Comparative genomics of large mitochondria in placozoans.

Comparative genomics of large mitochondria in placozoans.
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DOI:
10.1371/journal.pgen.0030013
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发表时间:
2007-01-12
期刊:
影响因子:
4.5
通讯作者:
Dellaporta SL
Dellaporta SL
中科院分区:
生物学2区
文献类型:
--
作者:
Signorovitch AY;Buss LW;Dellaporta SL

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第一个测序的长生动物 Trichoplax adhaerens 的线粒体基因组挑战了传统观点,即紧凑的线粒体基因组是所有动物的共同特征。另外三个代表高度分化分支的长生动物线粒体基因组已被测序,以确定大毛盘虫 mtDNA 是否是长生动物门成员之间的共同特征,还是独特的衍生条件。发现所有三个线粒体基因组都非常大,为 32 至 37 kb,环状分子,具有典型的 12 个呼吸链基因、24 个 tRNA、rnS 和 rnL。它们与 Trichoplax 线粒体基因组相同,缺乏 atp8、atp9 和所有核糖体蛋白基因,存在多个 cox1 内含子,以及包含 I 组内含子 LAGLIDADG 核酸内切酶结构域的大型开放阅读框。 Placozoa 内 mtDNA 大小的差异是由于基因间间隔区域的变化以及功能未知的长开放阅读框的存在或不存在造成的。 12 个呼吸链基因的系统发育分析支持扁虫的单系性。这里报道的三个线粒体基因组与 Trichoplax 的 mtDNA 在组成和结构上的相似性表明,它们的未压缩状态是其他非后生动物共有的祖先特征,而它们的基因内容是仅在后生动物中共享的衍生特征。动物的线粒体基因组通常比非动物单细胞生物和真菌小得多。动物线粒体基因组的特点是保守基因和其他功能元件紧密结合,而较大的非动物线粒体基因组通常包含非编码区域,例如动物中不存在的内含子和其他基因。因此有人认为,在动物出现之前,线粒体尺寸的急剧减小发生在进化历史的深处。然而,在这项研究中,我们表明,扁动物门(可以说是最古老的动物类群之一)拥有中等大小的线粒体基因组,小于典型的非动物基因组,但比典型动物中发现的线粒体基因组大得多。与非动物一样,长生动物线粒体基因组大小的增加是由于额外基因、内含子和长非编码区的存在。尽管已经发现了其他大型动物线粒体基因组,但它们只是特定物种中的孤立发现,并且没有一个包含像门水平一样大的分类群。由于大型线粒体基因组是所有长生动物的共同特征,并且考虑到该门在动物树中的系统发育位置,我们得出的结论是,与传统观点相反,祖先动物线粒体可能是一个大的、非致密的分子。
The first sequenced mitochondrial genome of a placozoan, Trichoplax adhaerens, challenged the conventional wisdom that a compact mitochondrial genome is a common feature among all animals. Three additional placozoan mitochondrial genomes representing highly divergent clades have been sequenced to determine whether the large Trichoplax mtDNA is a shared feature among members of the phylum Placozoa or a uniquely derived condition. All three mitochondrial genomes were found to be very large, 32- to 37-kb, circular molecules, having the typical 12 respiratory chain genes, 24 tRNAs, rnS, and rnL. They share with the Trichoplax mitochondrial genome the absence of atp8, atp9, and all ribosomal protein genes, the presence of several cox1 introns, and a large open reading frame containing an intron group I LAGLIDADG endonuclease domain. The differences in mtDNA size within Placozoa are due to variation in intergenic spacer regions and the presence or absence of long open reading frames of unknown function. Phylogenetic analyses of the 12 respiratory chain genes support the monophyly of Placozoa. The similarities in composition and structure between the three mitochondrial genomes reported here and that of Trichoplax's mtDNA suggest that their uncompacted state is a shared ancestral feature to other nonmetazoans while their gene content is a derived feature shared only among the Metazoa. Animals typically have much smaller mitochondrial genomes than do nonanimal single-celled organisms and fungi. Whereas animal mitochondrial genomes are characterized by a tightly packed collection of conserved genes and other functional elements, the larger nonanimal mitochondrial genomes generally contain noncoding regions, such as introns and additional genes not present among animals. It has thus been argued that drastic mitochondrial size reduction occurred deep in evolutionary history, before the emergence of animals. In this study, however, we show that the phylum Placozoa, arguably one of the most ancient animal groups, possesses mitochondrial genomes of intermediate size, smaller than the typical nonanimal genome yet much larger than the mitochondrial genome found in typical animals. As in nonanimals, the increased size of the placozoan mitochondrial genome is due to the presence of additional genes, introns, and long noncoding regions. Although other large animal mitochondrial genomes have been discovered, they have been isolated findings in particular species and none encompassed as large a taxonomic group as the level of phylum. Because large mitochondrial genomes are a shared feature among all placozoans and given this phylum's phylogenetic position in the animal tree, we conclude that, contrary to conventional wisdom, the ancestral animal mitochondria was likely a large, noncompacted molecule.
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