Environmental Genomics, Christian-Albrechts University of Kiel, Kiel, Germany.
Max Planck Institute for Evolutionary Biology, Plön, Germany.
mBio. 2023 Jun 27;14(3):e0329022. doi: 10.1128/mbio.03290-22. Epub 2023 Apr 24.
Meiosis is associated with genetic changes in the genome-via recombination, gene conversion, and mutations. The occurrence of gene conversion and mutations during meiosis may further be influenced by the chromatin conformation, similar to the effect of the chromatin conformation on the mitotic mutation rate. To date, however, the exact distribution and type of meiosis-associated changes and the role of the chromatin conformation in this context are largely unexplored. Here, we determine recombination, gene conversion, and mutations using whole-genome sequencing of all meiotic products of 23 individual meioses in Zymoseptoria tritici, an important pathogen of wheat. We confirm a high genome-wide recombination rate of 65 centimorgan (cM)/Mb and see higher recombination rates on the accessory compared to core chromosomes. A substantial fraction of 0.16% of all polymorphic markers was affected by gene conversions, showing a weak GC-bias and occurring at higher frequency in regions of constitutive heterochromatin, indicated by the histone modification H3K9me3. The mutation rate associated with meiosis was approximately three orders of magnitude higher than the corresponding mitotic mutation rate. Importantly, repeat-induced point mutation (RIP), a fungal defense mechanism against duplicated sequences, is active in and responsible for the majority of these meiotic mutations. Our results indicate that the genetic changes associated with meiosis are a major source of variability in the genome of an important plant pathogen and shape its evolutionary trajectory. The impact of meiosis on the genome composition via gene conversion and mutations is mostly poorly understood, in particular, for non-model species. Here, we sequenced all four meiotic products for 23 individual meioses and determined the genetic changes caused by meiosis for the important fungal wheat pathogen Zymoseptoria tritici. We found a high rate of gene conversions and an effect of the chromatin conformation on gene conversion rates. Higher conversion rates were found in regions enriched with the H3K9me3-a mark for constitutive heterochromatin. Most importantly, meiosis was associated with a much higher frequency of mutations than mitosis; 78% of the meiotic mutations were caused by repeat-induced point mutations-a fungal defense mechanism against duplicated sequences. In conclusion, the genetic changes associated with meiosis are therefore a major factor shaping the genome of this fungal pathogen.
减数分裂伴随着基因组的遗传变化——通过重组、基因转换和突变。减数分裂过程中基因转换和突变的发生可能进一步受到染色质构象的影响，这类似于染色质构象对有丝分裂突变率的影响。然而，迄今为止，减数分裂相关变化的确切分布和类型以及染色质构象在这方面的作用在很大程度上仍未被探索。在这里，我们通过对 23 个 Zymoseptoria tritici 个体减数分裂的所有减数分裂产物进行全基因组测序，确定了重组、基因转换和突变。Zymoseptoria tritici 是一种重要的小麦病原体。我们证实了全基因组范围内 65 厘摩（cM）/Mb 的高重组率，并在附加染色体上观察到比核心染色体更高的重组率。相当一部分 0.16%的多态性标记受到基因转换的影响，表现出较弱的 GC 偏向性，并且在组成型异染色质区域发生的频率更高，这由组蛋白修饰 H3K9me3 所指示。与减数分裂相关的突变率大约比相应的有丝分裂突变率高出三个数量级。重要的是，重复诱导点突变（RIP）是真菌对抗重复序列的防御机制，在减数分裂中是活跃的，并且是这些减数分裂突变的主要原因。我们的结果表明，与减数分裂相关的遗传变化是重要植物病原体基因组中变异性的主要来源，并塑造了其进化轨迹。减数分裂通过基因转换和突变对基因组组成的影响在很大程度上仍未被理解，特别是对于非模式物种。在这里，我们对 23 个个体减数分裂的所有四个减数分裂产物进行了测序，并确定了重要的真菌小麦病原体 Zymoseptoria tritici 减数分裂引起的遗传变化。我们发现基因转换的速率很高，并且染色质构象对基因转换速率有影响。在富含 H3K9me3 的区域发现了更高的转换率——这是组成型异染色质的一个标志。最重要的是，减数分裂与有丝分裂相比，引起突变的频率要高得多；78%的减数分裂突变是由重复诱导点突变引起的——这是一种真菌对抗重复序列的防御机制。总之，与减数分裂相关的遗传变化是塑造这种真菌病原体基因组的主要因素。
