Restoring pistil‐side self‐incompatibility factors recapitulates an interspecific reproductive barrier between tomato species

Abstract

Interspecific reproductive barriers are poorly understood, but are central to the biological species concept. The pre-zygotic barriers between red- and green-fruited species in the tomato clade of the genus Solanum provide a model to better understand these barriers in plants. Compatibility usually follows the SI x SC rule: pollen from self-compatible (SC) red-fruited species is rejected on pistils of the predominantly self-incompatible (SI) green-fruited species, but the reciprocal crosses are compatible. This suggests that the interspecific reproductive barrier may be linked to the intraspecific SI mechanism. However, pollen from the SC red-fruited species is also rejected by SC accessions of green-fruited species that lack S-RNase, a key protein expressed in pistils of SI Solanum species. Thus, multiple mechanisms may contribute to the barrier between red- and green-fruited species. We tested whether an S-RNase-dependent barrier is sufficient for rejection of pollen from red-fruited species by introducing functional S-RNase, HT-A and HT-B genes from SI species into Solanum lycopersicum (cultivated tomato). We found that expressing S-RNase in combination with either HT-A or HT-B in the pistil is sufficient to cause rejection of pollen from all four red-fruited species. Thus, redundant mechanisms must operate side by side to prevent crosses between red- and green-fruited species in the clade, underlining the complexity of interspecific pollination barriers. Our results also have implications for mating system transitions. We suggest that these transitions must occur in a specific sequence, and that the transition from SI to SC also affects interspecific compatibility.