Mechanism of self/nonself-discrimination in Brassica self-incompatibility

Kohji Murase; Yoshitaka Moriwaki; Tomoyuki Mori; Xiao Liu; Chiho Masaka; Yoshinobu Takada; Ryoko Maesaki; Masaki Mishima; Sota Fujii; Yoshinori Hirano; Zen Kawabe; Koji Nagata; Tohru Terada; Go Suzuki; Masao Watanabe; Kentaro Shimizu; Toshio Hakoshima; Seiji Takayama

doi:10.1038/s41467-020-18698-w

Mechanism of self/nonself-discrimination in Brassica self-incompatibility

Kohji Murase, Yoshitaka Moriwaki, Tomoyuki Mori, Xiao Liu, Chiho Masaka, Yoshinobu Takada, Ryoko Maesaki, Masaki Mishima, Sota Fujii, Yoshinori Hirano, Zen Kawabe, Koji Nagata, Tohru Terada, Go Suzuki, Masao Watanabe, Kentaro Shimizu, Toshio Hakoshima, Seiji Takayama

LIF - Molecular and Chemical Life Science

Research output: Contribution to journal › Article › peer-review

13 Citations (Scopus)

Abstract

Self-incompatibility (SI) is a breeding system that promotes cross-fertilization. In Brassica, pollen rejection is induced by a haplotype-specific interaction between pistil determinant SRK (S receptor kinase) and pollen determinant SP11 (S-locus Protein 11, also named SCR) from the S-locus. Although the structure of the B. rapa S₉-SRK ectodomain (eSRK) and S₉-SP11 complex has been determined, it remains unclear how SRK discriminates self- and nonself-SP11. Here, we uncover the detailed mechanism of self/nonself-discrimination in Brassica SI by determining the S₈-eSRK–S₈-SP11 crystal structure and performing molecular dynamics (MD) simulations. Comprehensive binding analysis of eSRK and SP11 structures reveals that the binding free energies are most stable for cognate eSRK–SP11 combinations. Residue-based contribution analysis suggests that the modes of eSRK–SP11 interactions differ between intra- and inter-subgroup (a group of phylogenetically neighboring haplotypes) combinations. Our data establish a model of self/nonself-discrimination in Brassica SI.

Original language	English
Article number	4916
Journal	Nature communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-18698-w
Publication status	Published - 2020 Dec 1

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-020-18698-w

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Murase, K., Moriwaki, Y., Mori, T., Liu, X., Masaka, C., Takada, Y., Maesaki, R., Mishima, M., Fujii, S., Hirano, Y., Kawabe, Z., Nagata, K., Terada, T., Suzuki, G., Watanabe, M., Shimizu, K., Hakoshima, T., & Takayama, S. (2020). Mechanism of self/nonself-discrimination in Brassica self-incompatibility. Nature communications, 11(1), [4916]. https://doi.org/10.1038/s41467-020-18698-w

Murase, K, Moriwaki, Y, Mori, T, Liu, X, Masaka, C, Takada, Y, Maesaki, R, Mishima, M, Fujii, S, Hirano, Y, Kawabe, Z, Nagata, K, Terada, T, Suzuki, G, Watanabe, M, Shimizu, K, Hakoshima, T & Takayama, S 2020, 'Mechanism of self/nonself-discrimination in Brassica self-incompatibility', Nature communications, vol. 11, no. 1, 4916. https://doi.org/10.1038/s41467-020-18698-w

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title = "Mechanism of self/nonself-discrimination in Brassica self-incompatibility",

abstract = "Self-incompatibility (SI) is a breeding system that promotes cross-fertilization. In Brassica, pollen rejection is induced by a haplotype-specific interaction between pistil determinant SRK (S receptor kinase) and pollen determinant SP11 (S-locus Protein 11, also named SCR) from the S-locus. Although the structure of the B. rapa S9-SRK ectodomain (eSRK) and S9-SP11 complex has been determined, it remains unclear how SRK discriminates self- and nonself-SP11. Here, we uncover the detailed mechanism of self/nonself-discrimination in Brassica SI by determining the S8-eSRK–S8-SP11 crystal structure and performing molecular dynamics (MD) simulations. Comprehensive binding analysis of eSRK and SP11 structures reveals that the binding free energies are most stable for cognate eSRK–SP11 combinations. Residue-based contribution analysis suggests that the modes of eSRK–SP11 interactions differ between intra- and inter-subgroup (a group of phylogenetically neighboring haplotypes) combinations. Our data establish a model of self/nonself-discrimination in Brassica SI.",

author = "Kohji Murase and Yoshitaka Moriwaki and Tomoyuki Mori and Xiao Liu and Chiho Masaka and Yoshinobu Takada and Ryoko Maesaki and Masaki Mishima and Sota Fujii and Yoshinori Hirano and Zen Kawabe and Koji Nagata and Tohru Terada and Go Suzuki and Masao Watanabe and Kentaro Shimizu and Toshio Hakoshima and Seiji Takayama",

