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Functional diversification of closely related ARF-GEFs in protein secretion and recycling

Nature volume 448, pages 488–492 (2007)Cite this article

Abstract

Guanine-nucleotide exchange factors on ADP-ribosylation factor GTPases (ARF-GEFs) regulate vesicle formation in time and space by activating ARF substrates on distinct donor membranes1. Mammalian GBF1 (ref. 2) and yeast Gea1/2 (ref. 3) ARF-GEFs act at Golgi membranes, regulating COPI-coated vesicle formation. In contrast, their Arabidopsis thaliana homologue GNOM (GN) is required for endosomal recycling, playing an important part in development4. This difference indicates an evolutionary divergence of trafficking pathways between animals and plants, and raised the question of how endoplasmic reticulum–Golgi transport is regulated in plants. Here we demonstrate that the closest homologue of GNOM in Arabidopsis, GNOM-LIKE1 (GNL1; NM_123312; At5g39500), performs this ancestral function. GNL1 localizes to and acts primarily at Golgi stacks, regulating COPI-coated vesicle formation. Surprisingly, GNOM can functionally substitute for GNL1, but not vice versa. Our results suggest that large ARF-GEFs of the GBF1 class perform a conserved role in endoplasmic reticulum–Golgi trafficking and secretion, which is done by GNL1 and GNOM in Arabidopsis, whereas GNOM has evolved to perform an additional plant-specific function of recycling from endosomes to the plasma membrane. Duplication and diversification of ARF-GEFs in plants contrasts with the evolution of entirely new classes of ARF-GEFs5 for endosomal trafficking in animals, which illustrates the independent evolution of complex endosomal pathways in the two kingdoms.

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Figure 1: Identification of the GNL1 compartment.
Figure 2: Localization of BFA-resistant and BFA-sensitive GNL1 after BFA treatment.
Figure 3: Phenotype of gnl1 mutants and relationship of GNL1 to GN.
Figure 4: Functional relationship between GN and GNL1.

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Acknowledgements

We thank N. Takada and L. Müller for technical assistance, A. Vieten, J. Friml, F. El-Kasmi, G. Strompen and K. Steinborn for screening the Cologne T-DNA insertion lines, K. Schumacher, I. Hwang, M. Grebe, A. Schlereth and D.Weijers for providing materials, O. Teh and I. Moore for sharing unpublished material and results, and N. Anders, U. Mayer, K. Schumacher and D. Weigel for critically reading the manuscript and suggestions. We especially thank N. Anders for advice and discussions. This work was supported by an EMBO long-term Fellowship to J.S. and by grants from the Human Frontier in Science Program Organization and the SFB 446 of the Deutsche Forschungsgemeinschaft to G.J.

Author Contributions S.R. carried out most of the experiments, N.G. initiated the project, J.S. generated the RNAi and promoter-swap lines, H.W. generated the ARA7–GFP marker line, Y.-D.S. performed the electron microscopy analysis and immunogold localization experiments, G.R. and C.K. provided the T-DNA collection, D.G.R. generated antisera against markers, and G.J. and S.R. designed the experiments, discussed the results and wrote the manuscript.

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Author notes

  1. Niko Geldner & Gabino Rios

    Present address: Present addresses: Salk Institute for Biological Studies, La Jolla, California 92037, USA (N.G.); Departamento Bioquímica y Biología Molecular, Facultad Biología, Universidad de Valencia, E-46100 Burjassot, Spain (G.R.).,

Authors and Affiliations

  1. ZMBP, Entwicklungsgenetik, and,

    Sandra Richter, Niko Geldner, Jarmo Schrader, Hanno Wolters & Gerd Jürgens

  2. ZMBP, Mikroskopie, Universität Tübingen, Auf der Morgenstelle 3, D-72076 Tübingen, Germany,

    York-Dieter Stierhof

  3. Max-Planck-Institut für Pflanzenzüchtung, Carl-von-Linné-Weg 10, D-50829 Köln, Germany,

    Gabino Rios & Csaba Koncz

  4. Department of Cell Biology, Heidelberg Institute for Plant Sciences, University of Heidelberg, D-69120 Heidelberg, Germany,

    David G. Robinson

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Richter, S., Geldner, N., Schrader, J. et al. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488–492 (2007). https://doi.org/10.1038/nature05967

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