A lectin receptor-like kinase controls self-pollen recognition in Phlox

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 Phlox
(Polemoniaceae) to characterize a novel gene causing self-pollen
recognition which we name Phlox drummondii Pistil Identity Receptor Kinase
(PdPIRK). Recognition of self-pollen associates with a single genomic
region containing the Phlox S-locus. We generate predictions regarding how
S-loci must function and evolve to identify a single candidate gene within
this S-associated region. This gene, PdPIRK, 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
PdPIRK is necessary for self-incompatibility, and we further demonstrate
allele specific activity, confirming its role in self-pollen recognition
per se. PdPIRK encodes a G-type lectin receptor-like kinase, which is a
member of the same gene family as SRK, 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 S-loci evolve and add to our understanding of the diverse molecular
mechanisms through which organisms achieve self-recognition.