Successful sexual reproduction in angiosperms relies on precise communication between pollen and pistil. We have established that a stigmatic gatekeeper, composed of the FERONIA receptor kinase and its homolog ANJEA (FER–ANJ), perceives the RAPID ALKALINIZATION FACTOR peptides RALF23/33, inducing the generation of reactive oxygen species (ROS) in stigma papillary cells. During pollination, the POLLEN COAT PROTEIN B-class peptides (PCP-Bs) compete with RALF23/33 for binding to FER–ANJ, leading to a reduction in stigmatic ROS and subsequently facilitating pollen hydration. This study underscores the precise regulation of plant development by receptor kinases that perceive and switch between different types of peptide ligands. In our examination of the CrRLK1L–LRE/LLG receptor-co-receptor complex, we identified glycosylphosphatidylinositol-anchored proteins LRE/LLGs as chaperones that facilitate the trafficking of CrRLK1L receptor kinases from the endoplasmic reticulum to the plasma membrane. In this capacity, they serve as coreceptors for peptides–CrRLK1L signalings. Further exploration revealed that FER/ANJ and their homologs regulate a ROS generation signaling pathway comprising RALF peptides–CrRLK1L receptor kinases–LRE/LLG co-receptors–RAC/ROPs–NADPH oxidases in various cell types. Therefore, we utilized the root hair cells to explore the downstream signaling of the CrRLK1L–ROS pathway. We found that auxin activates the FER–ROS pathway to regulate the TIR1/AFB2-mediated auxin responses through oxidative modifications. In addition, we obtained some interesting findings in unraveling the signaling pathways governing basal stigmatic responses regulated by pollen peptides and pistil receptor kinases.