A stigmatic gene confers interspecies incompatibility in the Brassicaceae

Abstract

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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Fig. 1: Identification of an interspecific incompatibility-related gene locus via GWAS.
Fig. 2: SPRI1 function has been lost multiple times in the self-compatible A. thaliana.
Fig. 3: SPRI1 is functionally independent of SI.
Fig. 4: Col-0 pollen can mentor the penetration of M. littorea pollen tubes into A. thaliana stigma.
Fig. 5: SPRI1 rejects pollen from distantly related species.
Fig. 6: SPRI1 ensures efficient fertilization under heterologous pollination conditions.

Data availability

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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Acknowledgements

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.

Author information

S. Fujii, K.K.S. and S. Takayama conceived the study. S. Fujii, T.T., K.K.S. and S. Takayama wrote the manuscript. S. Fujii conducted most of the experiments and data analysis. T.T. conducted the GWAS and the geographical analysis. H.S.-A., S. Furukawa, W.I. and Y.W. contributed to phenotyping in the GWAS. Y.K. performed the fluorescent pollen experiment. S.I. contributed to the transgenic experiments. S. Tangpranomkorn contributed to the sequence analysis. M.I. performed the microarray analysis and W.I. performed the real-time PCR.

Correspondence to Sota Fujii or Seiji Takayama.

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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 information

Supplementary Information

Supplementary Figs. 1–8, Supplementary Tables 1–5, and titles and legends for Supplementary Videos 1 and 2.

Reporting Summary

Supplementary Video 1

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).

Supplementary Video 2

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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