IHB OpenIR  > 水生生物分子与细胞生物学研究中心  > 期刊论文
Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena
Xiong, Jie1,2; Yang, Wentao1,2; Chen, Kai1,2; Jiang, Chuanqi1,2; Ma, Yang1,2; Chai, Xiaocui1,2; Yan, Guanxiong1,2; Wang, Guangying1,2; Yuan, Dongxia1; Liu, Yifan3; Bidwell, Shelby L.4; Zafar, Nikhat4; Hadjithomas, Michalis4; Krishnakumar, Vivek4; Coyne, Robert S.4; Orias, Eduardo5; Miao, Wei1,2,6,7
2019-06-01
Source PublicationPLOS BIOLOGY
ISSN1544-9173
Volume17Issue:6Pages:38
Abstract

A morphospecies is defined as a taxonomic species based wholly on morphology, but often morphospecies consist of clusters of cryptic species that can be identified genetically or molecularly. The nature of the evolutionary novelty that accompanies speciation in a morphospecies is an intriguing question. Morphospecies are particularly common among ciliates, a group of unicellular eukaryotes that separates 2 kinds of nuclei-the silenced germline nucleus (micronucleus [MIC]) and the actively expressed somatic nucleus (macronucleus [MAC])-within a common cytoplasm. Because of their very similar morphologies, members of the Tetrahymena genus are considered a morphospecies. We explored the hidden genomic evolution within this genus by performing a comprehensive comparative analysis of the somatic genomes of 10 species and the germline genomes of 2 species of Tetrahymena. These species show high genetic divergence; phylogenomic analysis suggests that the genus originated about 300 million years ago (Mya). Seven universal protein domains are preferentially included among the species-specific (i.e., the youngest) Tetrahymena genes. In particular, leucine-rich repeat (LRR) genes make the largest contribution to the high level of genome divergence of the 10 species. LRR genes can be sorted into 3 different age groups. Parallel evolutionary trajectories have independently occurred among LRR genes in the different Tetrahymena species. Thousands of young LRR genes contain tandem arrays of exactly 90-bp exons. The introns separating these exons show a unique, extreme phase 2 bias, suggesting a clonal origin and successive expansions of 90-bp-exon LRR genes. Identifying LRR gene age groups allowed us to document a Tetrahymena intron length cycle. The youngest 90-bp exon LRR genes in T. thermophila are concentrated in pericentromeric and subtelomeric regions of the 5 micronuclear chromosomes, suggesting that these regions act as genome innovation centers. Copies of a Tetrahymena Long interspersed element (LINE)-like retrotransposon are very frequently found physically adjacent to 90-bp exon/intron repeat units of the youngest LRR genes. We propose that Tetrahymena species have used a massive exon-shuffling mechanism, involving unequal crossing over possibly in concert with retrotransposition, to create the unique 90-bp exon array LRR genes.

DOI10.1371/journal.pbio.3000294
Funding OrganizationNational Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; 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National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; 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Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute
Indexed BySCI
Language英语
Funding ProjectNational Natural Science Foundation of China[31525021] ; National Natural Science Foundation of China[91631303] ; National Natural Science Foundation of China[31672281] ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation[MCB-1158346] ; National Human Genome Research Institute[U54 HG003067]
WOS Research AreaBiochemistry & Molecular Biology ; Life Sciences & Biomedicine - Other Topics
WOS SubjectBiochemistry & Molecular Biology ; Biology
WOS IDWOS:000473675900019
WOS KeywordLEUCINE-RICH REPEAT ; PHYLOGENETIC ANALYSIS ; POPULATION-STRUCTURE ; MOLECULAR EVOLUTION ; DIVERGENCE TIMES ; TANDEM REPEATS ; PYRIFORMIS ; SEQUENCE ; DIVERSITY ; PROTEINS
PublisherPUBLIC LIBRARY SCIENCE
Funding OrganizationNational Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; 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Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; 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Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; National Natural Science Foundation of China ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Knowledge Innovation Program of the Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; Youth Innovation Promotion Association, Chinese Academy of Sciences ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute ; National Human Genome Research Institute
Citation statistics
Document Type期刊论文
Identifierhttp://ir.ihb.ac.cn/handle/342005/31732
Collection水生生物分子与细胞生物学研究中心_期刊论文
Corresponding AuthorMiao, Wei
Affiliation1.Chinese Acad Sci, Inst Hydrobiol, Key Lab Aquat Biodivers & Conservat, Wuhan, Hubei, Peoples R China
2.Univ Chinese Acad Sci, Beijing, Peoples R China
3.Univ Michigan, Dept Pathol, Ann Arbor, MI 48109 USA
4.J Craig Venter Inst, Rockville, MD USA
5.Univ Calif Santa Barbara, Dept Mol Cellular & Dev Biol, Santa Barbara, CA 93106 USA
6.CAS Ctr Excellence Anim Evolut & Genet, Kunming, Yunnan, Peoples R China
7.State Key Lab Freshwater Ecol & Biotechnol China, Wuhan, Hubei, Peoples R China
Recommended Citation
GB/T 7714
Xiong, Jie,Yang, Wentao,Chen, Kai,et al. Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena[J]. PLOS BIOLOGY,2019,17(6):38.
APA Xiong, Jie.,Yang, Wentao.,Chen, Kai.,Jiang, Chuanqi.,Ma, Yang.,...&Miao, Wei.(2019).Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena.PLOS BIOLOGY,17(6),38.
MLA Xiong, Jie,et al."Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena".PLOS BIOLOGY 17.6(2019):38.
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