The Retromer Protein VPS29 Links Cell Polarity and Organ Initiation in Plants

Abstract

A key feature of plants (as opposed to animals) is their ability to establish new organs not only during embryogenesis, but also throughout their development. A master regulator of organ initiation in plants is the phytohormone auxin. Auxin acts locally as a morphogen and is directionally transported from cell to cell by polarized auxin efflux carriers, termed PIN-FORMED (PIN) proteins. Here we report that the Arabidopsis ortholog of the yeast and mammalian vacuolar protein sorting 29 (VPS29), a member of the retromer complex, mediates the formation of new axes of development. Furthermore, we show that VPS29 is required for endosome homeostasis, PIN protein cycling, and dynamic PIN1 repolarization during development. We propose a model that links VPS29 function, PIN1 polarity, and organ initiation in plants.

Cellular Auxin Homeostasis under High Temperature Is Regulated through a SORTING NEXIN1–Dependent Endosomal Trafficking Pathway

“…However, polarization of PIN2 in epidermal and lateral root cap cells is independent of this pathway (Rahman et al, 2010). Recycling and intracellular trafficking of PIN2 require the retromer proteins SNX1 and VACUOLAR PROTEIN SORTING29 (VPS29) (Jaillais et al, 2006(Jaillais et al, , 2007. SNX1 and VPS29, which reside in late endosomes, are thought to be necessary for retrieval of PIN2 from late endosomes and thus prevent it from being internalized into lytic vacuoles (Kleine-Vehn et al, 2008).…”

“…The direction of auxin flow largely depends on the polar localization of PIN proteins. It has been demonstrated that the polar targeting of a subset of PIN proteins (e.g., PIN1 and PIN2) is regulated by various protein trafficking pathways, including ADP ribosylation factor GTP-exchanging factor-dependent clathrinmediated internalization, Rab GTPases, and retromer complexmediated endosomal pathways (Geldner et al, 2001;Jaillais et al, 2006Jaillais et al, , 2007Michniewicz et al, 2007;Kleine-Vehn et al, 2008). The dynamic trafficking process that contributes toward facilitating the polar targeting of the newly synthesized nonpolar PINs to the plasma membrane (Dhonukshe et al, 2008) can be modified following physiological or environmental changes, resulting in the formation of altered intracellular auxin gradient as well as redirection of auxin flow (Paciorek et al, 2005;Laxmi et al, 2008;Shibasaki et al, 2009;Wan et al, 2012).…”

Trafficking of Vacuolar Proteins: The Crucial Role of Arabidopsis Vacuolar Protein Sorting 29 in Recycling Vacuolar Sorting Receptor

“…VSRs play a crucial role in sorting soluble proteins at the TGN and recycle from the PVC to the TGN (Li et al, 2002;Tse et al, 2004;Kim et al, 2010), although a recent study proposed that VSRs recycle from the TGN to the ER, where they are involved in sorting vacuolar proteins (Niemes et al, 2010a). Arabidopsis VPS29 is a component of the retromer complex (Oliviusson et al, 2006;Shimada et al, 2006;Jaillais et al, 2007), which is thought to be responsible for recycling VSRs (Oliviusson et al, 2006). Initially, the localization of VSR1 was examined in protoplasts from mag1-1 plants.…”

The AP-3 adaptor complex is required for vacuolar function in Arabidopsis

“…Seedlings of wild-type Col-0 and all mutant lines: pat4-1 (EMS mutant), pat4-2 (AP-3 δ SALK mutant; At1g48760; [57]), pat2-2 (AP-3 β SAIL mutant; At3G55480, [10]), vps29 (At3g47810, [58]), double mutant line pat4-2 × pat2-2, crossed lines: pat4-1 × PIN2-GFP, pat4-1 × PIP2a-GFP, pat4-1 × BRI1-GFP, pat4-1 × GFPRABF2b, GFP tagged lines: PIN1 pro :PIN1-GFP (At1g73590, [59]), PIN2 pro :PIN2-GFP (At5G57090; [21]), 35S pro :PIP2a-GFP (X75883, [22]), BRI1 pro :BRI1-GFP (AT4G39400, [23]), RABF2b pro :GFPRABF2b (AT4g19640, [34]), AP-3 β pro :AP-3 β-GFP (At3G55480, [10]), AP-3 δ pro :AP-3 δ-GFP (At3G55480, [56]), as well as obtained by Gateway-based cloning strategy transgenic lines: fulllength Atµ3 (At1g56590) and the (18 amino acids truncated) dominant negative version were grown vertically in Petri dishes on 0.8% agar 0.5× Murashige and Skoog (MS) medium containing 1% sucrose (pH 5.9) at 18 °C, long-day photoperiod.…”