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Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes.

ABSTRACT: Lateral gene transfer from prokaryotes to animals is poorly understood, and the scarce documented examples generally concern genes of uncharacterized role in the receiver organism. In contrast, in plant-parasitic nematodes, several genes, usually not found in animals and similar to bacterial homologs, play essential roles for successful parasitism. Many of these encode plant cell wall-degrading enzymes that constitute an unprecedented arsenal in animals in terms of both abundance and diversity. Here we report that independent lateral gene transfers from different bacteria, followed by gene duplications and early gain of introns, have shaped this repertoire. We also show protein immunolocalization data that suggest additional roles for some of these cell wall-degrading enzymes in the late stages of these parasites' life cycle. Multiple functional acquisitions of exogenous genes that provide selective advantage were probably crucial for the emergence and proficiency of plant parasitism in nematodes.

SUBMITTER: Danchin EG

PROVIDER: S-EPMC2955110 | biostudies-literature | 2010 Oct

REPOSITORIES: biostudies-literature

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Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes.

Danchin Etienne G J EG Rosso Marie-Noëlle MN Vieira Paulo P de Almeida-Engler Janice J Coutinho Pedro M PM Henrissat Bernard B Abad Pierre P

Proceedings of the National Academy of Sciences of the United States of America 20100927 41

Lateral gene transfer from prokaryotes to animals is poorly understood, and the scarce documented examples generally concern genes of uncharacterized role in the receiver organism. In contrast, in plant-parasitic nematodes, several genes, usually not found in animals and similar to bacterial homologs, play essential roles for successful parasitism. Many of these encode plant cell wall-degrading enzymes that constitute an unprecedented arsenal in animals in terms of both abundance and diversity. ...[more]

PMID: 20876108

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Project description:Lateral gene transfers (LGT), species to species transmission of genes by means other than direct inheritance from a common ancestor, have played significant role in shaping prokaryotic genomes and are involved in gain or transfer of important biological processes. Whether LGT significantly contributed to the composition of an animal genome is currently unclear. In nematodes, multiple LGT are suspected to have favored emergence of plant-parasitism. With the availability of whole genome sequences it is now possible to assess whether LGT have significantly contributed to the composition of an animal genome and to establish a comprehensive list of these events. We generated clusters of homologous genes and automated phylogenetic inference, to detect LGT in the genomes of root-knot nematodes and found that up to 3.34% of the genes originate from LGT of non-metazoan origin. After their acquisition, the majority of genes underwent series of duplications. Compared to the rest of the genes in these species, several predicted functional categories showed a skewed distribution in the set of genes acquired via LGT. Interestingly, functions related to metabolism, degradation or modification of carbohydrates or proteins were substantially more frequent. This suggests that genes involved in these processes, related to a parasitic lifestyle, have been more frequently fixed in these parasites after their acquisition. Genes from soil bacteria, including plant-pathogens were the most frequent closest relatives, suggesting donors were preferentially bacteria from the rhizosphere. Several of these bacterial genes are plasmid-borne, pointing to a possible role of these mobile genetic elements in the transfer mechanism. Our analysis provides the first comprehensive description of the ensemble of genes of non-metazoan origin in an animal genome. Besides being involved in important processes regarding plant-parasitism, genes acquired via LGT now constitute a substantial proportion of protein-coding genes in these nematode genomes.

Project description:BackgroundTo understand the evolutionary role of Lateral Gene Transfer (LGT), accurate methods are needed to identify transferred genes and infer their timing of acquisition. Phylogenetic methods are particularly promising for this purpose, but the reconciliation of a gene tree with a reference (species) tree is computationally hard. In addition, the application of these methods to real data raises the problem of sorting out real and artifactual phylogenetic conflict.ResultsWe present Prunier, a new method for phylogenetic detection of LGT based on the search for a maximum statistical agreement forest (MSAF) between a gene tree and a reference tree. The program is flexible as it can use any definition of "agreement" among trees. We evaluate the performance of Prunier and two other programs (EEEP and RIATA-HGT) for their ability to detect transferred genes in realistic simulations where gene trees are reconstructed from sequences. Prunier proposes a single scenario that compares to the other methods in terms of sensitivity, but shows higher specificity. We show that LGT scenarios carry a strong signal about the position of the root of the species tree and could be used to identify the direction of evolutionary time on the species tree. We use Prunier on a biological dataset of 23 universal proteins and discuss their suitability for inferring the tree of life.ConclusionsThe ability of Prunier to take into account branch support in the process of reconciliation allows a gain in complexity, in comparison to EEEP, and in accuracy in comparison to RIATA-HGT. Prunier's greedy algorithm proposes a single scenario of LGT for a gene family, but its quality always compares to the best solutions provided by the other algorithms. When the root position is uncertain in the species tree, Prunier is able to infer a scenario per root at a limited additional computational cost and can easily run on large datasets.Prunier is implemented in C++, using the Bio++ library and the phylogeny program Treefinder. It is available at: http://pbil.univ-lyon1.fr/software/prunier.

Project description:The capacity of halophiles to thrive in extreme hypersaline habitats derives partly from the tight regulation of ion homeostasis, the salt-dependent adjustment of plasma membrane fluidity, and the increased capability to manage oxidative stress. Halophilic bacteria, and archaea have been intensively studied, and substantial research has been conducted on halophilic fungi, and the green alga Dunaliella. By contrast, there have been very few investigations of halophiles that are phagotrophic protists, i.e., protozoa. To gather fundamental knowledge about salt adaptation in these organisms, we studied the transcriptome-level response of Halocafeteria seosinensis (Stramenopiles) grown under contrasting salinities. We provided further evolutionary context to our analysis by identifying genes that underwent recent duplications. Genes that were highly responsive to salinity variations were involved in stress response (e.g., chaperones), ion homeostasis (e.g., Na+/H+ transporter), metabolism and transport of lipids (e.g., sterol biosynthetic genes), carbohydrate metabolism (e.g., glycosidases), and signal transduction pathways (e.g., transcription factors). A significantly high proportion (43%) of duplicated genes were also differentially expressed, accentuating the importance of gene expansion in adaptation by H. seosinensis to high salt environments. Furthermore, we found two genes that were lateral acquisitions from bacteria, and were also highly up-regulated and highly expressed at high salt, suggesting that this evolutionary mechanism could also have facilitated adaptation to high salt. We propose that a transition toward high-salt adaptation in the ancestors of H. seosinensis required the acquisition of new genes via duplication, and some lateral gene transfers (LGTs), as well as the alteration of transcriptional programs, leading to increased stress resistance, proper establishment of ion gradients, and modification of cell structure properties like membrane fluidity.

Dataset Information

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes.

Publications

Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes.

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