Degradation of plant cell walls by a nematode

Popeijus, Herman E.; Overmars, H.A.; Jones, John T.; Blok, Vivian C.; Goverse, A.; Helder, J.; Schots, A.; Bakker, J.; Smant, G.

doi:10.1038/35017641

Cited by 154 publications

(126 citation statements)

References 8 publications

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“…In root-knot nematodes, PL3s are present as multigenic families in both M. incognita and Meloidogyne hapla (7,14). Functional PL3's have also been isolated in cyst nematodes (15,16) and in Aphelenchoidea. Nematodes that belong to this last Spectrum of the presence in nematodes is indicated according to the taxonomy in SI Appendix, Fig.…”

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.

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: 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.

302

285

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“…However, this approach has limited potential because it predominately identifies only parasitism genes whose translation products are obviously related to parasitism, like cell-wall digesting enzymes (Popeijus et al, 2000a;Dautova et al, 2001). 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).…”

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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“…Even though pinewood nematode infected trees usually wither and die within a couple of months (Mamiya, 1975), we still do not understand the molecular and cellular pathophysiology underlying the abilities of pinewood nematodes to infection and propagate in the trees. However, the presence of diverse cell wall degrading enzymes such as endoglucanases (Kikuchi et al, 2004;Smant et al, 1998), pectate lyases (Kikuchi et al, 2006;Popeijus et al, 2000) and expansins (EXPs) (Kikuchi et al, 2009) that to play crucial roles in initiation and progression of the plant diseases are present in B. xylophilus genomes suggested that secreted cell wall degrading enzymes from B. xylophilus may be important factors involved with infections and propagation in host trees.…”

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confidence: 99%

Identification and Characterization of Expansins from Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae)

Lee¹,

Seo²,

Kang³

et al. 2012

The Plant Pathology Journal

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We identified two novel expansin (EXP) genes in the expressed sequence tag database of Bursaphelenchus xylophilus, designated as Bx-EXPB2 and -EXPB3. Novel Bx-EXPBs encoded 150 amino acids and their similarities in coding sequence were 70.7−84.0% to the previously reported EXPB1 of B. xylophilus. Bx-EXPB2 and Bx-EXPB3 were clustered with Bx-EXPB1 and Bm-EXPB1, respectively, forming the independent phylogeny with other nematode EXPs. All identified Bx-EXPBs contained the signal peptide and were only expressed during the propagative stage, suggesting that they are secreted to facilitate nematode migration through hosts by loosening cell walls during infection. Quantitative real-time PCR analysis showed that the relative accumulation of Bx-EXPB3 mRNAs was the highest among the three Bx-EXPs examined and the order of mRNA accumulation was as follows: Bx-EXPB3 > Bx-EXPB2 >> Bx-EXPB1. Homology modeling of BxEXPBs showed that the structurally optimum template was EXLX1 protein of Bacillus subtilis, whichshared residues essential for catalytic activity with Bx-EXPB1 and Bx-EXPB2 except for Bx-EXPB3. Taken together, Bx-EXPB1 and Bx-EXPB2 may be involved migration through plant tissues and play a role in pathogenesis.

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Degradation of plant cell walls by a nematode

Cited by 154 publications

References 8 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

Identification and Characterization of Expansins from Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae)

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