1. ZMBP, Entwicklungsgenetik, and
2. ZMBP, Mikroskopie, Universität Tübingen, Auf der Morgenstelle 3, D-72076 Tübingen, Germany
3. Max-Planck-Institut für Pflanzenzüchtung, Carl-von-Linné-Weg 10, D-50829 Köln, Germany
4. Department of Cell Biology, Heidelberg Institute for Plant Sciences, University of Heidelberg, D-69120 Heidelberg, Germany
5. 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.).

Correspondence to: Gerd Jürgens¹ Correspondence and requests for materials should be addressed to G.J. (Email: gerd.juergens@zmbp.uni-tuebingen.de).

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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