A Membrane Receptor-Mediated Mechanosensing System Maintains Cell Integrity During Invasive Growth

Abstract

Invasive growth is critical for developmental and reproductive processes (e.g., pollen tube penetration of pistils) and disease progression (e.g., cancer metastasis and fungal hyphae invasion). The invading cells experience drastic changes in mechanical pressure from the surroundings and must balance growth with cell integrity. Here we show that Arabidopsis pollen tubes sense mechanical changes via a cell-surface receptor kinase CUPID1 while penetrating compressing female tissues. Pollen tubes carrying cupid1 mutations fail to maintain cell integrity and burst after exiting these tissues. The mechanosensing function of CUPID1 is established in a microfluidic channel device that mimics the mechanical features of the in vivo growth path. CUPID1-based mechanosensing activates ROP1 GTPase signaling to promote exocytosis that facilitates the secretion of CUPID1's ligands for mechanical signal amplification and cell wall rigidification in pollen tubes. These findings uncover a membrane receptor-mediated mechanosensing system for cells to cope with the physical challenges during invasive growth.