Genomic rearrangements promote diversification of a facultative meiotic parthenogenetic nematode pest (Meloidogyne graminicola)

Meloidogyne graminicola (Mg), commonly known as the rice root-knot nematode, is a highly destructive pest that inflicts significant damage on rice crops worldwide. Mg is thought to reproduce primarily by meiotic parthenogenesis, but its success across diverse habitats and hosts raises important questions about its adaptation mechanisms, particularly those driving the evolution of its virulence. Documenting the origin of the pathogen, its reproductive strategies and other evolutionary processes shaping its genome are thus crucial to understand its recent, rapid expansion. In this study, we first improved gene annotations of the Mg genome to enhance identification of potential secreted parasitism genes. Next, comparative genomics analyses of 13 Mg isolates from diverse geographic locations revealed evolutionary changes in the genome, including single nucleotide variations (SNVs), loss of heterozygosity (LoH), and copy number variations (CNVs). These events affected a substantial number of genes, including those coding for secreted proteins, suggesting their roles in nematode adaptation. LoH, the reduction of linkage disequilibrium between SNPs with distance as well as the 4-gamete test all provide evidence for meiotic recombination, supporting some sexual reproduction in Mg. Clustering of populations, based on LoH profiles and SNVs, allowed the definition of groups of isolates not correlating with current geographic distribution. The low sequence divergence at the genome level and the lack of clear phylogeographic structure among isolates support the hypothesis of a recent, widespread dissemination of the parasite, especially across Southeast Asia. Overall, our study supports a dual reproductive mode (sexual/asexual) in Mg, which offers an evolutionary advantage by balancing clonal proliferation in favorable conditions with occasional sexual reproduction allowing generation of new allelic combinations in adverse environments.