Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors

Nature Cell Biology volume 14, pages80–86(2012)Cite this article

Abstract

Polarized tip growth is a fundamental cellular process in many eukaryotic organisms, mediating growth of neuronal axons and dendrites1 or fungal hyphae2. In plants, pollen and root hairs are cellular model systems for analysing tip growth3,4,5. Cell growth depends on membrane traffic. The regulation of this membrane traffic is largely unknown for tip-growing cells, in contrast to cells exhibiting intercalary growth. Here we show that in Arabidopsis, GBF1-related exchange factors for the ARF GTPases (ARF GEFs) GNOM and GNL2 play essential roles in polar tip growth of root hairs and pollen, respectively. When expressed from the same promoter, GNL2 (in contrast to the early-secretory ARF GEF GNL1) is able to replace GNOM in polar recycling of the auxin efflux regulator PIN1 from endosomes to the basal plasma membrane in non-tip growing cells. Thus, polar recycling facilitates polar tip growth, and GNL2 seems to have evolved to meet the specific requirement of fast-growing pollen in higher plants.

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Figure 1: Polarized tip growth depends on BFA-sensitive GBF1-related ARF GEFs.
Figure 2: Functional relationship of GBF-related ARF GEFs.
Figure 3: GNL2 mediates polar localization of pectin in pollen grains and pollen tubes.
Figure 4: Localized depositions of pectin in the intine layer are dependent on GNL2 action.
Figure 5: GNL2 is required for polar organization of the pollen tube.

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Acknowledgements

We thank J. Keicher, R. Gavidia and B. Maier for technical assistance, C. Knöll for formatting of data files, D. G. Robinson and S. McCormick for providing materials and members of the laboratory for critical reading of the manuscript. This work was financially supported by the Deutsche Forschungsgemeinschaft through SFB 446 (TP A9).

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Author notes

  1. Lena M. Müller & Niko Geldner

    Present address: Present addresses: Institute of Plant Biology, University of Zürich, 8008 Zürich, Switzerland (L.M.M.); DBMV, Université de Lausanne, UNIL-Sorge, 1015 Lausanne, Switzerland (N.G.),

Affiliations

  1. ZMBP, Entwicklungsgenetik, Universität Tübingen, Auf der Morgenstelle 3, 72076 Tübingen, Germany

    Sandra Richter, Lena M. Müller, Ulrike Mayer, Nozomi Takada, Anne Vieten, Niko Geldner & Gerd Jürgens

  2. ZMBP, Mikroskopie, Universität Tübingen, Auf der Morgenstelle 5, 72076 Tübingen, Germany

    York-Dieter Stierhof & Ulrike Mayer

  3. Department of Biology, Cell Biology, University of Erlangen-Nürnberg, 91058 Erlangen, Germany

    Benedikt Kost

  4. Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, 50829 Köln, Germany

    Csaba Koncz

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Contributions

S.R. and G.J. planned the experiments. S.R. carried out most of the experiments. L.M.M. did the analysis of pollen germination. N.T. cloned some GNL2 constructs. Y.D.S. and U.M. carried out electron microscopy and assisted in light microscopy. C.K. isolated the gnl2 mutant and A.V. did initial work on gnl2. B.K. cloned the Hypo2 construct. N.G. initiated the project. All authors analysed and discussed the data; S.R. and G.J. wrote the paper.

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Correspondence to Gerd Jürgens.

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Richter, S., Müller, L., Stierhof, YD. et al. Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat Cell Biol 14, 80–86 (2012). https://doi.org/10.1038/ncb2389

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