Mora-Carrera Emiliano, Yousefi Narjes, Potente Giacomo, Stubbs Rebecca Lynn, Keller Barbara, Léveillé-Bourret Étienne, Grob Stefan, Celep Ferhat, Tedoradze Giorgi, Conti Elena
Department of Systematic and Evolutionary Botany, University of Zurich, Zurich, Switzerland.
Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.
Mol Biol Evol. 2025 Jul 30;42(8). doi: 10.1093/molbev/msaf162.
Transitions from outcrossing to selfing and from diploidy to polyploidy often co-occur in plants, likely because the ability to produce selfed seed increases the likelihood of newly formed polyploids to become established. An ideal system to study these transitions is Primula, where the shift from diploid, outcrossing progenitors to polyploid, selfing descendants co-occurred repeatedly and the genetic basis of the mating-system shift is known. In Primula, outcrossing is enforced in distylous, typically diploid species characterized by florally heteromorphic, self-incompatible individuals, whereas selfing is enabled in homostylous, typically polyploid species, characterized by florally homomorphic populations of self-compatible plants. Distyly is controlled by the S-locus supergene. Small loss-of-function mutations in the S-locus CYPT gene, which controls style length and female self-incompatibility, are associated with loss of heterostyly in diploid, ancestrally heterostylous Primula species. However, CYPT and the S-locus have never been investigated in interspecific shifts from distylous, diploid species to homostylous, polyploid species. By analyzing the first assembled genome of a homostylous, polyploid species (Primula grandis) in a comparative framework, we discovered two, nearly identical S-locus alleles in the same subgenome, consistent with the hypothesis that the species originated from a cross between a homostylous, diploid pollen donor and a long-styled, diploid pollen recipient. Conformant to theoretical predictions, the macroevolutionary loss of distyly coincided with considerable degeneration of CYPT, including multiple mutations and exon loss, while other S-locus genes remained largely unaffected. This study advances knowledge on the macroevolutionary dynamics of supergenes and genomes in shifts between breeding systems and ploidy levels.
在植物中，从异交向自交的转变以及从二倍体向多倍体的转变常常同时发生，这可能是因为产生自交种子的能力增加了新形成的多倍体得以建立的可能性。报春花属是研究这些转变的理想系统，在该属中，从二倍体异交祖先向多倍体自交后代的转变反复出现，且交配系统转变的遗传基础是已知的。在报春花属中，异交在花柱异长的典型二倍体物种中强制进行，这些物种的个体在花型上具有异形性且自交不亲和，而自交在花柱同长的典型多倍体物种中得以实现，这些物种的花型同形且植株群体自交亲和。花柱异长由S位点超基因控制。S位点CYPT基因的小功能丧失突变控制花柱长度和雌性自交不亲和，与二倍体、祖先花柱异长的报春花属物种中异形性的丧失有关。然而，CYPT和S位点从未在从花柱异长的二倍体物种到花柱同长的多倍体物种的种间转变中被研究过。通过在比较框架下分析花柱同长的多倍体物种（巨花报春）的首个组装基因组，我们在同一亚基因组中发现了两个几乎相同的S位点等位基因，这与该物种起源于花柱同长的二倍体花粉供体和长花柱的二倍体花粉受体之间杂交的假设一致。符合理论预测的是，花柱异长的宏观进化丧失与CYPT的相当程度退化同时发生，包括多个突变和外显子丢失，而其他S位点基因基本未受影响。这项研究推进了我们对超基因和基因组在育种系统和倍性水平转变中的宏观进化动态的认识。
