Hybridization and polyploidy enable genomic plasticity without sex in the most devastating plant-parasitic nematodes

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.

Chromosome‐level reference genome of X12, a highly virulent race of the soybean cyst nematode Heterodera glycines

“…Repetitive sequence statistics and classification results are shown in Tables S10 and S11 and Figure S4. The genome of H. glycines is diploid and consists of repeated sequences with higher nucleotide divergence (19.21%) than the genomes of Meloidogyne species, which are polyploid and consist of duplicated regions with low nucleotide divergence (~8%) (Abad et al, ; Blanc‐Mathieu et al, ; Sato et al, ; Szitenberg et al, ).…”

Gene copy number variations as signatures of adaptive evolution in the parthenogenetic, plant‐parasitic nematode Meloidogyne incognita

“…Previous observations highlighted the occurrence of massive duplications that led to the formation of large multigene families in the genome of M. incognita , as illustrated for, for example, genes encoding cell wall‐degrading enzymes (Danchin et al., ) or proteases (Castagnone‐Sereno, Deleury, Danchin, Perfus‐Barbeoch, & Abad, ). Indeed, it is commonly accepted that the genome of parthenogenetic RKNs can tolerate drastic structural variations, for example, various states of aneuploidy (Triantaphyllou, ), or series of synteny breakpoints within the different scaffolds of the genome assembly (Blanc‐Mathieu et al., ; Castagnone‐Sereno & Danchin, ), that may be favoured by a relaxed selection pressure for homologous chromosome pairing in the absence of meiosis. More generally, high rates of gene copy number variations have been documented in various other asexual organisms such as trypanosoma, the ciliate Chilodonella uncinta , the water flea Daphnia pulex or aphids.…”

The Meloidogyne graminicola effector Mg16820 is secreted in the apoplast and cytoplasm to suppress plant host defense responses

“…The coding region of Mg16820 was blasted using default parameters with a cut‐off value of 50 (bitscore) against the M. graminicola genomics resource database (MGRAMBASE; https://insilico.iari.res.in/mgram/), the non‐redundant protein and nucleotide databases for all organisms of the National Center for Biotechnology Information (NCBI), fungal and oomycete genomes (FungiDB; https://fungidb.org/fungidb/), bacterial genomes (Microbial nucleotide blast on NCBI), and the four genomic datasets of the plant‐parasitic nematodes Bursaphelenchus xylophilus , Globodera pallida , M. incognita and M. hapla. In addition, a BLAST was performed against the online Meloidogyne genomic resources database (INRA; https://meloidogyne.inra.fr/; Blanc‐Mathieu et al, ). The alignment of the predicted protein was made using the ClustalW multiple alignment algorithm in Bioedit sequence alignment editor.…”