Peculiar hybrid genomes of devastating plant pests promote plasticity in the absence of sex and meiosis

ABSTRACT Root-knot nematodes (genus Meloidogyne ) show an intriguing diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most damaging species to the world agriculture are those that reproduce without meiosis and without sex. To understand this parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of 3 obligatory ameiotic asexual Meloidogyne species and have compared them to those of meiotic relatives with facultative or obligatory asexual reproduction. Our comparative genomic analysis shows that obligatory asexual root-knot nematodes have a higher abundance of transposable elements (TE) compared to the facultative sexual and contain 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. The average nucleotide divergence in the coding portions between duplicated regions is ~5-6 % and we detected diversifying selection between the corresponding gene copies. Genes under diversifying selection covered a wide spectrum of predicted functional categories which suggests a high impact of the genome structure at the functional level. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, suggesting that these putative hybrids share a recent common maternal donor lineage. The intriguing parasitic success of mitotic root-knot nematodes in the absence of sex may be partly explained by TE-rich composite genomes resulting from multiple allo-polyploidization events and promoting plasticity in the absence of sex.