changes in body plan associated with shade avoidance.
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                Author and article information

                Contributors
                Journal
                Trends Plant Sci
                Trends Plant Sci
                Trends in Plant Science
                Elsevier Science, Ltd
                1360-1385
                1878-4372
                1 September 2018
                September 2018
                : 23
                : 9
                : 783-793
                Affiliations
                [1 ]University of Amsterdam, Plant Cell Biology, Swammerdam Institute for Life Sciences, 1090GE Amsterdam, The Netherlands
                [2 ]Laboratory of Plant Physiology, 6708PB Wageningen University and Research, Wageningen, The Netherlands
                Author notes
                Article
                S1360-1385(18)30129-8
                10.1016/j.tplants.2018.05.011
                6121082
                29914722
                88db9325-1d1b-4a38-9a12-419df0e34f9d
                © 2018 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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                Categories
                Article

                Plant science & Botany
                auxin,auxin transport,iaa homeostasis,abiotic stress,mathematical modeling,root phenotypic plasticity

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