S-RNase-based self-incompatibility in angiosperms: Degradation, condensation, and evolution

The S-RNase-based self-incompatibility (SI) system is a key mechanism in angiosperms that safeguards against self-pollination, thereby promoting outcrossing and 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 (SLF) proteins. In cross-pollination, SLFs assemble into Skp1/Cullin1//F-box (SCF) ubiquitin ligase complexes. These complexes selectively recognize non-self S-RNases and targets them for proteasomal degradation, allowing pollen tube growth to proceed unimpeded and fertilize the host ovule. In self-pollination, S-RNases capable of escaping degradation by self SCF complex 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.