CVP2- and CVL1-mediated phosphoinositide signaling as a regulator of the ARF GAP SFC/VAN3 in establishment of foliar vein patterns

In foliar organs of dicots, veins are arranged in a highly branched or reticulated pattern for efficient distribution of water, photosynthates and signaling molecules. Recent evidence suggests that the patterns rely in part on regulation of intracellular vesicle transport and cell polarity in selected cells during leaf development. The sorting of vesicle cargos to discrete cellular sites is regulated in yeast and animal cells by the binding of specific phosphoinositides (PIs). We report here that, in the plant Arabidopsis, specific PIs guide the vesicle traffic that is essential for polarized and continuous vein pattern formation. Mutations in SFC/VAN3, an ADP-ribosylation factor GTPase-activating protein (ARF GAP) with a PI-binding pleckstrin homology domain, result in discontinuous vein patterns. Plants with mutations in both CVP2 and CVL1, which encode inositol polyphosphate 5'-phosphatases that generate the specific PI ligand for the pleckstrin homology domain of SFC/VAN3, phosphatidylinositol-4-monophosphate (PI(4)P), have a discontinuous vein phenotype identical to that of sfc / van3 mutants. Single cvp2 or cvl1 mutants show weak and no discontinuous vein phenotypes, respectively, suggesting that they act redundantly. We propose that these two 5'-phosphatases regulate vein continuity and cell polarity by generating a specific PI ligand for SFC/VAN3.