T2T genome of the basal nematode Xiphinema index reveals major adaptive events associated with plant parasitism and epigenetic regulation

Background Nematodes constitute a particularly speciose animal phylum, occupying an exceptionally broad range of biomes and encompassing free-living microbe-feeders, predators, and notorious plant or animal parasites. However, the limited availability of genome resources for early-branching nematode clades has constrained our understanding of the molecular determinants underlying these multiple evolutionary adaptations. Results We present the genome of the plant-parasitic nematode Xiphinema index, constituting the first telomere-to-telomere assembly for the Dorylaimida, an early-branching nematode order. Phylogenetic analyses suggest that horizontal gene transfers (HGTs) have played a pivotal role in the emergence of plant parasitism in this phylum. Remarkably, we identify the first documented case of a plant-derived HGT in a nematode genome. This gene encodes a predicted secreted effector of parasitism, underscoring the diversity of evolutionary events that contributed to the parasitic arsenal. Indeed, beyond bacteria and fungi, plants seem to have themselves provided crucial genes for parasitism that may now be used by the nematodes to manipulate them. Our comparative genomic analyses across more than 70 nematode species uncovered an epigenetic toolkit unprecedented in any other invertebrate genome. Indeed, X. index harbors a complete set of canonical DNA methyltransferases, a full-length ATRX chromatin remodeler, and a homolog of the 3D-chromatin architectural CTCF protein. Consistent with this repertoire, we detected genome-wide CpG methylation, which inversely correlates with gene expression and chromatin accessibility. Conclusions Overall, these findings reveal a vertebrate-like epigenetic machinery in an early-branching nematode and call for a fundamental reassessment of the prevailing epigenetic paradigm in nematodes and, more broadly, in animals.