title: Neofunctionalization of duplicated Tic40 genes caused a gain-of-function variation related to male fertility in Brassica oleracea lineages.
abstract: Gene duplication followed by functional divergence in the event of polyploidization is a major contributor to evolutionary novelties. The Brassica genus evolved from a common ancestor after whole-genome triplication. Here, we studied the evolutionary and functional features of Brassica spp. homologs to Tic40 (for translocon at the inner membrane of chloroplasts with 40 kDa). Four Tic40 loci were identified in allotetraploid Brassica napus and two loci in each of three basic diploid Brassica spp. Although these Tic40 homologs share high sequence identities and similar expression patterns, they exhibit altered functional features. Complementation assays conducted on Arabidopsis thaliana tic40 and the B. napus male-sterile line 7365A suggested that all Brassica spp. Tic40 homologs retain an ancestral function similar to that of AtTic40, whereas BolC9.Tic40 in Brassica oleracea and its ortholog in B. napus, BnaC9.Tic40, in addition, evolved a novel function that can rescue the fertility of 7365A. A homologous chromosomal rearrangement placed bnac9.tic40 originating from the A genome (BraA10.Tic40) as an allele of BnaC9.Tic40 in the C genome, resulting in phenotypic variation for male sterility in the B. napus near-isogenic two-type line 7365AB. Assessment of the complementation activity of chimeric B. napus Tic40 domain-swapping constructs in 7365A suggested that amino acid replacements in the carboxyl terminus of BnaC9.Tic40 cause this functional divergence. The distribution of these amino acid replacements in 59 diverse Brassica spp. accessions demonstrated that the neofunctionalization of Tic40 is restricted to B. oleracea and its derivatives and thus occurred after the divergence of the Brassica spp. A, B, and C genomes.
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Xiaoling
authors.initials: X
authors.lastname: Dun
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Wenhao
authors.initials: W
authors.lastname: Shen
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Kaining
authors.initials: K
authors.lastname: Hu
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Zhengfu
authors.initials: Z
authors.lastname: Zhou
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Shengqian
authors.initials: S
authors.lastname: Xia
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Jing
authors.initials: J
authors.lastname: Wen
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Bin
authors.initials: B
authors.lastname: Yi
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Jinxiong
authors.initials: J
authors.lastname: Shen
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Chaozhi
authors.initials: C
authors.lastname: Ma
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.) tujx@mail.hzau.edu.cn.
authors.forename: Jinxing
authors.initials: J
authors.lastname: Tu
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Tingdong
authors.initials: T
authors.lastname: Fu
authors.affiliation: National Key Laboratory of Crop Genetic Improvement, National Center of Rapeseed Improvement, Huazhong Agricultural University, Wuhan 430070, China (X.D., W.S., K.H., Z.Z., S.X., J.W., B.Y., J.S., C.M., J.T., T.F.); andDepartment of Ecology and Genetics, Evolutionary Biology Center, Uppsala University, Uppsala SE-75236, Sweden (U.L.).
authors.forename: Ulf
authors.initials: U
authors.lastname: Lagercrantz
mesh_terms: D029681:Arabidopsis Proteins / Q000235:genetics; D001937:Brassica / Q000235:genetics* / Q000502:physiology; D029688:Brassica napus / Q000235:genetics / Q000502:physiology; D004171:Diploidy; D019143:Evolution, Molecular; D005298:Fertility / Q000235:genetics; D020440:Gene Duplication; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D005816:Genetic Complementation Test; D018745:Genome, Plant; D008565:Membrane Proteins / Q000235:genetics; D018832:Molecular Chaperones / Q000235:genetics; D010802:Phylogeny; D030821:Plants, Genetically Modified
chemical_list: D029681:Arabidopsis Proteins; D008565:Membrane Proteins; D018832:Molecular Chaperones; C476397:Tic40 protein, Arabidopsis