A lectin receptor-like kinase controls self-pollen recognition in <i>Phlox</i>

Self-incompatibility (SI) describes a widespread collection of genetic mechanisms in flowering plants used to specifically recognize and reject self-pollen. These mechanisms are fundamental to plant sexual reproduction and offer valuable insight into the molecular basis of cell-cell communication and self-recognition more broadly. Here, we leverage an independent evolution of SI in the lineage containing <i>Phlox</i> (Polemoniaceae) <i>to identify the gene causing self-pollen recognition which we name <i>Phlox drummondii</i></i> <i>Pistil Identity Receptor Kinase</i> (<i>PdPIRK</i>). Recognition of self-pollen associates with a single genomic region containing the <i>Phlox S</i>-locus. We generate predictions regarding how <i>S</i>-loci must function and evolve to identify a single candidate gene within this <i>S</i>-associated region. This gene, <i>PdPIRK</i>, is highly and specifically expressed in the pistil and has exceptionally high polymorphism maintained by negative frequency-dependent selection, two hallmarks of self-pollen recognition genes. Functional validation with gene silencing confirms that <i>PdPIRK</i> is necessary for self-incompatibility, and we further demonstrate allele-specific activity, confirming its role in self-pollen recognition per se. <i>PdPIRK</i> encodes a G-type lectin receptor-like kinase, which is a member of the same gene family as <i>SRK</i>, the gene controlling self-pollen recognition in the distantly related Brassicaceae. Our findings suggest the presence of genetic constraints or paths of least resistance governing how <i>S</i>-loci evolve and add to our understanding of the diverse molecular mechanisms through which organisms achieve self-recognition.