note = "Funding Information: We thank K. Maenaka for critical advice on protein expression, SPring-8, and Photon Factory (PF) staff for assistance of data collection, and R. Kurata and H. Okubo for MALDI-TOF-MS and protein sequence analysis. This work was supported by JSPS KAKENHI grant numbers 15K18683 and 20K05824 (to K.M.), 18KT0048 and 19K22342 (to M.W.), and 16H06380 (to S.T.); JSPS Bilateral Programs grant number 18032211-000481 (to M.W.); MEXT KAKENHI grant numbers 23113006 (to G.S.), 16H06470, 16H06464, and 16K21727 (to M.W.), and 16H06467 (to S.T.); the Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research [BINDS]) from AMED under Grant Number JP20am0101107 (support number 0840); The Nakajima Foundation (to K.M.); the Takeda Science Foundation (to K.M.); and the Toray Science Foundation (to K.M.). K.M. Funding Information: was supported by a Postdoctoral Fellowship for Young Scientists from JSPS. Data collection experiments at SPring-8 and PF were supported by JASRI (Proposal numbers: 2015A6549, 2015B6549, 2016A2519, 2016B2519, 2017A6759, 2017B6759, 2018A2529, 2018B2529, and 2019B2516) and KEK (Proposal number, 2014G706). The NMR experiments were partly performed at RIKEN of the NMR Platform supported by the MEXT. Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-020-18698-w",

language = "English",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

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T1 - Mechanism of self/nonself-discrimination in Brassica self-incompatibility

AU - Murase, Kohji

AU - Moriwaki, Yoshitaka

AU - Mori, Tomoyuki

AU - Liu, Xiao

AU - Masaka, Chiho

AU - Takada, Yoshinobu

AU - Maesaki, Ryoko

AU - Mishima, Masaki

AU - Fujii, Sota

AU - Hirano, Yoshinori

AU - Kawabe, Zen

AU - Nagata, Koji

AU - Terada, Tohru

AU - Suzuki, Go

AU - Watanabe, Masao

AU - Shimizu, Kentaro

AU - Hakoshima, Toshio

AU - Takayama, Seiji

N1 - Funding Information: We thank K. Maenaka for critical advice on protein expression, SPring-8, and Photon Factory (PF) staff for assistance of data collection, and R. Kurata and H. Okubo for MALDI-TOF-MS and protein sequence analysis. This work was supported by JSPS KAKENHI grant numbers 15K18683 and 20K05824 (to K.M.), 18KT0048 and 19K22342 (to M.W.), and 16H06380 (to S.T.); JSPS Bilateral Programs grant number 18032211-000481 (to M.W.); MEXT KAKENHI grant numbers 23113006 (to G.S.), 16H06470, 16H06464, and 16K21727 (to M.W.), and 16H06467 (to S.T.); the Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research [BINDS]) from AMED under Grant Number JP20am0101107 (support number 0840); The Nakajima Foundation (to K.M.); the Takeda Science Foundation (to K.M.); and the Toray Science Foundation (to K.M.). K.M. Funding Information: was supported by a Postdoctoral Fellowship for Young Scientists from JSPS. Data collection experiments at SPring-8 and PF were supported by JASRI (Proposal numbers: 2015A6549, 2015B6549, 2016A2519, 2016B2519, 2017A6759, 2017B6759, 2018A2529, 2018B2529, and 2019B2516) and KEK (Proposal number, 2014G706). The NMR experiments were partly performed at RIKEN of the NMR Platform supported by the MEXT. Publisher Copyright: © 2020, The Author(s).

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Self-incompatibility (SI) is a breeding system that promotes cross-fertilization. In Brassica, pollen rejection is induced by a haplotype-specific interaction between pistil determinant SRK (S receptor kinase) and pollen determinant SP11 (S-locus Protein 11, also named SCR) from the S-locus. Although the structure of the B. rapa S9-SRK ectodomain (eSRK) and S9-SP11 complex has been determined, it remains unclear how SRK discriminates self- and nonself-SP11. Here, we uncover the detailed mechanism of self/nonself-discrimination in Brassica SI by determining the S8-eSRK–S8-SP11 crystal structure and performing molecular dynamics (MD) simulations. Comprehensive binding analysis of eSRK and SP11 structures reveals that the binding free energies are most stable for cognate eSRK–SP11 combinations. Residue-based contribution analysis suggests that the modes of eSRK–SP11 interactions differ between intra- and inter-subgroup (a group of phylogenetically neighboring haplotypes) combinations. Our data establish a model of self/nonself-discrimination in Brassica SI.

AB - Self-incompatibility (SI) is a breeding system that promotes cross-fertilization. In Brassica, pollen rejection is induced by a haplotype-specific interaction between pistil determinant SRK (S receptor kinase) and pollen determinant SP11 (S-locus Protein 11, also named SCR) from the S-locus. Although the structure of the B. rapa S9-SRK ectodomain (eSRK) and S9-SP11 complex has been determined, it remains unclear how SRK discriminates self- and nonself-SP11. Here, we uncover the detailed mechanism of self/nonself-discrimination in Brassica SI by determining the S8-eSRK–S8-SP11 crystal structure and performing molecular dynamics (MD) simulations. Comprehensive binding analysis of eSRK and SP11 structures reveals that the binding free energies are most stable for cognate eSRK–SP11 combinations. Residue-based contribution analysis suggests that the modes of eSRK–SP11 interactions differ between intra- and inter-subgroup (a group of phylogenetically neighboring haplotypes) combinations. Our data establish a model of self/nonself-discrimination in Brassica SI.

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U2 - 10.1038/s41467-020-18698-w

DO - 10.1038/s41467-020-18698-w

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VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4916

ER -

Mechanism of self/nonself-discrimination in Brassica self-incompatibility

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