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      TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls

      research-article
      1 , 2 , 1 , *
      eLife
      eLife Sciences Publications, Ltd
      auxin, growth, cell wall, hypocotyl, A. thaliana

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          Abstract

          Despite being composed of immobile cells, plants reorient along directional stimuli. The hormone auxin is redistributed in stimulated organs leading to differential growth and bending. Auxin application triggers rapid cell wall acidification and elongation of aerial organs of plants, but the molecular players mediating these effects are still controversial. Here we use genetically-encoded pH and auxin signaling sensors, pharmacological and genetic manipulations available for Arabidopsis etiolated hypocotyls to clarify how auxin is perceived and the downstream growth executed. We show that auxin-induced acidification occurs by local activation of H +-ATPases, which in the context of gravity response is restricted to the lower organ side. This auxin-stimulated acidification and growth require TIR1/AFB-Aux/IAA nuclear auxin perception. In addition, auxin-induced gene transcription and specifically SAUR proteins are crucial downstream mediators of this growth. Our study provides strong experimental support for the acid growth theory and clarified the contribution of the upstream auxin perception mechanisms.

          DOI: http://dx.doi.org/10.7554/eLife.19048.001

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          Most cited references54

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          NIH Image to ImageJ: 25 years of image analysis.

          For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the analysis of scientific images. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.
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            Local, efflux-dependent auxin gradients as a common module for plant organ formation.

            Plants, compared to animals, exhibit an amazing adaptability and plasticity in their development. This is largely dependent on the ability of plants to form new organs, such as lateral roots, leaves, and flowers during postembryonic development. Organ primordia develop from founder cell populations into organs by coordinated cell division and differentiation. Here, we show that organ formation in Arabidopsis involves dynamic gradients of the signaling molecule auxin with maxima at the primordia tips. These gradients are mediated by cellular efflux requiring asymmetrically localized PIN proteins, which represent a functionally redundant network for auxin distribution in both aerial and underground organs. PIN1 polar localization undergoes a dynamic rearrangement, which correlates with establishment of auxin gradients and primordium development. Our results suggest that PIN-dependent, local auxin gradients represent a common module for formation of all plant organs, regardless of their mature morphology or developmental origin.
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              Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis.

              Long-standing models propose that plant growth responses to light or gravity are mediated by asymmetric distribution of the phytohormone auxin. Physiological studies implicated a specific transport system that relocates auxin laterally, thereby effecting differential growth; however, neither the molecular components of this system nor the cellular mechanism of auxin redistribution on light or gravity perception have been identified. Here, we show that auxin accumulates asymmetrically during differential growth in an efflux-dependent manner. Mutations in the Arabidopsis gene PIN3, a regulator of auxin efflux, alter differential growth. PIN3 is expressed in gravity-sensing tissues, with PIN3 protein accumulating predominantly at the lateral cell surface. PIN3 localizes to the plasma membrane and to vesicles that cycle in an actin-dependent manner. In the root columella, PIN3 is positioned symmetrically at the plasma membrane but rapidly relocalizes laterally on gravity stimulation. Our data indicate that PIN3 is a component of the lateral auxin transport system regulating tropic growth. In addition, actin-dependent relocalization of PIN3 in response to gravity provides a mechanism for redirecting auxin flux to trigger asymmetric growth.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                14 September 2016
                2016
                : 5
                : e19048
                Affiliations
                [1 ]Institute of Science and Technology Austria , Klosterneuburg, Austria
                [2 ]deptInstitut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech , INRA - Centre de Versailles-Grignon, Saclay Plant Science , Versailles, France
                [3]University of Missouri , United States
                [4]University of Missouri , United States
                Author notes
                Author information
                http://orcid.org/0000-0002-8302-7596
                Article
                19048
                10.7554/eLife.19048
                5045290
                27627746
                4a3d1194-7d8e-45b7-8f83-afb2dfcd3604
                © 2016, Fendrych et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 22 June 2016
                : 13 September 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: project ERC-2011-StG-20101109-PSDP
                Award Recipient :
                Funded by: Marie Curie Actions FP7 2007-2013;
                Award ID: REA grant agreement n.291734
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Cell Biology
                Plant Biology
                Research Article
                Custom metadata
                2.5
                The nuclear pathway for auxin perception is responsible for the rapid auxin-induced cell wall acidification and growth of aerial organs of plants.

                Life sciences
                auxin,growth,cell wall,hypocotyl,a. thaliana
                Life sciences
                auxin, growth, cell wall, hypocotyl, a. thaliana

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