Parasitic success without sexual reproduction: what more than 10 years of root-knot nematode genomics revealed?

Abstract

Plant-parasitic nematodes are responsible for the destruction of ca. 11% of the worldwide life-sustaining crop production every year. Feeding an ever-growing human population without affecting more negatively our planet, will require important efforts aiming at reducing the agricultural losses caused by plant pests. In this context, understanding how these parasites have evolved and how adaptive they are is highly important. Plant parasitism has evolved at least four times independently in the phylum Nematoda and the root-knot nematodes (RKN) are the most devastating of them. Curiously, the RKN that display the wider range of compatible host plants and the broader geographic distribution reproduce without sex and meiosis. This parasitic success without sex has long been considered an evolutionary mystery.
In 2008, we coordinated the genome sequencing and analysis of the RKN Meloidogyne incognita, using 1st generation sequencing technology (Sanger). This was the first genome for a plant-parasitic animal and the first for an animal reproducing without sex and meiosis. In 2017, we published a more complete genome assembly for M. incognita and produced genome sequences for two other devastating asexually reproducing RKN, M. javanica and M. arenaria, using 2nd generation sequencing technology (illumina + 454). This provided the most comprehensive set of protein-coding genes for a plant-parasitic nematode and enabled comparative genomics analyses. Phylogenomics analyses based on these new genomes and gene sets revealed the polyploid hybrid origin of these species. This also allowed demonstrating that the resulting gene copies differ in their expression patterns and that some have underwent diversifying selection. Hence, the genome structure might provide an evolutionary advantage. Recently, using population genomics on the genome of M. incognita we could confirm the absence of sexual recombination in this species, which reinforced the paradoxical nature of the parasitic success.
In this presentation, I will summarize what the 1st and 2nd generation genomics analyses have allowed to learn and understand about the genome structure of parthenogenetic RKN in relation to their surprising parasitic success despite asexual reproduction. I will also give an overview of the latest progresses obtained thanks to 3rd generation long read sequencing and the new opportunities opened.