Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.

Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization.
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DOI:
10.1371/journal.pgen.1004785
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发表时间:
2014-11
期刊:
影响因子:
4.5
通讯作者:
Weigel D
Weigel D
中科院分区:
生物学2区
文献类型:
--
作者:
Seymour DK;Koenig D;Hagmann J;Becker C;Weigel D

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DNA 甲基化是大多数真核生物中发现的一种古老的分子修饰。在植物中,DNA 甲基化不仅对于转录沉默转座子至关重要,而且还可以通过改变蛋白质编码基因的表达来影响表型。然而,由于与 DNA 突变无关的表观等位基因的稳定性有限,其在进化过程中对表型多样性的贡献程度尚不清楚。为了剖析 DNA 甲基化对转座子监测和宿主基因调控的相对贡献,我们利用了基因组结构不同的十字花科三个物种(荠菜、拟南芥和拟南芥)的信息。我们发现转座子和重复序列的谱系特异性扩张和收缩是 DNA 甲基化种间差异的主要驱动因素。因此,基因组甲基化程度最高的部分在序列水平上并不保守。除了重复相关的甲基化之外,位于基因体中的单个核苷酸的甲基化存在令人惊讶的保守程度。最后,在所有物种中,动态 DNA 甲基化更多地受到组织类型的影响,而不是环境差异的影响,但这些反应并不保守。物种间的大部分 DNA 甲基化变异存在于高变基因组区域,因此,在宏观进化的背景下,其表型结果有限。 DNA甲基化是植物中的一种表观遗传标记,由于它可以稳定地代代相传,因此受到了广泛的关注。然而,DNA 甲基化变化或表突变的速率大于 DNA 突变的速率。此外,与 DNA 序列不同,DNA 甲基化在个体内部可能会因发育或环境因素而发生变化。改变的性状是否可以通过 DNA 甲基化的定向修饰传递给下一代是一个非常有趣的问题。我们以三种密切相关的十字花科植物为例,比较了 DNA 甲基化在物种、组织和环境之间的变化。我们发现根和芽之间的 DNA 甲基化是不同的,并且会随着温度的变化而变化,但这种变化在物种之间并不保守。此外,大多数甲基化位点在物种之间并不保守。这表明 DNA 甲基化可能会对环境中的即时波动做出反应,但这种反应不会在长期的进化过程中保留。因此,与转录反应相反,DNA 甲基化水平上的保守表观遗传反应并不普遍。相反,DNA 甲基化的模式很大程度上是由基因组结构的进化决定的,而响应位点很可能是这一过程的短暂意外。
DNA methylation is an ancient molecular modification found in most eukaryotes. In plants, DNA methylation is not only critical for transcriptionally silencing transposons, but can also affect phenotype by altering expression of protein coding genes. The extent of its contribution to phenotypic diversity over evolutionary time is, however, unclear, because of limited stability of epialleles that are not linked to DNA mutations. To dissect the relative contribution of DNA methylation to transposon surveillance and host gene regulation, we leveraged information from three species in the Brassicaceae that vary in genome architecture, Capsella rubella, Arabidopsis lyrata, and Arabidopsis thaliana. We found that the lineage-specific expansion and contraction of transposon and repeat sequences is the main driver of interspecific differences in DNA methylation. The most heavily methylated portions of the genome are thus not conserved at the sequence level. Outside of repeat-associated methylation, there is a surprising degree of conservation in methylation at single nucleotides located in gene bodies. Finally, dynamic DNA methylation is affected more by tissue type than by environmental differences in all species, but these responses are not conserved. The majority of DNA methylation variation between species resides in hypervariable genomic regions, and thus, in the context of macroevolution, is of limited phenotypic consequence. DNA methylation is an epigenetic mark that has received a great deal of attention in plants because it can be stably transmitted across generations. However, the rate of DNA methylation change, or epimutation, is greater than that of DNA mutation. In addition, different from DNA sequence, DNA methylation can vary within an individual in response to developmental or environmental cues. Whether altered characters can be passed on to the next generation via directed modifications in DNA methylation is a question of great interest. We have compared how DNA methylation changes between species, tissues, and environments using three closely related crucifers as examples. We found that DNA methylation is different between roots and shoots and changes with temperatures, but that such changes are not conserved across species. Moreover, most of the methylated sites are not conserved between species. This suggests that DNA methylation may respond to immediate fluctuations in the environment, but this response is not retained over long evolutionary periods. Thus, in contrast to transcriptional responses, conserved epigenetic responses at the level of DNA methylation are not widespread. Instead, the patterns of DNA methylation are largely determined by the evolution of genome structure, and responsive loci are likely short-lived accidents of this process.
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