Origin and evolution of spliceosomal introns.

Origin and evolution of spliceosomal introns.
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DOI:
10.1186/1745-6150-7-11
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发表时间:
2012-04-16
期刊:
影响因子:
5.5
通讯作者:
Koonin EV
Koonin EV
中科院分区:
生物学2区
文献类型:
--
作者:
Rogozin IB;Carmel L;Csuros M;Koonin EV

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真核基因外显子-内含子结构的进化一直是一个长期而激烈的争论。内含子-早期的概念,后来更名为“内含子优先”,认为编码蛋白质的基因即使在生命进化的最早阶段也被大量内含子打断,内含子通过促进编码小蛋白质/肽模块的序列的重组在蛋白质的起源中发挥着重要作用。内含子晚期的概念认为,内含子只出现在真核生物中,新的内含子在真核生物进化过程中不断积累。对完全测序的真核生物基因组中的同源基因进行分析,发现在动物和植物的同源基因中,甚至在动物、植物和原生动物之间,都存在着许多相同的内含子位置,这表明自上一个真核生物共同祖先(LECA)以来,许多祖先的内含子一直存在。利用不断增长的各种真核生物基因组和日益先进的概率模型重建内含子的获得和丢失,令人信服地表明LECA和每个真核超类群的祖先都有丰富的内含子基因,内含子密度与最丰富的现代基因组中的内含子密度相当,如脊椎动物的基因组。大多数真核生物谱系随后的进化主要涉及内含子的丢失,只有少数几个重要内含子的获得可能伴随着重大进化创新,如后生动物的起源。第二类自剪接内含子的原始入侵可能源于线粒体内共生体,可能是真核发生的一个关键因素,特别是触发了内膜和核的起源。相反,剪接错误会导致选择性剪接,这是造成多细胞真核生物生物学复杂性的主要原因。没有迹象表明任何原核生物曾经在蛋白质编码基因中拥有剪接体或内含子,除了相对罕见的可移动的自剪接内含子。因此,没有任何证据支持内含子优先的假设,但蛋白质编码基因的外显子-内含子结构似乎是与真核细胞一起进化的,内含子是整个真核生物历史上进化的主要因素。本文由I·金·乔丹、曼努埃尔·艾里米亚(由安东尼·普尔提名)、托拜厄斯·莫里耶(由安东尼·普尔提名)和费奥多·康德拉索夫审阅。有关完整的报告,请参阅审阅者报告部分。
Evolution of exon-intron structure of eukaryotic genes has been a matter of long-standing, intensive debate. The introns-early concept, later rebranded ‘introns first’ held that protein-coding genes were interrupted by numerous introns even at the earliest stages of life's evolution and that introns played a major role in the origin of proteins by facilitating recombination of sequences coding for small protein/peptide modules. The introns-late concept held that introns emerged only in eukaryotes and new introns have been accumulating continuously throughout eukaryotic evolution. Analysis of orthologous genes from completely sequenced eukaryotic genomes revealed numerous shared intron positions in orthologous genes from animals and plants and even between animals, plants and protists, suggesting that many ancestral introns have persisted since the last eukaryotic common ancestor (LECA). Reconstructions of intron gain and loss using the growing collection of genomes of diverse eukaryotes and increasingly advanced probabilistic models convincingly show that the LECA and the ancestors of each eukaryotic supergroup had intron-rich genes, with intron densities comparable to those in the most intron-rich modern genomes such as those of vertebrates. The subsequent evolution in most lineages of eukaryotes involved primarily loss of introns, with only a few episodes of substantial intron gain that might have accompanied major evolutionary innovations such as the origin of metazoa. The original invasion of self-splicing Group II introns, presumably originating from the mitochondrial endosymbiont, into the genome of the emerging eukaryote might have been a key factor of eukaryogenesis that in particular triggered the origin of endomembranes and the nucleus. Conversely, splicing errors gave rise to alternative splicing, a major contribution to the biological complexity of multicellular eukaryotes. There is no indication that any prokaryote has ever possessed a spliceosome or introns in protein-coding genes, other than relatively rare mobile self-splicing introns. Thus, the introns-first scenario is not supported by any evidence but exon-intron structure of protein-coding genes appears to have evolved concomitantly with the eukaryotic cell, and introns were a major factor of evolution throughout the history of eukaryotes. This article was reviewed by I. King Jordan, Manuel Irimia (nominated by Anthony Poole), Tobias Mourier (nominated by Anthony Poole), and Fyodor Kondrashov. For the complete reports, see the Reviewers’ Reports section.
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