title: Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes.
abstract: New gene origination is a major source of genomic innovations that confer phenotypic changes and biological diversity. Generation of new mitochondrial genes in plants may cause cytoplasmic male sterility (CMS), which can promote outcrossing and increase fitness. However, how mitochondrial genes originate and evolve in structure and function remains unclear. The rice Wild Abortive type of CMS is conferred by the mitochondrial gene WA352c (previously named WA352) and has been widely exploited in hybrid rice breeding. Here, we reconstruct the evolutionary trajectory of WA352c by the identification and analyses of 11 mitochondrial genomic recombinant structures related to WA352c in wild and cultivated rice. We deduce that these structures arose through multiple rearrangements among conserved mitochondrial sequences in the mitochondrial genome of the wild rice Oryza rufipogon, coupled with substoichiometric shifting and sequence variation. We identify two expressed but nonfunctional protogenes among these structures, and show that they could evolve into functional CMS genes via sequence variations that could relieve the self-inhibitory potential of the proteins. These sequence changes would endow the proteins the ability to interact with the nucleus-encoded mitochondrial protein COX11, resulting in premature programmed cell death in the anther tapetum and male sterility. Furthermore, we show that the sequences that encode the COX11-interaction domains in these WA352c-related genes have experienced purifying selection during evolution. We propose a model for the formation and evolution of new CMS genes via a "multi-recombination/protogene formation/functionalization" mechanism involving gradual variations in the structure, sequence, copy number, and function.
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Huiwu
authors.initials: H
authors.lastname: Tang
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Xingmei
authors.initials: X
authors.lastname: Zheng
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Chuliang
authors.initials: C
authors.lastname: Li
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Xianrong
authors.initials: X
authors.lastname: Xie
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Yuanling
authors.initials: Y
authors.lastname: Chen
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.|Guangdong Provincial Key Laboratory of Protein Function and Regulation in Agricultural Organisms, Guangzhou 510642, China.
authors.forename: Letian
authors.initials: L
authors.lastname: Chen
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Xiucai
authors.initials: X
authors.lastname: Zhao
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Huiqi
authors.initials: H
authors.lastname: Zheng
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Jiajian
authors.initials: J
authors.lastname: Zhou
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Shan
authors.initials: S
authors.lastname: Ye
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Jingxin
authors.initials: J
authors.lastname: Guo
authors.affiliation: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangzhou 510642, China.|Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions, Guangzhou 510642, China.|College of Life Sciences, South China Agricultural University, Guangzhou 510642, China.
authors.forename: Yao-Guang
authors.initials: YG
authors.lastname: Liu
mesh_terms: D000595:Amino Acid Sequence; D001483:Base Sequence; D003593:Cytoplasm / Q000235:genetics*; D056915:DNA Copy Number Variations / Q000235:genetics; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D056726:Genetic Association Studies; D014644:Genetic Variation; D054629:Genome, Mitochondrial; D008957:Models, Genetic; D012275:Oryza / Q000235:genetics; D051479:Plant Infertility / Q000235:genetics*; D010940:Plant Proteins / Q000737:chemistry / Q000235:genetics; D011995:Recombination, Genetic / Q000235:genetics; D012641:Selection, Genetic
chemical_list: D010940:Plant Proteins