Department of Plant Biology, Sciences III, University of Geneva, CH-1211 Geneva 4, Switzerland.
Proc Natl Acad Sci U S A. 2012 Apr 10;109(15):5880-5. doi: 10.1073/pnas.1120841109. Epub 2012 Mar 26.
During sexual reproduction, one-half of the genetic material is deposited in gametes, and a complete set of chromosomes is restored upon fertilization. Reduction of the genetic information before gametogenesis occurs in meiosis, when cross-overs (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it was postulated that DNA hypermethylation is inhibitory to COs. Here, when analyzing meiotic recombination in mutant plants with hypomethylated DNA, we observed unexpected and counterintuitive effects of DNA methylation losses on CO distribution. Recombination was further promoted in the hypomethylated chromosome arms while it was inhibited in heterochromatic regions encompassing pericentromeric DNA. Importantly, the total number of COs was not affected, implying that loss of DNA methylation led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influence recombination--whether directly in cis or indirectly in trans by changing expression of genes encoding recombination components--we analyzed CO distribution in wild-type lines with randomly scattered and well-mapped hypomethylated chromosomal segments. The results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. Because DNA methylation exhibits significant variation even within a single species, our results imply that it may influence the evolution of plant genomes through the control of meiotic recombination.
在有性生殖过程中,一半的遗传物质储存在配子中,而在受精时则会恢复一整套染色体。在减数分裂过程中,遗传信息在配子发生之前就会减少,此时同源染色体之间的交叉(COs)会确保它们的遗传信息发生交换。COs 并非均匀分布在染色体上,而且在包含紧密、高甲基化着丝粒和着丝粒周围 DNA 的染色体区域中受到抑制。因此,有人假设 DNA 高甲基化对 COs 具有抑制作用。在这里,当分析 DNA 去甲基化突变植物中的减数重组时,我们观察到 DNA 甲基化缺失对 CO 分布的出人意料和反直觉的影响。在去甲基化的染色体臂中,重组进一步得到促进,而在包含着丝粒周围 DNA 的异染色质区域中则受到抑制。重要的是,CO 的总数没有受到影响,这意味着 DNA 甲基化的丧失导致 CO 沿着染色体的全局重新分配。为了确定改变 DNA 甲基化水平如何影响重组——是直接在顺式中影响,还是通过改变编码重组组件的基因的表达间接在反式中影响——我们分析了在野生型系中具有随机分散且映射良好的去甲基化染色体片段的 CO 分布。这些实验的结果,得到了表达谱数据的支持,表明 DNA 甲基化在顺式中影响减数重组。由于 DNA 甲基化即使在单个物种内也存在显著差异,因此我们的结果表明,它可能通过控制减数重组来影响植物基因组的进化。