Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii

Vanholme, Bartel; Mitreva, Makedonka; Criekinge, Wim Van; Logghe, Marc; Bird, David; McCarter, James P.; Gheysen, Godelieve

doi:10.1007/s00436-005-0029-3

Cited by 51 publications

(61 citation statements)

References 50 publications

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“…This suggests that GH43 genes have been acquired in nematodes via LGT of bacterial origin (probably an ancestral or relative of Actinomycetales). Interestingly, a putative arabinogalactan endo-1,4-β-galactosidase (EC 3.2.1.89) from family GH53, unrelated to GH43, was found in ESTs from the cyst nematode Heterodera schachtii, and we identified only a homolog in the draft genome of H. glycines (19,20), suggesting that it is restricted to cyst nematodes.…”

Section: Resultsmentioning

confidence: 87%

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

Danchin

Rosso

Vieira

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

302

285

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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.LGT) is the transmission of genes between organisms by mechanisms other than vertical inheritance from an ancestor to an offspring. Although largely documented as an important evolutionary mechanism in prokaryotes (1), LGT in animals that have a separate germline and whose genome is segregated in a nucleus is poorly explored. Although some examples have been described (2-4), most concern transfers from endosymbiotic bacteria, and none provide a clear link between the activity of the transferred gene products and the biology of the host species. Thus, arguments are lacking to support a selective advantage that would have driven fixation of transferred genes at the level of a population or species. By contrast, in plant-parasitic nematodes, a series of genes encoding plant cell wall-degrading or -modifying enzymes, which are usually absent from animals, exhibit similarity to bacteria and may thus originate from LGT. These genes are transcriptionally active, their products have been biochemically characterized, they are secreted in plant tissues, and their inactivation impairs parasitism efficiency (5). The most damaging nematodes to agriculture worldwide belong to the suborder Tylenchina in clade IV that comprises root-knot nematodes and cyst nematodes, the two most-studied lineages (SI Appendix, Fig. S1). These nematodes are able to penetrate and migrate into plant tissue and establish sophisticated parasitic interactions with their hosts. Invasion of the root tissues by nematodes requires degradation of the plant cell wall protective barrier, constituted mainly of cellulose and hemicelluloses as well as pectin and its branched decorations. The first plant cell wall-degrading enzymes from an animal were characterized in cyst nematodes in 1998 (6). Ten years later, analysis of the genome of Meloidogyne incognita, the first genome analysis for a plant-parasitic nematode, revealed that the repertoire of cell wall-degrading enzymes in a single species is diverse and abundant with more than 60 genes covering six different pro...

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Section: Resultsmentioning

confidence: 87%

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

Danchin

Rosso

Vieira

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

302

285

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“…Secretion of proteins that are capable of modifying or manipulating the host environment is one of the adaptations during parasitism evolution to permit survival of parasites in the potentially hostile host (Harcus et al, 2004;Vanholme et al, 2005). Of the 1793 D. immitis clusters, we were able to identify putative signal peptides for secretion in 36 clusters and nine of these were further predicted as putative secreted proteins after meeting our criteria (see Section 2).…”

Section: Functional Categorization and Other Sequence Analysismentioning

confidence: 95%

Identification and analysis of genes expressed in the adult filarial parasitic nematode Dirofilaria immitis

Yin

Martin

McCarter

et al. 2006

International Journal for Parasitology

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The heartworm Dirofilaria immitis is a filarial parasitic nematode infecting dogs and other mammals worldwide causing fatal complications. Here, we present the first large-scale survey of the adult heartworm transcriptome by generation and analysis of 4005 expressed sequence tags, identifying about 1800 genes and expanding the available sequence information for the parasite significantly. Brugia malayi genomic data offered the most valuable information to interpret heartworm genes, with about 70% of D. immitis genes showing significant similarities to the assembly. Comparative genomic analyses revealed both genes common to metazoans or nematodes and genes specific to filarial parasites that may relate to parasitism. Characterization of abundant transcripts suggested important roles for genes involved in energy generation and antioxidant defense in adults. In particular, we proposed that adult heartworm likely adopted an anaerobic electron transfer-based energy generation system distinct from the aerobic pathway utilized by its mammalian host, making it a promising target in developing next generation macrofilaricides and other treatments. Our survey provided novel insights into the D. immitis transcriptome and laid a foundation for further comparative studies on biology, parasitism and evolution within the phylum Nematoda. q

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“…Obtaining ESTs from these and other nematode cDNA libraries contributes to an ever growing pool of transcriptomic data available in databases. Thorough comparisons of these EST data and focused bioinformatics searches based on expected characteristics of parasitism genes and expected functions achieved further identification of parasitism genes Dautova et al 2001;Jones et al 2003;Jones et al 2004;Mitreva-Dautova et al 2006;Vanholme et al 2006;Roze et al 2008). Although bioinformatics EST analyses can provide a priority list of candidate parasitism genes, these genes need to be verified.…”

Section: Intra-specific Transcriptomics Has Proven a Powerful Approacmentioning

confidence: 98%

Transcriptomes of Plant-Parasitic Nematodes

Jacob

Mitreva²

2011

Genomics and Molecular Genetics of Plant-Nematode Interactions

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Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii

Cited by 51 publications

References 50 publications

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

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

Identification and analysis of genes expressed in the adult filarial parasitic nematode Dirofilaria immitis

Transcriptomes of Plant-Parasitic Nematodes

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