Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena
Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena
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形态种中隐藏的基因组进化——四膜虫快速进化基因的景观
DOI：
10.1371/journal.pbio.3000294
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发表时间：
2019-06-01
期刊：
影响因子：
9.8
通讯作者：
Miao, Wei
中科院分区：
文献类型：
--
作者：
Xiong, Jie;Yang, Wentao;Miao, Wei
形态种被定义为完全基于形态学的分类学物种，但形态种通常由隐性物种群组成，这些隐性物种可通过遗传学或分子方法进行鉴定。伴随形态种形成的进化新特征的本质是一个引人入胜的问题。形态种在纤毛虫中尤为常见，纤毛虫是一类单细胞真核生物，在共同的细胞质内区分出两种细胞核——沉默的生殖系细胞核（微核[MIC]）和活跃表达的体细胞核（大核[MAC]）。由于其非常相似的形态，四膜虫属的成员被视为一个形态种。我们通过对10种四膜虫的体细胞核基因组以及2种四膜虫的生殖系基因组进行全面的比较分析，探索了该属内隐藏的基因组进化。这些物种显示出高度的遗传差异；系统基因组分析表明该属起源于约3亿年前。7种通用蛋白质结构域优先包含在四膜虫的物种特异性（即最年轻的）基因中。特别是，富含亮氨酸重复序列（LRR）基因对10个物种的高水平基因组差异贡献最大。LRR基因可分为3个不同的年龄组。不同四膜虫物种的LRR基因之间独立地出现了平行进化轨迹。数千个年轻的LRR基因包含恰好90bp外显子的串联阵列。分隔这些外显子的内含子显示出独特的、极端的第2相偏好，这表明90bp外显子LRR基因具有克隆起源和连续扩增。对LRR基因年龄组的鉴定使我们能够记录四膜虫内含子长度周期。嗜热四膜虫中最年轻的90bp外显子LRR基因集中在5条微核染色体的着丝粒周围和亚端粒区域，这表明这些区域是基因组创新中心。一种类似四膜虫长散在元件（LINE）的反转录转座子的拷贝经常在物理上紧邻最年轻LRR基因的90bp外显子/内含子重复单元。我们提出四膜虫物种利用了一种大规模的外显子洗牌机制，可能涉及不等交换以及反转录转座，以产生独特的90bp外显子阵列LRR基因。
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.