Two Loci Contribute Epistastically to Heterospecific Pollen Rejection, a Postmating Isolating Barrier Between Species

Recognition and rejection of heterospecific male gametes occurs in a broad range of taxa, although the complexity of mechanisms underlying these components of postmating cryptic female choice is poorly understood. In plants, the arena for postmating interactions is the female reproductive tract (pistil), within which heterospecific pollen tube growth can be arrested via active molecular recognition and rejection. Unilateral incompatibility (UI) is one such postmating barrier in which pollen arrest occurs in only one direction of an interspecific cross. We investigated the genetic basis of pistil-side UI between Solanum species, with the specific goal of understanding the role and magnitude of epistasis between UI QTL. Using heterospecific introgression lines (ILs) between Solanum pennellii and S. lycopersicum, we assessed the individual and pairwise effects of three chromosomal regions (ui1.1, ui3.1, and ui12.1) previously associated with interspecific UI among Solanum species. Specifically, we generated double introgression (‘pyramided’) genotypes that combined ui12.1 with each of ui1.1 and ui3.1, and assessed the strength of UI pollen rejection in the pyramided lines, compared to single introgression genotypes. We found that none of the three QTL individually showed UI rejection phenotypes, but lines combining ui3.1 and ui12.1 showed significant pistil-side pollen rejection. Furthermore, double ILs (DILs) that combined different chromosomal regions overlapping ui3.1 differed significantly in their rate of UI, consistent with at least two genetic factors on chromosome three contributing quantitatively to interspecific pollen rejection. Together, our data indicate that loci on both chromosomes 3 and 12 are jointly required for the expression of UI between S. pennellii and S. lycopersicum, suggesting that coordinated molecular interactions among a relatively few loci underlie the expression of this postmating prezygotic barrier. In addition, in conjunction with previous data, at least one of these loci appears to also contribute to conspecific self-incompatibility (SI), consistent with a partially shared genetic basis between inter- and intraspecific mechanisms of postmating prezygotic female choice.