Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice

Yohei Koide, Atsushi Ogino, Takanori Yoshikawa, Yuki Kitashima, Nozomi Saito, Yoshitaka Kanaoka, Kazumitsu Onishi, Yoshihiro Yoshitake, Takuji Tsukiyama, Hiroki Saito, Masayoshi Teraishi, Yoshiyuki Yamagata, Aiko Uemura, Hiroki Takagi, Yoriko Hayashi, Tomoko Abe, Yoshimichi Fukuta, Yutaka Okumoto, Akira Kanazawa

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Abstract

Understanding the genetic basis of reproductive barriers between species has been a central issue in evolutionary biology. The S1 locus in rice causes hybrid sterility and is a major reproductive barrier between two rice species, Oryza sativa and Oryza glaberrima. The O. glaberrima-derived allele (denoted S1g) on the S1 locus causes preferential abortion of gametes with its allelic alternative (denoted S1s) in S1g/S1s heterozygotes. Here, we used mutagenesis and screening of fertile hybrid plants to isolate a mutant with an allele, S1mut, which does not confer sterility in the S1mut/S1g and S1mut/S1s hybrids. We found that the causal mutation of the S1mut allele was a deletion in the peptidase-coding gene (denoted “SSP”) in the S1 locus of O. glaberrima. No orthologous genes of SSP were found in the O. sativa genome. Transformation experiments indicated that the introduction of SSP in carriers of the S1s allele did not induce sterility. In S1mut/S1s heterozygotes, the insertion of SSP led to sterility, suggesting that SSP complemented the loss of the functional phenotype of the mutant and that multiple factors are involved in the phenomenon. The polymorphisms caused by the lineage-specific acquisition or loss of the SSP gene were implicated in the generation of hybrid sterility. Our results demonstrated that artificial disruption of a single gene for the reproductive barrier creates a “neutral” allele, which facilitates interspecific hybridization for breeding programs.

Original languageEnglish
Pages (from-to)E1995-E1962
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number9
DOIs
Publication statusPublished - Feb 27 2018

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Infertility
Alleles
Genes
Heterozygote
Germ Cells
Mutagenesis
Breeding
Peptide Hydrolases
Oryza
Genome
Phenotype
Mutation

All Science Journal Classification (ASJC) codes

  • General

Cite this

Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice. / Koide, Yohei; Ogino, Atsushi; Yoshikawa, Takanori; Kitashima, Yuki; Saito, Nozomi; Kanaoka, Yoshitaka; Onishi, Kazumitsu; Yoshitake, Yoshihiro; Tsukiyama, Takuji; Saito, Hiroki; Teraishi, Masayoshi; Yamagata, Yoshiyuki; Uemura, Aiko; Takagi, Hiroki; Hayashi, Yoriko; Abe, Tomoko; Fukuta, Yoshimichi; Okumoto, Yutaka; Kanazawa, Akira.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 9, 27.02.2018, p. E1995-E1962.

Research output: Contribution to journalArticle

Koide, Y, Ogino, A, Yoshikawa, T, Kitashima, Y, Saito, N, Kanaoka, Y, Onishi, K, Yoshitake, Y, Tsukiyama, T, Saito, H, Teraishi, M, Yamagata, Y, Uemura, A, Takagi, H, Hayashi, Y, Abe, T, Fukuta, Y, Okumoto, Y & Kanazawa, A 2018, 'Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 9, pp. E1995-E1962. https://doi.org/10.1073/pnas.1711656115
Koide, Yohei ; Ogino, Atsushi ; Yoshikawa, Takanori ; Kitashima, Yuki ; Saito, Nozomi ; Kanaoka, Yoshitaka ; Onishi, Kazumitsu ; Yoshitake, Yoshihiro ; Tsukiyama, Takuji ; Saito, Hiroki ; Teraishi, Masayoshi ; Yamagata, Yoshiyuki ; Uemura, Aiko ; Takagi, Hiroki ; Hayashi, Yoriko ; Abe, Tomoko ; Fukuta, Yoshimichi ; Okumoto, Yutaka ; Kanazawa, Akira. / Lineage-specific gene acquisition or loss is involved in interspecific hybrid sterility in rice. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 9. pp. E1995-E1962.
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AU - Onishi, Kazumitsu

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AU - Saito, Hiroki

AU - Teraishi, Masayoshi

AU - Yamagata, Yoshiyuki

AU - Uemura, Aiko

AU - Takagi, Hiroki

AU - Hayashi, Yoriko

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