Sexual reproduction in angiosperms relies on precise communications between
the pollen and pistil. The molecular mechanisms underlying these communications
remain elusive. We established that in Arabidopsis, a
stigmatic gatekeeper, the ANJEA–FERONIA (ANJ–FER) receptor kinase complex,
perceives the RAPID ALKALINIZATION FACTOR peptides RALF23 and RALF33 to induce
reactive oxygen species (ROS) production in the stigma papillae, whereas
pollination reduces stigmatic ROS, allowing pollen hydration. Upon pollination,
the POLLEN COAT PROTEIN B-class peptides (PCP-Bs) compete with RALF23/33 for
binding to the ANJ–FER complex, leading to a decline of stigmatic ROS that
facilitates pollen hydration. Our results elucidate a molecular gating mechanism
in which distinct peptide classes from pollen compete with stigma peptides for
interaction with a stigmatic receptor kinase complex, allowing the pollen to
hydrate and germinate.