Identification of the pollen self-incompatibility determinant in Papaver rhoeas

Higher plants produce seed through pollination, using specific interactions between pollen and pistil. Self-incompatibility (SI) is an important mechanism used in many species to prevent inbreeding, and is controlled by a multi-allelic S locus1,2. “Self” (incompatible) pollen is discriminated from “non-self” (compatible) pollen, by interaction of pollen and pistil S locus components, and is subsequently inhibited. In Papaver rhoeas, the pistil S locus product is a small protein that interacts with incompatible pollen, triggering a Ca(2+)-dependent signalling network, resulting in pollen inhibition and programmed cell death3-7. Here we have cloned three alleles of a highly polymorphic pollen-expressed gene, PrpS, from Papaver and provide evidence that this encodes the pollen S locus determinant. PrpS is a single copy gene linked to the pistil S gene, PrsS. Sequence analysis indicates that PrsS and PrpS are equally ancient and are likely to have co-evolved. PrpS encodes a novel ~20 kDa protein. Consistent with predictions that it is a transmembrane protein, PrpS is associated with the plasma membrane. We show that a predicted extracellular loop segment of PrpS interacts with PrsS and, using PrpS antisense oligonucleotides, we demonstrate that PrpS is involved in S-specific inhibition of incompatible pollen. Identification of PrpS represents a major advance in our understanding of the Papaver SI system. As a novel cell-cell recognition determinant it contributes to the available information concerning the origins and evolution of cell-cell recognition systems involved in discrimination between “self” and “non-self”, which also include histocompatibility systems in primitive chordates and vertebrates.