Burgin Grace A, Roda Federico, Farnitano Matthew, Hale Charles, Serrato-Capuchina Antonio, Hopkins Robin
Department of Organismic and Evolutionary Biology, The Arnold Arboretum, Harvard University, Cambridge, MA 02138, United States.
Genetics. 2025 Sep 3;231(1). doi: 10.1093/genetics/iyaf132.
Flowering plants display extensive variation in selfing rate, a trait with significant ecological and evolutionary consequences. Many species use genetic mechanisms to recognize and reject self-pollen (termed self-incompatibility or SI), and the loss of SI is one of the most common evolutionary transitions among flowering plants. Despite the ubiquity of transitions to self-compatibility (SC), little is known about the genetic architecture through which SC evolves. Specifically, it is important to determine if SC has a simple or polygenic basis and if variation localizes to the self-pollen recognition locus (the "S-locus"). Phlox drummondii (Polemoniaceae) is a model system for exploring mating system evolution and expresses range-wide variation in SI. Here, we investigate the genetic architecture of SC variants segregating within this otherwise SI species. Using multiple independent crosses, we uncover numerous QTLs associated with intraspecific SI variation, consistent with a polygenic genetic architecture. While some QTLs overlap across mapping experiments, other QTLs are unique, suggesting that multiple genetic routes to SC exist. We demonstrate that P. drummondii has a sporophytic SI system, revealing an independent evolution of SI within the Phlox lineage. We map this novel S-locus and find that the genomic region containing the S-locus is associated with intraspecific variation in SI in one of the 3 mapping populations. Although further work is necessary to clarify the conditions under which quantitative variation in SI represents a transitional pathway to complete SC, our study reveals the genetic architecture upon which selection could act to drive this frequent and evolutionarily significant transition.
开花植物在自交率方面表现出广泛的变异，这一性状具有重要的生态和进化后果。许多物种利用遗传机制来识别和排斥自花花粉（称为自交不亲和或 SI），而 SI 的丧失是开花植物中最常见的进化转变之一。尽管向自交亲和性（SC）转变很普遍，但对于 SC 进化所通过的遗传结构却知之甚少。具体而言，确定 SC 是具有简单还是多基因基础，以及变异是否定位于自花花粉识别位点（“S 位点”）非常重要。矮牵牛（花荵科）是探索交配系统进化的模型系统，并且在 SI 方面表现出广泛的变异。在这里，我们研究了在这个原本具有 SI 的物种中分离的 SC 变异体的遗传结构。通过多个独立杂交，我们发现了许多与种内 SI 变异相关的 QTL，这与多基因遗传结构一致。虽然一些 QTL 在不同的定位实验中重叠，但其他 QTL 是独特的，这表明存在多条通向 SC 的遗传途径。我们证明矮牵牛具有孢子体 SI 系统，揭示了 SI 在矮牵牛谱系中的独立进化。我们定位了这个新的 S 位点，发现在 3 个定位群体之一中，包含 S 位点的基因组区域与种内 SI 变异相关。尽管需要进一步的工作来阐明 SI 的定量变异代表向完全 SC 转变的过渡途径的条件，但我们的研究揭示了选择可能作用于推动这一频繁且具有进化意义的转变所依据的遗传结构。
