Blanc-Mathieu Romain, Perfus-Barbeoch Laetitia, Aury Jean-Marc, Da Rocha Martine, Gouzy Jérôme, Sallet Erika, Martin-Jimenez Cristina, Bailly-Bechet Marc, Castagnone-Sereno Philippe, Flot Jean-François, Kozlowski Djampa K, Cazareth Julie, Couloux Arnaud, Da Silva Corinne, Guy Julie, Kim-Jo Yu-Jin, Rancurel Corinne, Schiex Thomas, Abad Pierre, Wincker Patrick, Danchin Etienne G J
INRA, Université Côte d'Azur, CNRS, ISA, France.
Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, Japan.
PLoS Genet. 2017 Jun 8;13(6):e1006777. doi: 10.1371/journal.pgen.1006777. eCollection 2017 Jun.
Root-knot nematodes (genus Meloidogyne) exhibit a diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most widespread and devastating species to global agriculture are those that reproduce asexually, without meiosis. To disentangle this surprising parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of three obligatory ameiotic and asexual Meloidogyne. We have compared them to those of relatives able to perform meiosis and sexual reproduction. We show that the genomes of ameiotic asexual Meloidogyne are large, polyploid and made of duplicated regions with a high within-species average nucleotide divergence of ~8%. Phylogenomic analysis of the genes present in these duplicated regions suggests that they originated from multiple hybridization events and are thus homoeologs. We found that up to 22% of homoeologous gene pairs were under positive selection and these genes covered a wide spectrum of predicted functional categories. To biologically assess functional divergence, we compared expression patterns of homoeologous gene pairs across developmental life stages using an RNAseq approach in the most economically important asexually-reproducing nematode. We showed that >60% of homoeologous gene pairs display diverged expression patterns. These results suggest a substantial functional impact of the genome structure. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, signifying that these putative hybrids share a recent common maternal ancestor. Transposable elements (TE) cover a ~1.7 times higher proportion of the genomes of the ameiotic asexual Meloidogyne compared to the sexual relative and might also participate in their plasticity. The intriguing parasitic success of asexually-reproducing Meloidogyne species could be partly explained by their TE-rich composite genomes, resulting from allopolyploidization events, and promoting plasticity and functional divergence between gene copies in the absence of sex and meiosis.
根结线虫（Meloidogyne属）表现出多样的繁殖方式，从 obligatory sexual 到完全无性繁殖。有趣的是，对全球农业来说，分布最广、危害最大的物种是那些无性繁殖、不进行减数分裂的物种。为了弄清楚尽管没有有性生殖和基因交换，这些线虫却能取得惊人的寄生成功的原因，我们对三种 obligatory ameiotic 和无性繁殖的根结线虫的基因组进行了测序和组装。我们将它们与能够进行减数分裂和有性生殖的亲缘物种的基因组进行了比较。我们发现，ameiotic 无性繁殖的根结线虫的基因组很大，是多倍体，由重复区域组成，种内平均核苷酸差异约为8%，很高。对这些重复区域中存在的基因进行系统基因组分析表明，它们起源于多次杂交事件，因此是同源基因。我们发现，高达22%的同源基因对受到正选择，这些基因涵盖了广泛的预测功能类别。为了从生物学角度评估功能差异，我们在经济上最重要的无性繁殖线虫中，使用RNAseq方法比较了同源基因对在不同发育阶段的表达模式。我们发现，超过60%的同源基因对表现出不同的表达模式。这些结果表明基因组结构具有重大的功能影响。与种内核基因组的高差异形成对比的是，这三种ameiotic无性繁殖线虫之间的线粒体基因组差异非常低，这表明这些假定的杂交种有一个最近的共同母系祖先。与有性生殖的亲缘物种相比，转座元件（TE）在ameiotic无性繁殖的根结线虫基因组中所占比例高出约1.7倍，并且可能也参与了它们的可塑性。无性繁殖的根结线虫物种令人着迷的寄生成功，可能部分是由于它们富含TE的复合基因组，这些基因组是异源多倍体化事件的结果，并且在没有有性生殖和减数分裂的情况下，促进了基因拷贝之间的可塑性和功能差异。
