A Living Fossil in the Genome of a Living Fossil: Harbinger Transposons in the Coelacanth Genome

A Living Fossil in the Genome of a Living Fossil: Harbinger Transposons in the Coelacanth Genome
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DOI:
10.1093/molbev/msr267
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发表时间:
2012-03-01
影响因子:
10.7
通讯作者:
Amemiya, Chris T.
Amemiya, Chris T.
中科院分区:
生物学1区
文献类型:
--
作者:
Smith, Jeramiah J.;Sumiyama, Kenta;Amemiya, Chris T.

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来自腔棘鱼基因组的新数据开始揭示四足动物基因和非编码元素的起源和进化。特别相关的是,腔棘鱼保留了转座元件的活性副本,这些转座元件曾经是脊椎动物谱系中新功能序列进化的原材料。认识到腔棘鱼基因组在这方面的进化意义,我们采用了从头开始的搜索策略来进一步对其重复互补进行分类。这一分析揭示了一类散布的元素(Latimeria Harbinger 1-LatiHarb1),它是腔棘鱼基因组结构和基因含量(类似于1%至4%或基因组)的主要贡献者。序列分析表明:1)每个类似8.7kb的LatiHarb1元件都含有两个编码区,一个转座酶基因和一个功能未知的基因(MYB类);2)LatiHarb1的拷贝在腔棘鱼基因组中保持着生物活性。功能分析验证了LatiHarb1在体内的转录和增强子活性,并揭示了转录去偶联,这可能允许MYB样基因发挥与转座没有直接联系的功能。因此,LatiHarb1代表了脊椎动物基因组中具有当代活性的先兆超家族转座子的第一个已知实例。对LatiHarb1的分析进一步证实了这样的观点,即过去活跃的先兆元件的释放至少产生了两个脊椎动物基因(harbi1和neif1),并表明脊椎动物基因tsnare1也可以追溯到这个转座子超家族。基于我们对LatiHarb1的分析,我们推测前导元件的几个功能特征可能使转座子超家族倾向于细胞编码基因的反复突出性进化。此外,这些分析进一步加强了腔棘鱼基因组和其他“外群”基因组在理解脊椎动物基因和基因组的祖先和进化方面的广泛用途。
Emerging data from the coelacanth genome are beginning to shed light on the origin and evolution of tetrapod genes and noncoding elements. Of particular relevance is the realization that coelacanth retains active copies of transposable elements that once served as raw material for the evolution of new functional sequences in the vertebrate lineage. Recognizing the evolutionary significance of coelacanth genome in this regard, we employed an ab initio search strategy to further classify its repetitive complement. This analysis uncovered a class of interspersed elements (Latimeria Harbinger 1-LatiHarb1) that is a major contributor to coelacanth genome structure and gene content (similar to 1% to 4% or the genome). Sequence analyses indicate that 1) each similar to 8.7 kb LatiHarb1 element contains two coding regions, a transposase gene and a gene whose function is as yet unknown (MYB-like) and 2) copies of LatiHarb1 retain biological activity in the coelacanth genome. Functional analyses verify transcriptional and enhancer activities of LatiHarb1 in vivo and reveal transcriptional decoupling that could permit MYB-like genes to play functional roles not directly linked to transposition. Thus, LatiHarb1 represents the first known instance of a harbinger-superfamily transposon with contemporary activity in a vertebrate genome. Analyses of LatiHarb1 further corroborate the notion that exaptation of anciently active harbinger elements gave rise to at least two vertebrate genes (harbi1 and naif1) and indicate that the vertebrate gene tsnare1 also traces its ancestry to this transposon superfamily. Based on our analyses of LatiHarb1, we speculate that several functional features of harbinger elements may predispose the transposon superfamily toward recurrent exaptive evolution of cellular coding genes. In addition, these analyses further reinforce the broad utility of the coelacanth genome and other "outgroup" genomes in understanding the ancestry and evolution of vertebrate genes and genomes.