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Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts.

ABSTRACT: Wolbachia, one of the most widespread endosymbionts, is a target for biological control of mosquito-borne diseases (malaria and dengue virus), and antibiotic elimination of infectious filarial nematodes. We sequenced and analyzed the genome of a new Wolbachia strain (wPpe) in the plant-parasitic nematode Pratylenchus penetrans. Phylogenomic analyses placed wPpe as the earliest diverging Wolbachia, suggesting two evolutionary invasions into nematodes. The next branches comprised strains in sap-feeding insects, suggesting Wolbachia may have first evolved as a nutritional mutualist. Genome size, protein content, %GC, and repetitive DNA allied wPpe with mutualistic Wolbachia, whereas gene repertoire analyses placed it between parasite (A, B) and mutualist (C, D, F) groups. Conservation of iron metabolism genes across Wolbachia suggests iron homeostasis as a potential factor in its success. This study enhances our understanding of this globally pandemic endosymbiont, highlighting genetic patterns associated with host changes. Combined with future work on this strain, these genomic data could help provide potential new targets for plant-parasitic nematode control.

SUBMITTER: Brown AM

PROVIDER: S-EPMC5062116 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts.

Brown Amanda M V AM Wasala Sulochana K SK Howe Dana K DK Peetz Amy B AB Zasada Inga A IA Denver Dee R DR

Scientific reports 20161013

Wolbachia, one of the most widespread endosymbionts, is a target for biological control of mosquito-borne diseases (malaria and dengue virus), and antibiotic elimination of infectious filarial nematodes. We sequenced and analyzed the genome of a new Wolbachia strain (wPpe) in the plant-parasitic nematode Pratylenchus penetrans. Phylogenomic analyses placed wPpe as the earliest diverging Wolbachia, suggesting two evolutionary invasions into nematodes. The next branches comprised strains in sap-fe ...[more]

PMID: 27734894

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Project description:Disease prediction tools improve management efforts for many plant diseases. Prediction and downstream prevention demand information about disease etiology, which can be complicated for some diseases, like those caused by soilborne microorganisms. Fortunately, the availability of machine learning methods has enabled researchers to elucidate complex relationships between hosts and pathogens without invoking difficult-to-satisfy assumptions. The etiology of a destructive plant disease, Verticillium wilt of mint, caused by the fungus Verticillium dahliae was reevaluated with several supervised machine learning methods. Specifically, the objective of this research was to identify drivers of wilt in commercial mint fields, describe the relationships between these drivers, and predict wilt. Soil samples were collected from commercial mint fields. Wilt foci, V. dahliae, and plant-parasitic nematodes that can exacerbate wilt were quantified. Multiple linear regression, a generalized additive model, random forest, and an artificial neural network were fit to the data, validated with 10-fold cross-validation, and measures of explanatory and predictive performance were compared. All models selected nematodes within the genus Pratylenchus as the most important predictor of wilt. The fungus after which this disease is named, V. dahliae, was the fourth most important predictor of wilt, after crop age and cultivar. All models explained around 50% of the total variation (R2 ≤ 0.46), and exhibited comparable predictive error (RMSE ≤ 1.21). Collectively, these models revealed that the quantitative relationships between two pathogens, mint cultivars and age are required to explain wilt. The ascendance of Pratylenchus spp. in predicting symptoms of a disease assumed to primarily be caused by V. dahliae exposes the underestimated contribution of these nematodes to wilt. This research provides a foundation on which predictive forecasting tools can be developed for mint growers and reminds us of the lessons that can be learned by revisiting assumptions about disease etiology.

Project description: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.

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Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts.

Publications

Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts.

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