Phased chromosome-scale genome assembly of an asexual, allopolyploid root-knot nematode reveals complex subgenomic structure

Abstract

We present the chromosome-scale genome of the allopolyploid root-knot nematode Meloidogyne javanica. We show that the M. javanica genome is predominantly allotetraploid, comprising two subgenomes, A and B, that most likely originated from hybridisation of two ancestral parental species. The assembly is annotated using full-length non-chimeric transcripts, comparison to reference databases, and ab initio prediction techniques, and the subgenomes are phased using ancestral k-mer spectral analysis. Subgenome B appears to show greater fission of chromosomal contigs, and while there is substantial synteny between subgenomes, we also identify regions lacking synteny that may have diverged in the ancestral genomes prior to or following hybridisation. Indels are common both between alleles within a subgenome, and between the A and B subgenomes, suggesting the M. javanica genome exists in a dynamic hypo-tetraploidy where copy number can vary along the chromosome. This annotated and phased genome assembly forms a significant resource for understanding the origins and genetics of these globally important plant pathogens. Author SummaryRoot-knot nematodes represent one of the most significant crop parasites globally. Despite their agricultural importance, only rudimentary genomic resources have been published to date, leaving a gap in the understanding of genetic mechanisms driving genome evolution and crop virulence. Here, we have used modern genomic and bioinformatic approaches to create a chromosome-scale reference genome to investigate the origins and genomic constitution of the root-knot nematode species Meloidogyne javanica. This species reproduces by ameiotic parthenogenesis and has an allopolyploid genome and is among the most damaging plant parasitic nematodes with a large and evolving plant host range. Utilising modern long-range DNA sequencing and bioinformatics approaches, we successfully phased the genome into its constituent subgenomes, a first for this agriculturally important clade. While we find the genomic landscape is mostly syntenic between subgenomes, we identified regions of minimal similarity, and highlight structural divergence between subgenomes. We demonstrate that this species was originally tetraploid, but insertions and deletions have been the major force in generating diversity, resulting in a hypo-tetraploid genome with local variations in ploidy.