Mechanosensitive ion channel MSL8 is required for pulsatile growth and cell wall dynamics in Arabidopsis pollen tubes

HIGHLIGHTPollen tube growth requires tight control of apical wall expansion. We present evidence for a mechanosensitive ion channel, MSL8, as a braking signal in growth dynamics through cell wall regulation. The male gametophyte in flowering plants, pollen, both performs the critical role of fertilization and represents a unique and accessible system for interrogating plant cell mechanics. Pollen endures multiple mechanical hurdles during its lifecycle: desiccation in the anther, rapid rehydration on the stigma, and germination to produce a rapidly growing pollen tube that will eventually reach the ovule. A key component in this robust mechanical system is MscS-Like 8 (MSL8), a mechanosensitive ion channel. We previously proposed that that MSL8 serves as an "osmotic safety valve", regulating pressure in the germinating pollen tube by releasing anions in response to plasma membrane tension, thereby preventing pollen tube rupture. However, we subsequently identified defects in the cell walls of msl8 mutant pollen, suggesting that it plays a role independent of osmoregulation, a conclusion also supported by mathematical modeling. Here, we show that pollen tubes lacking MSL8 channel function by genetic knockout or channel-blocking point mutation lose major growth pauses, have altered pectin esterification patterns, and are sensitive to pectin crosslinking. Together, these data suggest a mechanism whereby tension-gated ion release through mechanosensitive channels regulates apoplastic function and cell wall dynamics.