Genetic interactions and natural variation underlying S-RNase-independent unilateral incompatibility in Solanum

Pistils of self-incompatible (SI) species/populations typically reject pollen of related self-compatible (SC) species/populations, but not vice versa, a pattern known as unilateral incompatibility (UI). UI is complex and includes both S-RNase-dependent and S-RNase-independent mechanisms. Pistils of Solanum pennellii LA0716 (SC, no S-RNase) reject pollen of cultivated tomato, Solanum lycopersicum (SC); UI in this system involves the expression of ornithine decarboxylase2 (ODC2) and HT-A/-B genes in the pistil, and farnesyl pyrophosphate synthase2 (FPS2), ui6.2, and ui12.2 in pollen. We show that IL12-3 (HT-A/-B) × IL3-3 (ODC2) double introgression lines reject S. lycopersicum pollen, while odc2 or ht-a mutants do not, demonstrating that ODC2 and HT-A are required for UI. Transmission ratio distortion in favor of pennellii alleles was observed in interspecific F₂ S. lycopersicum × S. pennellii near ui6.2 and ui12.2, and in F₂ IL12-3 × IL3-3 near ui12.2. Equivalent populations made with odc2 mutants segregate in Mendelian ratios, while ht-a mutants have little effect, indicating ui6.2 and ui12.2 interact primarily with ODC2. Pollen from fps2 mutants in S. pennellii LA0716 are incompatible on pistils of all tested S. pennellii and some Solanum habrochaites accessions, but compatible with all other tomato clade species, suggesting ODC2-dependent UI evolved in a common ancestor to S. pennellii and S. habrochaites. Within S. habrochaites, fps2 pollen rejection was observed mainly in SI or mixed mating populations, suggesting an association with outcrossing. Triple mutants of S. pennellii and S. habrochaites lacking functional ODC2, HT-A/-B, and S-RNase are cross-compatible as female parents with S. lycopersicum, allowing transfer of their cytoplasmic genomes into cultivated tomato.