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Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats.

ABSTRACT: Using long-read sequencing, we assembled and unzipped the polyploid genomes of Meloidogyne incognita, M. javanica and M. arenaria, three of the most devastating plant-parasitic nematodes. We found the canonical nematode telomeric repeat to be missing in these and other Meloidogyne genomes. In addition, we find no evidence for the enzyme telomerase or for orthologs of C. elegans telomere-associated proteins, suggesting alternative lengthening of telomeres. Instead, analyzing our assembled genomes, we identify species-specific composite repeats enriched mostly at one extremity of contigs. These repeats are G-rich, oriented, and transcribed, similarly to canonical telomeric repeats. We confirm them as telomeric using fluorescent in situ hybridization. These repeats are mostly found at one single end of chromosomes in these species. The discovery of unusual and specific complex telomeric repeats opens a plethora of perspectives and highlights the evolutionary diversity of telomeres despite their central roles in senescence, aging, and chromosome integrity.

SUBMITTER: Mota APZ

PROVIDER: S-EPMC10844300 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats.

Mota Ana Paula Zotta APZ Koutsovoulos Georgios D GD Perfus-Barbeoch Laetitia L Despot-Slade Evelin E Labadie Karine K Aury Jean-Marc JM Robbe-Sermesant Karine K Bailly-Bechet Marc M Belser Caroline C Péré Arthur A Rancurel Corinne C Kozlowski Djampa K DK Hassanaly-Goulamhoussen Rahim R Da Rocha Martine M Noel Benjamin B Meštrović Nevenka N Wincker Patrick P Danchin Etienne G J EGJ

Nature communications 20240205 1

Using long-read sequencing, we assembled and unzipped the polyploid genomes of Meloidogyne incognita, M. javanica and M. arenaria, three of the most devastating plant-parasitic nematodes. We found the canonical nematode telomeric repeat to be missing in these and other Meloidogyne genomes. In addition, we find no evidence for the enzyme telomerase or for orthologs of C. elegans telomere-associated proteins, suggesting alternative lengthening of telomeres. Instead, analyzing our assembled genomes ...[more]

PMID: 38316773

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Project description:BackgroundThe existence of "ancient asexuals", taxa that have persisted for long periods of evolutionary history without sexual recombination, is both controversial and important for our understanding of the evolution and maintenance of sexual reproduction. A lack of sex has consequences not only for the ecology of the asexual organism but also for its genome. Several genetic signatures are predicted from long-term asexual (apomictic) reproduction including (i) large "allelic" sequence divergence (ii) lack of phylogenetic clustering of "alleles" within morphological species and (iii) decay and loss of genes specific to meiosis and sexual reproduction. These genetic signatures can be hard to assess since it is difficult to demonstrate the allelic nature of very divergent sequences, divergence levels may be complicated by processes such as inter-specific hybridization, and genes may have secondary roles unrelated to sexual reproduction. Apomictic species of Meloidogyne root knot nematodes have been suggested previously to be ancient asexuals. Their relatives reproduce by meiotic parthenogenesis or facultative sexuality, which in combination with the abundance of nematode genomic sequence data, makes them a powerful system in which to study the consequences of reproductive mode on genomic divergence.ResultsHere, sequences from nuclear protein-coding genes are used to demonstrate that the first two predictions of ancient asexuality are found within the apomictic root knot nematodes. Alleles are more divergent in the apomictic taxa than in those species exhibiting recombination and do not group phylogenetically according to recognized species. In contrast some nuclear alleles, and mtDNA, are almost identical across species. Sequencing of Major Sperm Protein, a gamete-specific gene, from both meiotic and ameiotic species reveals no increase in evolutionary rate nor change in substitution pattern in the apomictic taxa, indicating that the locus has been maintained by selection.ConclusionThe data strongly suggests the tropical root knot nematode apomicts have a recent origin and are not anciently asexual. The results support that interspecific hybridization has been involved in the origin of this asexual group and has played a role in shaping the patterns of genetic diversity observed. This study suggests that genetic signatures of ancient asexuality must be taken with caution due to the confounding effect of interspecific hybridization, which has long been implicated in the origins of apomictic species.

Dataset Information

Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats.

Publications

Unzipped genome assemblies of polyploid root-knot nematodes reveal unusual and clade-specific telomeric repeats.

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