A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes

Pollen tubes are highly polarized plant cells specialized in delivering sperm for fertilization. Pollen tube growth is rapid, occurs exclusively at the tip, and can reach distances thousands of times the diameter of the pollen grain without cell division, thus representing an excellent model system for studying asymmetric cell growth. In flowering plants, pollen tube growth is dependent on the actin cytoskeleton, which supports an efficient vesicle trafficking system to deliver membrane and cell-wall materials to the tube tip. A highly dynamic subapical actin structure and an apical vesicular zone are known to be critical for the tip-growth process. How this apical organization is maintained, how the subapical actin structure is assembled, and direct evidence for its functional coupling with tip growth remain to be established. Here, we show that a tip-located, cell membrane-anchored actin-nucleating protein, the Arabidopsis formin homology5 (FH5), stimulates actin assembly from the subapical membrane, provides actin filaments for vesicular trafficking to the apical dome, and mediates assembly of the subapical actin structure. Moreover, FH5-expressing pollen tubes provided a unique opportunity to demonstrate that assembly of the subapical actin structure is concomitant with the acquisition of rapid tip growth, providing further support for their functional coupling. Together, our results show that FH5 plays a pivotal role in establishing the subapical actin and apical vesicular organization critical for tip-focused growth in pollen tubes.