Abstract
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.
Highlights
Asexual reproduction occurs in only ~0.1% of animal lineages, which generally occupy shallow branches in the tree of life [1,2]
The genome assembly of M. incognita (Mi) was in the range of estimated size via flow cytometry whereas M. javanica (Mj) and M. arenaria (Ma) assemblies were smaller by 34–60 Mb
To check whether these differences in sizes could be explained by duplicated or repetitive regions collapsed during genome assembly, we plotted the distribution of read coverage along the genome (S1 Fig)
Summary
Asexual reproduction occurs in only ~0.1% of animal lineages, which generally occupy shallow branches in the tree of life [1,2]. Consistent with the geographical parthenogenesis model, parthenogenetic populations of plant and animals are generally present at the edge of the geographical distribution of species, in marginal or anthropologically disturbed environments [17,18]. Their uniparental clonal reproductive mode is supposed to be advantageous for colonizing marginal environments where they escape competition with their sexual relatives. Parthenogenetic species are frequently found at higher latitudes and altitudes [17]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
