Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates.

Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates.
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DOI:
10.1371/journal.pbio.1001241
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发表时间:
2012-01
期刊:
影响因子:
9.8
通讯作者:
Taylor DR
Taylor DR
中科院分区:
生物学1区
文献类型:
--
作者:
Sloan DB;Alverson AJ;Chuckalovcak JP;Wu M;McCauley DE;Palmer JD;Taylor DR

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蝇子草属中的一对物种进化出了已知最大的线粒体基因组,与突变率、重组活性和基因组结构的极端变化相吻合。基因组的大小和复杂性在真核生物物种及其细胞器中有很大差异。在差异很大的真核细胞谱系之间进行的比较表明,突变率的变化可能解释了这种多样性,增加的突变负担有利于减少基因组的大小和复杂性。线粒体突变率在密切相关的被子植物物种之间可以有数量级的差异,这一发现为检验这一假设提供了一个独特的机会。我们对被子植物蝇子草属中两个物种的线粒体基因组进行了测序,它们的线粒体突变率最近急剧加速。与理论预测相反,这些基因组经历了非编码内容的大规模增殖。6.7和11.3 Mb是迄今为止已知最大的线粒体基因组,比大多数细菌基因组甚至一些核基因组都要大。相比之下,两个缓慢进化的Silene线粒体基因组小于被子植物的平均水平。因此,该属捕获了约98%的细胞器基因组大小的已知变异。扩展的基因组揭示了几个结构上的变化,包括复杂的多染色体结构的进化(具有59和128个环状映射染色体,大小从44到192 kb不等)。它们还表现出重组和基因转换活性的显著降低,如通过替代基因组构象的相对频率和重复拷贝之间的序列差异水平所测量的。因此,突变率、基因组大小和染色体结构的进化可能非常迅速,并且以当前进化理论所无法预测的方式相互关联。我们的研究结果提出了一个假设,即重组过程中的变化,包括基因转换,可能是驱动突变率和基因组结构进化的核心力量。进化生物学的一个基本挑战是解释为什么生物体在基因组大小和复杂性上表现出巨大的变化。一种假说预测,DNA序列中的高突变率会产生针对大而复杂的基因组的选择,这些基因组更容易受到突变破坏。Silene属的开花植物的线粒体DNA突变率相差约100倍,这为测试高突变率对基因组进化的预测影响提供了极好的机会。与预期相反,突变率升高的Silene物种与其缓慢进化的亲属相比,线粒体基因组大小经历了戏剧性的扩张,导致已知最大的线粒体基因组。除了大小和突变率的增加,这些基因组还揭示了基因组结构快速变化的历史。它们被分割成几十条染色体,似乎经历了重组活动的重大减少。所有这些变化都发生在过去的几百万年里。这种线粒体基因组多样性的属内蝇子草提供了一个惊人的例子,快速基因组变化,并提出了新的假设突变率和基因组进化之间的关系。
A pair of species within the genus Silene have evolved the largest known mitochondrial genomes, coinciding with extreme changes in mutation rate, recombination activity, and genome structure. Genome size and complexity vary tremendously among eukaryotic species and their organelles. Comparisons across deeply divergent eukaryotic lineages have suggested that variation in mutation rates may explain this diversity, with increased mutational burdens favoring reduced genome size and complexity. The discovery that mitochondrial mutation rates can differ by orders of magnitude among closely related angiosperm species presents a unique opportunity to test this hypothesis. We sequenced the mitochondrial genomes from two species in the angiosperm genus Silene with recent and dramatic accelerations in their mitochondrial mutation rates. Contrary to theoretical predictions, these genomes have experienced a massive proliferation of noncoding content. At 6.7 and 11.3 Mb, they are by far the largest known mitochondrial genomes, larger than most bacterial genomes and even some nuclear genomes. In contrast, two slowly evolving Silene mitochondrial genomes are smaller than average for angiosperms. Consequently, this genus captures approximately 98% of known variation in organelle genome size. The expanded genomes reveal several architectural changes, including the evolution of complex multichromosomal structures (with 59 and 128 circular-mapping chromosomes, ranging in size from 44 to 192 kb). They also exhibit a substantial reduction in recombination and gene conversion activity as measured by the relative frequency of alternative genome conformations and the level of sequence divergence between repeat copies. The evolution of mutation rate, genome size, and chromosome structure can therefore be extremely rapid and interrelated in ways not predicted by current evolutionary theories. Our results raise the hypothesis that changes in recombinational processes, including gene conversion, may be a central force driving the evolution of both mutation rate and genome structure. A fundamental challenge in evolutionary biology is to explain why organisms exhibit dramatic variation in genome size and complexity. One hypothesis predicts that high rates of mutation in DNA sequence create selection against large and complex genomes, which are more susceptible to mutational disruption. Species of flowering plants in the genus Silene vary by approximately 100-fold in the rates of mutation in their mitochondrial DNA, providing an excellent opportunity to test the predicted effects of high mutation rates on genome evolution. Contrary to expectation, Silene species with elevated mutation rates have experienced dramatic expansions in mitochondrial genome size compared to their slowly evolving relatives, resulting in the largest known mitochondrial genomes. In addition to the increases in size and mutation rate, these genomes also reveal a history of rapid change in genome structure. They have been fragmented into dozens of chromosomes and appear to have experienced major reductions in recombination activity. All of these changes have occurred in just the past few million years. This mitochondrial genome diversity within the genus Silene provides a striking example of rapid genomic change and raises new hypotheses regarding the relationship between mutation rate and genome evolution.
DOI: 10.1105/tpc.111.087189
发表时间: 2011-07-01
期刊: PLANT CELL
影响因子: 11.6
作者:
Alverson, Andrew J.;Rice, Danny W.;Palmer, Jeffrey D.
通讯作者: Palmer, Jeffrey D.
DOI: 10.1093/molbev/msn009
发表时间: 2008-03-01
影响因子: 10.7
作者:
Chaw, Shu-Miaw;Shih, Arthur Chun-Chieh;Chou, The-Yuan
通讯作者: Chou, The-Yuan
DOI: 10.1093/molbev/msq029
发表时间: 2010-06-01
影响因子: 10.7
作者:
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通讯作者: Palmer, Jeffrey D.
DOI: 10.1038/ncomms1082
发表时间: 2010-09-21
影响因子: 16.6
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通讯作者: Keeling, Patrick J.