Deciphering the Transcriptomic Dynamics of Self-Incompatibility in Yellow Passion Fruit: Evidence of Modified Sporophytic Mechanism

Self-incompatibility (SI) is an important plant mechanism that prevents inbreeding depression by recognizing and rejecting self-pollen, thereby promoting outcrossing. However, SI can also act as a barrier in breeding programs, presenting significant challenges to breeders. Passion fruit (Passiflora edulis), a tropical fruit species of substantial economic importance, also serves as a valuable system for investigating SI mechanisms within the Passifloraceae. Nevertheless, the molecular basis of SI in passion fruit has not yet been elucidated. In this study, we investigated the SI system in yellow passion fruit (P. edulis f. flavicarpa) and employed transcriptomic analysis to examine the time-course transcriptional responses following different pollination treatments. Transcriptomic analysis revealed distinct gene expression dynamics under different pollination treatments: self-pollinated samples exhibited stronger and earlier transcriptional changes, whereas the number of differentially expressed genes (DEGs) in cross-pollinated samples was relatively lower. Numerous pathways previously associated with sporophytic self-incompatibility (SSI) were enriched in the stigma samples after self-pollination. Reactive oxygen species (ROS) are crucial signaling molecules involved in pollen germination and pollen tube growth during SI responses. Our results showed that ROS-related pathways were enriched in stigma tissues after self-pollination. In addition, oxidative stress-related responses were detected in the style shortly after self-pollination, suggesting that plastid-associated or general oxidative stress processes may also be involved, although the precise source of ROS requires further validation. FERONIA, ROP9, and ARC1 are key genes related to the SI system in Brassica. In the passion fruit SI response, the expression levels of these genes increased in the style, indicating a spatial expression pattern different from that reported in classical Brassicaceae SSI systems. Together with cytological observations showing that self-pollen rejection occurs at the stigma surface, our results suggest that yellow passion fruit may employ an SSI-like regulatory framework while exhibiting a lineage-specific spatial deployment of SI-related regulators. Overall, this study provides new transcriptomic insights into the SI mechanism of yellow passion fruit, establishes a molecular framework for understanding SI in P. edulis f. flavicarpa, and offers novel insights into the diversity of plant SI systems.