Pre-zygotic interspecies incompatibility in angiosperms is a male–female relationship that inhibits the formation of hybrids between two species. Here, we report on the identification of STIGMATIC PRIVACY 1 (SPRI1), an interspecies barrier gene in Arabidopsis thaliana. We show that the rejection activity of this stigma-specific plasma membrane protein is effective against distantly related Brassicaceae pollen tubes and is independent of self-incompatibility. Point-mutation experiments and functional tests of synthesized hypothetical ancestral forms of SPRI1 suggest evolutionary decay of SPRI1-controlled interspecies incompatibility in self-compatible A. thaliana. Hetero-pollination experiments indicate that SPRI1 ensures intraspecific fertilization in the pistil when pollen from other species are present. Our study supports the idea that SPRI1 functions as a barrier mechanism that permits entrance of pollen with an intrinsic signal from self species.
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Sequence data can be found at The Arabidopsis Information Resource database (https://www.arabidopsis.org/) or in the 1001 genomes website (1001genomes.org). Raw phenotype data used for the GWAS has been deposited in the GWA-Portal (https://gwas.gmi.oeaw.ac.at/#/study/4205/overview) and Arapheno (https://doi.org/10.21958/study:37). Raw data for pollen tube count was deposited to Mendeley (https://doi.org/10.17632/yzy85dtwk3.1). All other data are available in the article or in the Supplementary information.
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We thank M. Okamura, M. Nara, T. Manabe, Y. Yamamoto, M. Niidome and M. Ishii for their technical assistance and A. Kawabe and Y. Kato for helpful discussions. This work was supported in part by Grants-in-Aid for Scientific Research on Innovative Areas (23113002, 16H06467 and 16H06464 to S. Takayama; 16H01467 and 18H04776 to S. Fujii; 17H05833 and 18H04813 to T.T. and 16H06469 to K.K.S.), Grants-in-Aid for Scientific Research (25252021 and 16H06380 to S.Takayama and 18H02456 to S. Fujii), Grant-in-Aid for Challenging Exploratory Research (15K14626 to S. Fujii) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT), Swiss National Science Foundation to K.K.S. and Japan Science and Technology Agency (JST) PRESTO programme (JPMJPR16Q8) to S. Fujii.
The authors declare no competing interests.
Peer review information: Nature Plants thanks Daphne Goring and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Supplementary Figs. 1–8, Supplementary Tables 1–5, and titles and legends for Supplementary Videos 1 and 2.
Time-lapse imaging analysis of a M. littorea pollen grain attached on a Col-0 stigmatic papilla cell (left) and on a spri1-1 stigmatic papilla cell (right).
Time-lapse imaging analysis of Col-0 and M. littorea pollen grains adjacently attached on a spri1-2 + SPRI1A stigmatic papilla cell.
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Fujii, S., Tsuchimatsu, T., Kimura, Y. et al. A stigmatic gene confers interspecies incompatibility in the Brassicaceae. Nat. Plants 5, 731–741 (2019). https://doi.org/10.1038/s41477-019-0444-6
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