Independent S-Locus Mutations Caused Self-Fertility in Arabidopsis thaliana

A common yet poorly understood evolutionary transition among flowering plants is a switch from outbreeding to an inbreeding mode of mating. The model plant Arabidopsis thaliana evolved to an inbreeding state through the loss of self-incompatibility, a pollen-rejection system in which pollen recognition by the stigma is determined by tightly linked and co-evolving alleles of the S-locus receptor kinase (SRK) and its S-locus cysteine-rich ligand (SCR). Transformation of A. thaliana, with a functional AlSRKb-SCRb gene pair from its outcrossing relative A. lyrata, demonstrated that A. thaliana accessions harbor different sets of cryptic self-fertility�Cpromoting mutations, not only in S-locus genes, but also in other loci required for self-incompatibility. However, it is still not known how many times and in what manner the switch to self-fertility occurred in the A. thaliana lineage. Here, we report on our identification of four accessions that are reverted to full self-incompatibility by transformation with AlSRKb-SCRb, bringing to five the number of accessions in which self-fertility is due to, and was likely caused by, S-locus inactivation. Analysis of S-haplotype organization reveals that inter-haplotypic recombination events, rearrangements, and deletions have restructured the S locus and its genes in these accessions. We also perform a Quantitative Trait Loci (QTL) analysis to identify modifier loci associated with self-fertility in the Col-0 reference accession, which cannot be reverted to full self-incompatibility. Our results indicate that the transition to inbreeding occurred by at least two, and possibly more, independent S-locus mutations, and identify a novel unstable modifier locus that contributes to self-fertility in Col-0.

显花植物中一类常见却尚未被充分阐明的演化转变，是从异交交配模式向自交交配模式的切换。模式植物拟南芥（Arabidopsis thaliana）通过丢失自交不亲和系统演化至自交状态：该花粉排斥系统中，柱头对花粉的识别由紧密连锁且共演化的S位点受体激酶（S-locus receptor kinase, SRK）及其S位点富半胱氨酸配体（S-locus cysteine-rich ligand, SCR）的等位基因决定。将来自其异交近缘种琴叶拟南芥（A. lyrata）的功能性AlSRKb-SCRb基因对转化拟南芥，实验结果证实，拟南芥种质携带多组隐蔽的自育促进突变，这些突变不仅存在于S位点基因中，也分布于自交不亲和所需的其他基因座。然而，目前仍不清楚拟南芥谱系中向自育的转变发生了多少次、以何种方式完成。本研究鉴定出4个通过转化AlSRKb-SCRb即可恢复完全自交不亲和的种质，使自育由S位点失活导致且可能由其引发的拟南芥种质数量增至5个。对S单倍型结构的分析显示，单倍型间重组、重排与缺失事件重构了这些种质中的S位点及其基因。本研究还针对无法恢复完全自交不亲和的Col-0参考种质，开展了数量性状位点（Quantitative Trait Loci, QTL）分析，以鉴定与自育相关的修饰基因座。研究结果表明，向自交的转变至少由两次（或更多次）独立的S位点突变引发，并鉴定出一个新的不稳定修饰基因座，该位点可促进Col-0的自育。