Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene

Takashi Tsuchimatsu, Keita Suwabe, Rie Shimizu-Inatsugi, Sachiyo Isokawa, Pavlos Pavlidis, Thomas Städler, Go Suzuki, Seiji Takayama, Masao Watanabe, Kentaro K. Shimizu

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    92 Citations (Scopus)

    Abstract

    Ever since Darwin's pioneering research, the evolution of selffertilisation (selfing) has been regarded as one of themost prevalent evolutionary transitions in flowering plants1,2. A major mechanism to prevent selfing is the self-incompatibility (SI) recognition system, which consists of male and female specificity genes at the S-locus and SI modifier genes 2-4. Under conditions that favour selfing, mutations disabling the male recognition component are predicted to enjoy a relative advantage over those disabling the female component, because male mutations would increase through both pollen and seeds whereas female mutations would increase only through seeds5,6. Despite many studies on the genetic basis of loss of SI in the predominantly selfing plant Arabidopsis thaliana7-15, it remains unknown whether selfing arose through mutations in the female specificity gene (S-receptor kinase, SRK),male specificity gene (S-locus cysteine-rich protein, SCR; also known as S-locus protein 11, SP11) or modifier genes, and whether any of them rose to high frequency across large geographic regions. Here we report that a disruptive 213-base-pair (bp) inversion in the SCR gene (or its derivative haplotypes with deletions encompassing the entire SCR-A and a large portion of SRK-A) is found in 95% of European accessions, which contrasts with the genome-wide pattern of polymorphism in European A. thaliana16,17. Importantly, interspecific crossings using Arabidopsis halleri as a pollen donor reveal that some A. thaliana accessions, including Wei-1, retain the female SI reaction, suggesting that all female components including SRK are still functional. Moreover, when the 213-bp inversion in SCR was inverted and expressed in transgenic Wei-1 plants, the functional SCR restored the SI reaction. The inversion within SCR is the first mutation disrupting SI shown to be nearly fixed in geographically wide samples, and its prevalence is consistent with theoretical predictions regarding the evolutionary advantage of mutations in male components.

    Original languageEnglish
    Pages (from-to)1345-1346
    Number of pages2
    JournalNature
    Volume464
    Issue number7293
    DOIs
    Publication statusPublished - 2010 Apr 29

    ASJC Scopus subject areas

    • General

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    Tsuchimatsu, T., Suwabe, K., Shimizu-Inatsugi, R., Isokawa, S., Pavlidis, P., Städler, T., Suzuki, G., Takayama, S., Watanabe, M., & Shimizu, K. K. (2010). Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature, 464(7293), 1345-1346. https://doi.org/10.1038/nature08927