Pauline Moreels, Servane Bigot, Corentin Defalque, Marie Eve Renard, Juan Pablo Martinez, Stanley Lutts, Muriel Quinet
Reproductive barriers in wild tomato relatives limit the introgression of valuable stress-resistance traits into cultivated tomato, yet the molecular mechanisms governing these barriers in Solanum chilense remain poorly understood compared to model species like Nicotiana alata or Solanum pennellii. This study aimed to characterize the phenotypic and transcriptional architecture of gametophytic self-incompatibility and unilateral incompatibility in Solanum chilense and its interspecific hybrids with Solanum lycopersicum. We combined phenotypic assays of pollen tube growth and fruit set with quantitative gene expression profiling of candidate pistil-side factors across developmental stages and cross-types, supplemented by comparative genomic mapping. We found that the pistil's species identity, rather than compatibility status, was the primary driver of transcriptional variation, indicating a dominant genotype-specific background effect. Expression of the PELPIII-120K-TTSL-TTSR gene cluster and HT-A correlated strongly with barrier strength, while hybrids displayed a partial breakdown of incompatibility linked to altered expression balance. These results demonstrate that reproductive isolation in Solanum chilense relies on a complex, genotype-specific regulatory network rather than universal factors. This insight refines our understanding of plant reproductive evolution and identifies specific molecular targets to overcome hybridization bottlenecks for crop improvement.