Wang Ruiling, Deng Cecilia H, Cornille Amandine, Marande William, López-Girona Elena, Foster Toshi, Bowatte Deepa, Chen Ting-Hsuan, Chagné David, Schaffer Robert J, Ireland Hilary S
The New Zealand Institute for Plant and Food Research Ltd, Private Bag 92169, Auckland, 1142, New Zealand.
Université Paris Saclay, INRAE, CNRS, AgroParisTech, GQE-LeMoulon, 91190, Gif-sur- Yvette, France.
Sci Rep. 2025 Apr 26;15(1):14630. doi: 10.1038/s41598-025-99335-8.
Self-incompatibility (SI) in plants has evolved independently multiple times and S-RNase-based gametophytic self-incompatibility (GSI) is most common. The Rosaceae family possesses both self-recognition (Prunus) and nonself-recognition (Malus) GSI systems, and the latter is widespread in flowering plants. Gillenia trifoliata is a Rosaceae species related to Prunus and Malus, providing utility for understanding SI evolution. Gillenia is sister taxon to Malus, but unlike Malus, has not undergone polyploidisation. In addition, the common ancestor of Gillenia and Prunus is close to the origin of the subfamily. Using a highly contiguous Gillenia genome, orthologous regions to both Malus and Prunus S-loci were identified. Only the Prunus-like S-locus was highly polymorphic and had signatures of a functional S-locus including positive selection of the S-RNase. This suggests a self-recognition system controls SI in Gillenia, and the common ancestors of Gillenia and Prunus, and Gillenia and the apple tribe, likely had a self-recognition SI system. Comparative genomics between Gillenia and Malus suggest apple lost the self-recognition mechanism, and a nonself-recognition mechanism evolved independently from a rudimentary locus with at least one male S-determinant. Repetitive sequences in the Malus-like S-locus in Gillenia may facilitate illegitimate recombination, suggesting putative mechanisms of evolution of nonself-recognition S-loci.
植物中的自交不亲和性（SI）已经多次独立进化，基于S-核酸酶的配子体自交不亲和性（GSI）最为常见。蔷薇科既拥有自我识别（李属）和非自我识别（苹果属）的GSI系统，后者在开花植物中广泛存在。三叶吉利草是一种与李属和苹果属相关的蔷薇科物种，有助于理解SI的进化。吉利草是苹果属的姐妹分类群，但与苹果属不同，它没有经历多倍体化。此外，吉利草和李属的共同祖先接近该亚科的起源。利用高度连续的吉利草基因组，鉴定出了与苹果属和李属S位点的直系同源区域。只有类似李属的S位点具有高度多态性，并且具有功能性S位点的特征，包括S-核酸酶的正选择。这表明自我识别系统控制着吉利草中的SI，吉利草和李属以及吉利草和苹果族的共同祖先可能具有自我识别SI系统。吉利草和苹果属之间的比较基因组学表明，苹果失去了自我识别机制，非自我识别机制从一个至少有一个雄性S决定因子的基本位点独立进化而来。吉利草中类似苹果属的S位点中的重复序列可能促进非法重组，提示了非自我识别S位点的推定进化机制。
