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

Abstract

Polarized tip growth is a fundamental cellular process in many eukaryotic organisms, mediating growth of neuronal axons and dendrites or fungal hyphae. In plants, pollen and root hairs are cellular model systems for analysing tip growth. 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.

Exocyst SEC3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth

“…The GBF ADP Ribosylation Factor Guanine Nucleotide Exchange Factor (ARFGEF) family GNOM-LIKE2 (GNL2) regulates vesicle recycling. It has been shown that pollen tube growth and pectin secretion are compromised in Arabidopsis gnl2 mutants (Richter et al, 2011). A second family of ARFGEFs called BIGs functions redundantly in secretory vesicle trafficking, and around 50% of the pollen of big1243 2/+ quadruple mutants fails to germinate (Richter et al, 2014), similar to sec3a-1.…”

“…GNL2 and the BIGs regulate vesicle formation at the trans-Golgi network, while the exocyst functions in vesicle tethering at the PM and thus may function with both GNL2 and BIGs vesicle populations. GNL2 has been shown to reside in FM4-64-labeled and nonlabeled membranes (Richter et al, 2011). The spatial separation between strong PM and intracellular FM4-64 labeling and GFP-SEC3a accumulation at the tip-growing site indicates that at least part of the exocyst-dependent exocytosis might not be detected by differential labeling with both FM1-43 and FM4-64 (Zonia and Munnik, 2008).…”

Adaptor Protein Complex 2–Mediated Endocytosis Is Crucial for Male Reproductive Organ Development in Arabidopsis

“…In addition to pollen biogenesis in the anther, pollen grains from the ap2m plants also showed a defect in pollen tube elongation. Indeed, a recent study has provided evidence that an ARF-GEF involved in recycling plays a crucial role in pollen tube elongation in Arabidopsis (Richter et al, 2012).…”

Ethylene Regulates Differential Growth via BIG ARF-GEF-Dependent Post-Golgi Secretory Trafficking in Arabidopsis

“…It has previously been shown that ARF-GEFs can functionally replace each other. For example, GNOM can substitute for GNOM-LIKE1, and GNOM-LIKE2 can substitute for GNOM (Richter et al, 2007(Richter et al, , 2011. However, this does not appear to be the case for GNOM and BIG1-4 in hook development, as the distinct ARF-GEFs have stage-specific roles, with BIG1-4 operating redundantly and independently of GNOM to mediate apical hook maintenance (Figures 1B and 1C; Supplemental Figures 2A to 2D).…”