Data from: Evolution of interspecies unilateral incompatibility in the relatives of Arabidopsis thaliana

The evolutionary concurrence of intraspecies self-incompatibility (SI) and explosive angiosperm radiation in the Cretaceous has led to the hypothesis that SI was one of the predominant drivers of rapid speciation in angiosperms. Interspecies unilateral incompatibility (UI) usually occurs when pollen from a self-compatible (SC) species is rejected by the pistils of a SI species, while the reciprocal pollination is compatible (UC). Although this SI x SC type UI is most prevalent and viewed as a prezygotic isolation barrier to promote incipient speciation of angiosperms, comparative evidence to support such a role is lacking. We show that SI x SI type UI in SI species pairs is also common in the well-characterized accessions representing the 4 major lineages of the Arabidopsis genus and is developmentally regulated. This allowed us to reveal a strong correlation between UI strength and species divergence in these representative accessions. In addition, analyses of a SC accession and the pseudo-self-compatible (psc) spontaneous mutant of A. lyrata indicate that UI share, at least, common pollen rejection pathway with SI. Furthermore, genetic and genomic analyses of SI x SI type UI in A. lyrata x A. arenosa species pair showed that two major-effect quantitative trait loci are the stigma and pollen side determinant of UI respectively, which could be involved in heterospecies pollen discrimination. By revealing a close link between UI and SI pathway, particularly between UI and species divergence in the representative accessions, our findings establish a connection between SI and speciation. Thus, the preexistence of SI system would have facilitated the evolution of UI and accordingly promote speciation.白垩纪时期，种内自交不亲和（intraspecies self-incompatibility, SI）与被子植物爆发式辐射演化的进化同步性，催生了“SI是被子植物快速物种形成的核心驱动因子之一”这一经典假说。种间单侧不亲和（interspecies unilateral incompatibility, UI）通常表现为：自交亲和（self-compatible, SC）物种的花粉可被SI物种的雌蕊排斥，而反向授粉却可实现亲和（即UC型单侧不亲和）。尽管这类SI×SC型UI最为常见，且被视作促进被子植物初期物种形成的合子前隔离屏障，但目前仍缺乏支持该功能的比较性证据。我们的研究发现，在覆盖拟南芥属4个主要演化支且经过充分鉴定的种质株系中，SI×SI型UI同样普遍存在，且该过程受发育程序精准调控。借此我们揭示，在这些代表性种质株系中，UI强度与物种分化程度存在显著的正相关关系。此外，针对琴叶拟南芥（Arabidopsis lyrata, A. lyrata）的1个SC型种质株系及其自发拟自交不亲和（pseudo-self-compatible, psc）突变体的分析表明，UI至少与SI共享一套保守的花粉排斥通路。进一步地，针对琴叶拟南芥与沙生拟南芥（Arabidopsis arenosa, A. arenosa）杂交组合中SI×SI型UI的遗传与基因组学分析显示，两个效应显著的数量性状位点（quantitative trait loci, QTL）分别作为UI的柱头侧决定因子与花粉侧决定因子，可能参与了异种花粉的识别过程。通过揭示UI与SI通路之间的紧密关联，尤其是代表性种质株系中UI强度与物种分化的相关性，本研究建立了SI与物种形成之间的直接联系。由此可见，SI系统的预先存在，或许推动了UI的演化进程，进而助力被子植物的物种形成。