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Rapid turnover of antimicrobial-type cysteine-rich protein genes in closely related Oryza genomes

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Abstract

Defensive and reproductive protein genes undergo rapid evolution. Small, cysteine-rich secreted peptides (CRPs) act as antimicrobial agents and function in plant intercellular signaling and are over-represented among reproductively expressed proteins. Because of their roles in defense, reproduction and development and their presence in multigene families, CRP variation can have major consequences for plant phenotypic and functional diversification. We surveyed the CRP genes of six closely related Oryza genomes comprising Oryza sativa ssp. japonica and ssp. indica, Oryza glaberrima and three accessions of Oryza rufipogon to observe patterns of evolution in these gene families and the effects of variation on their gene expression. These Oryza genomes, like other plant genomes, have accumulated large reservoirs of CRP sequences, comprising 26 groups totaling between 676 and 843 genes, in contrast to antimicrobial CRPs in animal genomes. Despite the close evolutionary relationships between the genomes, we observed rapid changes in number and structure among CRP gene families. Many CRP sequences are in gene clusters generated by local duplications, have undergone rapid turnover and are more likely to be silent or specifically expressed. By contrast, conserved CRP genes are more likely to be highly and broadly expressed. Variable CRP genes created by repeated duplication, gene modification and inactivation can gain new functions and expression patterns in newly evolved gene copies. For the CRP proteins, the process of gain/loss by deletion or duplication at gene clusters seems to be an important mechanism in evolution of the gene families, which also contributes to their expression evolution.

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Acknowledgements

This work was supported partly from a grant by the Transdisciplinary Research Integration Center (TRIC) of the Research Organization of Information and Systems, and partly from the National BioResource Project, Japan (NBRP). We would like to thank Drs. Masahiro Fujita (NIG) and Qiang Zhao (CAS) for their help to register genome sequences. This work was funded by a grant from the Transdisciplinary Research Integration Center (TRIC) of the Research Organization of Information and Systems for the project “Genetic Function Systems”, and by the National BioResource Project Japan (NBRP) for the project “Rice Bioresources”.

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The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

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Authors and Affiliations

  1. Plant Genetics Laboratory, National Institute of Genetics, Yata 1111, Mishima, 411-8540, Japan

    Matthew R. Shenton, Hajime Ohyanagi, Toshifumi Nagata & Nori Kurata

  2. Comparative Genomics Laboratory, National Institute of Genetics, Yata 1111, Mishima, 411-8540, Japan

    Atsushi Toyoda & Asao Fujiyama

  3. Mitsubishi Space Software Co. Ltd., Tsukuba Mitsui Building 14F, 1-6-1, Takezono, Tsukuba, Ibaraki, 305-0032, Japan

    Hajime Ohyanagi

  4. National Center for Gene Research, Chinese Academy of Sciences, Shanghai, 500 Caobao Road, Shanghai, 200233, China

    Zi-Xuan Wang, Qi Feng & Bin Han

  5. Department of Genetics, School of Life Sciences, Graduate University of Advanced Studies, SOKENDAI, Yata 1111, Mishima, 411-8540, Japan

    Nori Kurata

  6. Transdisciplinary Research Integration Center, Research Organization of Information and Systems, Hulic Kamiyacho, 4-3-13 Toranomon, Minatoku, Tokyo, 105-0001, Japan

    Atsushi Toyoda, Asao Fujiyama & Nori Kurata

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  1. Matthew R. Shenton
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  9. Nori Kurata
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Correspondence to Nori Kurata.

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Communicated by B. Yang.

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Shenton, M.R., Ohyanagi, H., Wang, ZX. et al. Rapid turnover of antimicrobial-type cysteine-rich protein genes in closely related Oryza genomes. Mol Genet Genomics 290, 1753–1770 (2015). https://doi.org/10.1007/s00438-015-1028-4

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