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Auxin regulates aquaporin function to facilitate lateral root emergence

Nature Cell Biology volume 14, pages 991–998 (2012)Cite this article

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Abstract

Aquaporins are membrane channels that facilitate water movement across cell membranes. In plants, aquaporins contribute to water relations. Here, we establish a new link between aquaporin-dependent tissue hydraulics and auxin-regulated root development in Arabidopsis thaliana. We report that most aquaporin genes are repressed during lateral root formation and by exogenous auxin treatment. Auxin reduces root hydraulic conductivity both at the cell and whole-organ levels. The highly expressed aquaporin PIP2;1 is progressively excluded from the site of the auxin response maximum in lateral root primordia (LRP) whilst being maintained at their base and underlying vascular tissues. Modelling predicts that the positive and negative perturbations of PIP2;1 expression alter water flow into LRP, thereby slowing lateral root emergence (LRE). Consistent with this mechanism, pip2;1 mutants and PIP2;1-overexpressing lines exhibit delayed LRE. We conclude that auxin promotes LRE by regulating the spatial and temporal distribution of aquaporin-dependent root tissue water transport.

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Figure 1: Transcriptional downregulation of aquaporins during lateral root formation is mediated by auxin.
Figure 2: Auxin reduces aquaporin accumulation and hydraulic conductivity.
Figure 3: PIP2;1 expression oppositely mirrors auxin accumulation during lateral root formation.
Figure 4: Mathematical model of LRE.
Figure 5: LRE is delayed in the pip2;1 mutant and the PIP2;1 overexpressor.
Figure 6: Diagram illustrating the regulation of LRE by PIP2;1.

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Acknowledgements

This work was supported by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme PIEF-GA-2008-220506 (B.P.) and by a Grand Federative Project (Rhizopolis) of the Agropolis Fondation (Montpellier, France) to C.M. We are indebted to H. Scherb (Helmholtz Zentrum München) for his help with statistical analyses. L.R.B., U.V., M.L., D.M.W., J.R.K., O.E.J. and M.J.B. acknowledge the support of the Biotechnology and Biological Sciences Research Council (BBSRC) and Engineering and Physical Sciences Research Council (EPSRC) funding to the Centre for Plant Integrative Biology (CPIB), BBSRC responsive mode grant support to U.V., L.R.B. and M.J.B. and the BBSRC Professorial Research Fellowship funding to D.M.W. and M.J.B. A.R.S. and O.D.I. acknowledge the support of the Deutsche Forschungsgemeinschaft priority programme SPP1108 (SCHA 454/8).

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Author notes

  1. Benjamin Péret, Doan-Trung Luu & Olivier Da Ines

    Present address: Present addresses: Unité Mixte de Recherche 7265 Commissariat à l’Energie Atomique et aux Energies Alternatives, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement des Plantes, Université d’Aix-Marseille, 13108 Saint-Paul-lez-Durance, France (B.P.); Université des Sciences et Techniques de Hanoï, Institut de Recherche pour le Développement Laboratoire Mixte International Rice, Agronomical Genetics Institute, Ha Noi, Vietnam (D-T.L.); Génétique, Reproduction et Développement, Unité Mixte de Recherche 6293 Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale U1103, Université de Clermont-Ferrand, Aubière 63170, France (O.D.I.),

  2. Benjamin Péret, Guowei Li, Jin Zhao and Leah R. Band: These authors contributed equally to this work

Authors and Affiliations

  1. Centre for Plant Integrative Biology, University of Nottingham, LE12 5RD, UK

    Benjamin Péret, Leah R. Band, Ute Voß, Mikaël Lucas, Darren M. Wells, Laure Lazzerini, John R. King, Oliver E. Jensen & Malcolm J. Bennett

  2. Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes, Unité Mixte de Recherche 5004 Centre National de la Recherche Scientifique - Unité Mixte de Recherche 0386 Institut National de la Recherche Agronomique - MontpellierSupAgro - Université Montpellier 2, 2 Place Viala, F-34060 Montpellier Cedex 2, France

    Guowei Li, Olivier Postaire, Doan-Trung Luu, Philippe Nacry & Christophe Maurel

  3. Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, 85764 Neuherberg, Germany

    Jin Zhao, Olivier Da Ines & Anton R. Schäffner

  4. Universidad de Extremadura, Facultad de Ciencias, Badajoz 06006, Spain

    Ilda Casimiro

  5. School of Mathematics, University of Manchester, M13 9PL, UK

    Oliver E. Jensen

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Contributions

B.P., G.L., J.Z., U.V., O.P., D-T.L., O.D.I., I.C., M.L., D.M.W., L.L. and P.N. performed experimental work; B.P., G.L., J.Z., L.R.B., J.R.K., O.E.J., A.R.S., C.M. and M.J.B. performed data analysis; B.P., L.R.B., J.R.K., O.E.J., A.R.S., C.M. and M.J.B. oversaw project planning; B.P., L.R.B., A.R.S., C.M. and M.J.B. wrote the paper.

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Correspondence to Anton R. Schäffner, Christophe Maurel or Malcolm J. Bennett.

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Péret, B., Li, G., Zhao, J. et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 14, 991–998 (2012). https://doi.org/10.1038/ncb2573

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