A polygalacturonase of animal origin isolated from the root‐knot nematode <i>Meloidogyne incognita</i><sup>1</sup>

Jaubert, Stéphanie; Laffaire, Jean-Baptiste; Abad, Pierre; Rosso, Marie‐Noëlle

doi:10.1016/s0014-5793(02)02906-x

Cited by 123 publications

(88 citation statements)

References 20 publications

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“…Although generally absent from animals, this enzyme has been characterized in two phytophagous insects: Sitophilus oryzae (9), for which an acquisition via LGT from fungi has been proposed (10), and Phaedon cochleariae, in which the enzyme may be encoded by a gut digestive symbiont (11). In nematodes, polygalacturonase activity has been suspected in Ditylenchus dipsaci since the 1970s (12), and GH28 enzymes have been isolated and biochemically characterized in M. incognita (13). We identified polygalacturonase genes only in root-knot nematodes.…”

Section: Resultsmentioning

confidence: 99%

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.

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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: 99%

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.

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302

285

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“…Analysis of ESTs from a pre-parasitic second-stage juvenile cDNA library of G. rostochiensis identified a full-length cDNA that encoded a predicted protein with a signal peptide at its amino terminus that had strong homology to Class III pectate lyases of bacteria and fungi (Popeijus et al, 2000b). A putative pectate lyase cDNA also has been cloned from H. glycines and M. javanica (de Boer et al, 2002a;Doyle and Lambert, 2002) as has been a polygalacturonase cDNA from M. incognita (Jaubert et al, 2002). Localization of transcripts of the pectate lyases to the subventral esophageal gland cells in nematodes indicates the potential for secretion of a pectate lyase from the nematode stylet during early stages of plant parasitism.…”

Section: Rs Hussey Et Almentioning

confidence: 99%

Secrets in secretions: genes that control nematode parasitism of plants

Hussey

Davis

Baum

2002

Braz. J. Plant Physiol.

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The most evolutionary advanced adaptations for plant parasitism by nematodes are the products of parasitism genes expressed in their esophageal gland cells and secreted through their stylet into host tissue to control the complex process of parasitism. Molecular analyses of nematode parasitism genes are revealing the complexity of the tools that enable the nematode to attack plants, and the results paint a more elaborate picture of host cellular events under specific control by the parasite than previously hypothesized. Interestingly, the majority of the parasitism genes discovered encodes proteins unique to plant-parasitic nematodes. Identifying the nematode parasitome, i.e., the complete profile of parasitism gene products secreted through the nematode stylet during the parasitic cycle, is the key to understanding the molecular basis of nematode parasitism of plants. Such knowledge will identify vulnerable points in the parasitic process that can be interfered with to achieve nematode control to limit nematode-induced yield losses in crops.Key words: esophageal gland cells, nematode parasitism, parasitome, parasitism genes, secretion.Secredos em secreções: genes tque controlam o parasitismo de nematóides de plantas: As mais avançadas adaptações evolucionárias para o parasitismo de plantas por nematóides são os produtos dos genes de parasitismo expressos nas células da sua glândula esofagial e secretados através do estilete no tecido do hospedeiro, com a finalidade de controlar o complexo processo de parasitismo. Análises moleculares de genes de parasitismo de nematóides têm revelado a complexidade das ferramentas que os permitem atacar as plantas e também obter uma visão mais elaborada do que antes se tinha por hipótese, dos eventos celulares do hospedeiro sob controle específico do parasita. Interessantemente, a maioria dos genes de parasitismo de nematóides descobertos, codificam proteínas específicas para nematóides parasitas de plantas. Identificar o parasitoma do nematóide, isto é, o perfil completo dos produtos dos genes de parasitismo secretados através do estilete durante o ciclo parasítico, é a chave para a compreensão da base molecular do parasitismo de nematóides de plantas. Este conhecimento permitirá identificar os pontos vulneráveis no processo parasítico que podem sofrer interferência, a fim de se controlar o nematóide e limitar as perdas de produção que eles causam em plantas cultivadas.Palavras-chave: células da glândula esofogial, genes de parasitismo, parasitoma, parasitismo de nematóides, secreção.

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“…6]. Other genes thought to be involved in host-parasite interactions in plant parasitic nematodes are also thought to have been acquired by HGT from bacteria [7][8][9]. GHF5 cellulase genes have also been found in one migratory endoparasitic nematode Pratylenchus penetrans [10] that is related to cyst and root-knot nematodes.…”

Section: Introductionmentioning

confidence: 99%

A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus

Jones²,

et al. 2004

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We have characterized a family of GHF45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. The absence of such genes from other nematodes and their similarity to fungal genes suggests that they may have been acquired by horizontal gene transfer (HGT) from fungi. The cell wall degrading enzymes of other plant parasitic nematodes may have been acquired by HGT from bacteria. B. xylophilus is not directly related to other plant parasites and our data therefore suggest that horizontal transfer of cell wall degrading enzymes has played a key role in evolution of plant parasitism by nematodes on more than one occasion.

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A polygalacturonase of animal origin isolated from the root‐knot nematode Meloidogyne incognita¹

Cited by 123 publications

References 20 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

Secrets in secretions: genes that control nematode parasitism of plants

A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus

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A polygalacturonase of animal origin isolated from the root‐knot nematode Meloidogyne incognita1

Cited by 123 publications

References 20 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

Secrets in secretions: genes that control nematode parasitism of plants

A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus

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A polygalacturonase of animal origin isolated from the root‐knot nematode Meloidogyne incognita¹