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Auxin methylation is required for differential growth in Arabidopsis

Mohamad Abbas, Jorge Hernández-García, Stephan Pollmann, Sophia L. Samodelov, Martina Kolb, Jiří Friml, Ulrich Z. Hammes, Matias D. Zurbriggen, Miguel A. Blázquez, and David Alabadí
PNAS June 26, 2018 115 (26) 6864-6869; published ahead of print June 13, 2018 https://doi.org/10.1073/pnas.1806565115
Mohamad Abbas
aInstituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, 46022 Valencia, Spain;bInstitute of Science and Technology Austria, 3400 Klosterneuburg, Austria;
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Jorge Hernández-García
aInstituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, 46022 Valencia, Spain;
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  • ORCID record for Jorge Hernández-García
Stephan Pollmann
cCentro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid–Instituto Nacional de Investigación y Tecnología Agraria y Alimentación, 28223 Pozuelo de Alarcón, Spain;
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Sophia L. Samodelov
dInstitute of Synthetic Biology and Cluster of Excellence in Plant Sciences, University of Düsseldorf, 40225 Düsseldorf, Germany;eSpemann Graduate School of Biology and Medicine, University of Freiburg, 79085 Freiburg, Germany;
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Martina Kolb
fDepartment of Cell Biology and Biochemistry, Regensburg University, 93053 Regensburg, Germany
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Jiří Friml
bInstitute of Science and Technology Austria, 3400 Klosterneuburg, Austria;
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Ulrich Z. Hammes
fDepartment of Cell Biology and Biochemistry, Regensburg University, 93053 Regensburg, Germany
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Matias D. Zurbriggen
dInstitute of Synthetic Biology and Cluster of Excellence in Plant Sciences, University of Düsseldorf, 40225 Düsseldorf, Germany;
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Miguel A. Blázquez
aInstituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, 46022 Valencia, Spain;
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  • For correspondence: mblazquez@ibmcp.upv.es
David Alabadí
aInstituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas–Universidad Politécnica de Valencia, 46022 Valencia, Spain;
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  1. Edited by Ottoline Leyser, University of Cambridge, Cambridge, United Kingdom, and approved May 21, 2018 (received for review April 16, 2018)

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Significance

Auxin is a plant hormone required for the establishment of growth orientation. Redistribution of auxin across an organ allows reorientation, and this is achieved through changes in the polar localization of auxin efflux carriers. We have found that when auxin methylation is impaired, auxin is not correctly redistributed on gravistimulation, due to a general increase in basipetal auxin transport and deficient relocalization of auxin transporters. We conclude that auxin must be within a specific concentration range for its correct distribution, and this range is maintained by auxin methylation in the endodermis, the cell type that perceives gravity.

Abstract

Asymmetric auxin distribution is instrumental for the differential growth that causes organ bending on tropic stimuli and curvatures during plant development. Local differences in auxin concentrations are achieved mainly by polarized cellular distribution of PIN auxin transporters, but whether other mechanisms involving auxin homeostasis are also relevant for the formation of auxin gradients is not clear. Here we show that auxin methylation is required for asymmetric auxin distribution across the hypocotyl, particularly during its response to gravity. We found that loss-of-function mutants in Arabidopsis IAA CARBOXYL METHYLTRANSFERASE1 (IAMT1) prematurely unfold the apical hook, and that their hypocotyls are impaired in gravitropic reorientation. This defect is linked to an auxin-dependent increase in PIN gene expression, leading to an increased polar auxin transport and lack of asymmetric distribution of PIN3 in the iamt1 mutant. Gravitropic reorientation in the iamt1 mutant could be restored with either endodermis-specific expression of IAMT1 or partial inhibition of polar auxin transport, which also results in normal PIN gene expression levels. We propose that IAA methylation is necessary in gravity-sensing cells to restrict polar auxin transport within the range of auxin levels that allow for differential responses.

  • hormone regulation
  • auxin metabolism
  • homeostasis
  • gravitropism

Footnotes

  • ↵1Present address: Plant and Crop Science, University of Nottingham, Loughborough LE12 5RD, United Kingdom.

  • ↵2Present address: Department of Clinical Pharmacology and Toxicology, University Hospital Zurich, University of Zurich, 8091 Zurich, Switzerland.

  • ↵3Present address: Plant Systems Biology, Technical University of Munich, 85354 Freising, Germany.

  • ↵4To whom correspondence should be addressed. Email: mblazquez{at}ibmcp.upv.es.
  • Author contributions: M.A., J.F., U.Z.H., M.D.Z., M.A.B., and D.A. designed research; M.A., J.H.-G., S.P., S.L.S., and M.K. performed research; M.A., J.H.-G., S.P., S.L.S., M.K., J.F., U.Z.H., M.D.Z., M.A.B., and D.A. analyzed data; and M.A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1806565115/-/DCSupplemental.

Published under the PNAS license.

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Auxin methylation is required for differential growth in Arabidopsis
Mohamad Abbas, Jorge Hernández-García, Stephan Pollmann, Sophia L. Samodelov, Martina Kolb, Jiří Friml, Ulrich Z. Hammes, Matias D. Zurbriggen, Miguel A. Blázquez, David Alabadí
Proceedings of the National Academy of Sciences Jun 2018, 115 (26) 6864-6869; DOI: 10.1073/pnas.1806565115

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Auxin methylation is required for differential growth in Arabidopsis
Mohamad Abbas, Jorge Hernández-García, Stephan Pollmann, Sophia L. Samodelov, Martina Kolb, Jiří Friml, Ulrich Z. Hammes, Matias D. Zurbriggen, Miguel A. Blázquez, David Alabadí
Proceedings of the National Academy of Sciences Jun 2018, 115 (26) 6864-6869; DOI: 10.1073/pnas.1806565115
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