S-RNase-Based Self-Incompatibility in Angiosperms: Degradation, Condensation, and Evolution.

The S-RNase-based self-incompatibility (SI) system is a critical mechanism in angiosperms that safeguards against self-pollination, thereby preserving genetic diversity. Governed by a single multiallelic S-locus, this system is regulated by pistil-expressed S-RNases and pollen-expressed S-Locus F-box proteins (SLFs). In cross-pollination, SLFs assemble into an SCF ubiquitin ligase complex. They selectively recognize non-self S-RNases and target them for proteasomal degradation, allowing pollen tube growth to proceed unimpeded. In self-pollination, S-RNases undergo phase separation, forming cytoplasmic condensates that disrupt the cytoskeleton and redox homeostasis, ultimately triggering programmed cell death. Considered the ancestral SI system, S-RNase-based incompatibility likely emerged through the evolutionary linkage of ancestral S-RNase and SLF genes into a proto-S-locus. Other SI systems in angiosperms are hypothesized to have evolved secondarily via the loss of ancestral components within this evolutionary framework. Future research priorities include elucidating the molecular basis of SLF-mediated recognition of diverse S-RNases, unraveling the complex genetic architecture of the S-locus, and identifying novel SI mechanisms in understudied angiosperm lineages. This review underscores SI's molecular sophistication and evolutionary plasticity, highlighting its fundamental role in plant reproduction and its relevance to agricultural breeding strategies.