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      Transcription of TIR1-Controlled Genes Can be Regulated within 10 Min by an Auxin-Induced Process. Can TIR1 be the Receptor?

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          Abstract

          ABP1 and TIR1/AFBs are known as auxin receptors. ABP1 is linked to auxin responses several of which are faster than 10 min. TIR1 regulates auxin-induced transcription of early auxin genes also within minutes. We use transcription of such TIR1-dependent genes as indicator of TIR1 activity to show the rapid regulation of TIR1 by exogenous auxin. To this end, we used quantification of transcription of a set of fifteen early auxin-induced reporter genes at t = 10 and t = 30 min to measure this as a TIR1-dependent auxin response. We conducted this study in 22 mutants of auxin transporters ( pin5, abcb1, abcb19, and aux1/lax3), protein kinases and phosphatases ( ibr5, npr1, cpk3, CPK3-OX, d6pk1, d6pkl1-1, d6pkl3-2, d6pkl1-1/d6pkl2-2, and d6pkl1-1/d6pkl3-2), of fatty acid metabolism ( fad2-1, fad6-1, ssi2, lacs4, lacs9, and lacs4/lacs9) and receptors ( tir1, tir1/afb2, and tir1/afb3) and compared them to the wild type. After 10 min auxin application, in 18 out of 22 mutants mis-regulated expression of at least one reporter was found, and in 15 mutants transcription of two-to-three out of five selected auxin reporter genes was mis-regulated. After 30 min of auxin application to mutant plants, mis-regulation of reporter genes ranged from one to 13 out of 15 tested reporter genes. Those genes chosen as mutants were themselves not regulated in their expression by auxin for at least 1 h, excluding an influence of TIR1/AFBs on their transcription. The expression of TIR1/AFB genes was also not modulated by auxin for up to 3 h. Together, this excludes a feedback or feedforward of these mutant genes/proteins on TIR1/AFBs output of transcription in this auxin-induced response. However, an auxin-induced response needed an as yet unknown auxin receptor. We suggest that the auxin receptor necessary for the fast auxin-induced transcription modulation could be, instead, ABP1. The alternative hypothesis would be that auxin-induced expression of a protein, initiated by TIR1/AFBs receptors, could initiate these responses and that this unknown protein regulated TIR1/AFB activities within 10 min.

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          Most cited references52

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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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            Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses.

            Small-molecule hormones govern every aspect of the biology of plants. Many processes, such as growth, are regulated in similar ways by multiple hormones, and recent studies have revealed extensive crosstalk among different hormonal signaling pathways. These results have led to the proposal that a common set of signaling components may integrate inputs from multiple hormones to regulate growth. In this study, we tested this proposal by asking whether different hormones converge on a common set of transcriptional targets in Arabidopsis seedlings. Using publicly available microarray data, we analyzed the transcriptional effects of seven hormones, including abscisic acid, gibberellin, auxin, ethylene, cytokinin, brassinosteroid, and jasmonate. A high-sensitivity analysis revealed a surprisingly low number of common target genes. Instead, different hormones appear to regulate distinct members of protein families. We conclude that there is not a core transcriptional growth-regulatory module in young Arabidopsis seedlings.
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              Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression.

              Plant development displays an exceptional plasticity and adaptability that involves the dynamic, asymmetric distribution of the phytohormone auxin. Polar auxin flow, which requires polarly localized transport facilitators of the PIN family, largely contributes to the establishment and maintenance of the auxin gradients. Functionally overlapping action of PIN proteins mediates multiple developmental processes, including embryo formation, organ development and tropisms. Here we show that PIN proteins exhibit synergistic interactions, which involve cross-regulation of PIN gene expression in pin mutants or plants with inhibited auxin transport. Auxin itself positively feeds back on PIN gene expression in a tissue-specific manner through an AUX/IAA-dependent signalling pathway. This regulatory switch is indicative of a mechanism by which the loss of a specific PIN protein is compensated for by auxin-dependent ectopic expression of its homologues. The compensatory properties of the PIN-dependent transport network might enable the stabilization of auxin gradients and potentially contribute to the robustness of plant adaptive development.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 July 2016
                2016
                : 7
                : 995
                Affiliations
                [1] 1Abteilung Molekulare Ertragsphysiologie, Institut für Gartenbauliche Produktionssysteme, Leibniz Universität Hannover Hannover, Germany
                [2] 2Department of Biology, University of Al Azhar Indonesia Jakarta, Indonesia
                [3] 3Abteilung Biochemie der Pflanzen, Albrecht-von-Haller-Institut der Pflanzenwissenschaften, Universität Göttingen Göttingen, Germany
                Author notes

                Edited by: Irene Murgia, Università degli Studi di Milano, Italy

                Reviewed by: Alex Levine, Hadassah Medical School, Israel; Jutta Ludwig-Müller, Technische Universität Dresden, Germany

                *Correspondence: Günther F. E. Scherer, scherer@ 123456zier.uni-hannover.de

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2016.00995
                4939301
                27462327
                e8c781ad-15fc-4fcd-91b8-79e750b85bf6
                Copyright © 2016 Labusch, Effendi, Fulda and Scherer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 25 February 2016
                : 22 June 2016
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 63, Pages: 13, Words: 0
                Funding
                Funded by: Deutsches Zentrum für Luft- und Raumfahrt 10.13039/501100002946
                Award ID: 50WB1333
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Award ID: Sche207/24-1
                Funded by: Gottfried Wilhelm Leibniz Universität Hannover 10.13039/501100004115
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                auxin-binding protein 1,early auxin-induced genes,auxin transport mutants,auxin receptor mutants,fatty acid-metabolism mutants,protein kinase mutants,protein phosphatase mutants,transport inhibitor response 1

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