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A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice

Nature Genetics volume 45, pages 573–577 (2013)Cite this article

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Abstract

Plant cytoplasmic male sterility (CMS) results from incompatibilities between the organellar and nuclear genomes and prevents self pollination, enabling hybrid crop breeding to increase yields1,2,3,4,5,6. The Wild Abortive CMS (CMS-WA) has been exploited in the majority of 'three-line' hybrid rice production since the 1970s, but the molecular basis of this trait remains unknown. Here we report that a new mitochondrial gene, WA352, which originated recently in wild rice, confers CMS-WA because the protein it encodes interacts with the nuclear-encoded mitochondrial protein COX11. In CMS-WA lines, WA352 accumulates preferentially in the anther tapetum, thereby inhibiting COX11 function in peroxide metabolism and triggering premature tapetal programmed cell death and consequent pollen abortion. WA352-induced sterility can be suppressed by two restorer-of-fertility (Rf) genes, suggesting the existence of different mechanisms to counteract deleterious cytoplasmic factors. Thus, CMS-related cytoplasmic-nuclear incompatibility is driven by a detrimental interaction between a newly evolved mitochondrial gene and a conserved, essential nuclear gene.

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Figure 1: Identification and functional analyses of the new mitochondrial gene WA352 for CMS-WA.
Figure 2: Regulation of WA352 expression.
Figure 3: WA352 interacts with the nuclear-encoded mitochondrial protein COX11.
Figure 4: WA352 triggers a ROS burst and Cyt c release to induce premature tapetal PCD and CMS.

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Acknowledgements

We thank G. Zhang, X. Liu (South China Agricultural University) and Q. Qian (China National Rice Research Institute) for providing some rice materials, H. Pang for technical assistance (GIBH, CAS) and H. Ma (Fudan University), J.-M. Li (University of Michigan) and Z.-H. He (San Francisco State University) for critical reading of the manuscript. This work was supported by grants (2011CB100203/2013CBA01401, 31230052 and 2013CB126900) from the Ministry of Science and Technology of China and the National Natural Science Foundation of China to Y.-G.L.

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  1. Hong Xu

    Present address: Present address: College of Life Sciences, Northwest A&F University, Yangling, China.,

Authors and Affiliations

  1. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, College of Life Sciences, South China Agricultural University, Guangzhou, China

    Dangping Luo, Hong Xu, Zhenlan Liu, Jingxin Guo, Heying Li, Letian Chen, Qunyu Zhang, Mei Bai, Hong Wu, Hao Wu, Chonghui Ji, Huiqi Zheng, Yuanling Chen, Shan Ye, Xiaoyu Li, Xiucai Zhao, Riqing Li & Yao-Guang Liu

  2. College of Forestry, Guangxi University, Nanning, China

    Dangping Luo

  3. State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, China

    Ce Fang & Nan Yao

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Contributions

D.L. performed most of the experiments involving the CMS gene functions and mechanism. H.X. and Z.L. found the CMS gene and analyzed its expression. J.G. investigated the gene origin. H.L., L.C., C.F., M.B., N.Y. and Hong Wu conducted cytological observations. Hao Wu and C.J. did plant transformation. Q.Z. mapped the mRNA ends. H.Z. mapped the interaction domains. Y.C., S.Y., X.L., X.Z. and R.L. participated in the characterization of the genes. Y.-G.L. designed and supervised the study and wrote the manuscript. All of the authors discussed the results and commented on the manuscript.

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Correspondence to Yao-Guang Liu.

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Luo, D., Xu, H., Liu, Z. et al. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45, 573–577 (2013). https://doi.org/10.1038/ng.2570

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