Decoding pollen hydration: The role of FERONIA-mediated signaling in stigmatic actin cytoskeleton dynamics

During pollination, the dry stigma exhibits high selectivity in facilitating the hydration of pollen. Pollen Coat B-class peptides (PCP-Bs) compete with stigmatic rapid alkalinization factor peptides RALF23/33 for interaction with stigmatic receptor kinase FERONIA (FER)/ANJEA (ANJ) to promote pollen hydration. However, the molecular mechanisms underlying the FER-mediated signaling pathway involved in pollen hydration remain largely unexplored. Here, we discovered that the absence of FER in Arabidopsis (Arabidopsis thaliana) leads to alteration of actin cytoskeleton organization in stigmatic papillae and that RALF33 effectively counteracts the stigmatic actin depolymerization induced by Latrunculin B treatment. Next, we identified that ADF3, an actin depolymerizing factor, interacts with the cytoplasmic domain of FER. The mutant of ADF3 supported a significantly slower rate of pollen hydration compared with the wild type. Moreover, FER phosphorylated ADF3 at Thr52 and Thr94 residues in response to RALF33, repressing its actin disassembly activity and stabilizing actin organization in stigmatic papillae. Interestingly, Pollen Coat B-class peptide PCP-Bγ induced stigmatic actin remodeling via ADF3, potentially via FER, thereby facilitating pollen hydration. Taken together, this study reveals that FER-mediated signaling modulates actin cytoskeleton organization within stigmatic papillae by regulating ADF3 activity, thereby controlling stigma accessibility for pollen hydration.