Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis

Robertson, Lee; Robertson, W. M.; Sobczak, Mirosław; Helder, J.; Tétaud, Emmanuel; Ariyanayagam, Mark R.; Ferguson, Michael A. J.; Fairlamb, Alan H.; Jones, John T.

doi:10.1016/s0166-6851(00)00295-4

Cited by 102 publications

(66 citation statements)

References 21 publications

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“…In support, plant-parasitic nematodes themselves are believed to possess an antioxidant machinery to protect their bodies against ROS produced by the host. Putatively secreted enzymes to scavenge ROS, such as superoxide dismutase, CAT, peroxidase, and GPX, have been identified in root-knot and cyst nematodes (Molinari and Miacola, 1997;Robertson et al, 2000;Jones et al, 2004;Dubreuil et al, 2007). It could be that the developing syncytium, required for successful cyst nematode parasitism, needs ROS protection as a safeguard for nematode survival.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis Spermidine Synthase Is Targeted by an Effector Protein of the Cyst Nematode Heterodera schachtii

et al. 2009

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Cyst nematodes are sedentary plant parasites that cause dramatic cellular changes in the plant root to form feeding cells, socalled syncytia. 10A06 is a cyst nematode secretory protein that is most likely secreted as an effector into the developing syncytia during early plant parasitism. A homolog of the uncharacterized soybean cyst nematode (Heterodera glycines), 10A06 gene was cloned from the sugar beet cyst nematode (Heterodera schachtii), which is able to infect Arabidopsis (Arabidopsis thaliana). Constitutive expression of 10A06 in Arabidopsis affected plant morphology and increased susceptibility to H. schachtii as well as to other plant pathogens. Using yeast two-hybrid assays, we identified Spermidine Synthase2 (SPDS2), a key enzyme involved in polyamine biosynthesis, as a specific 10A06 interactor. In support of this protein-protein interaction, transgenic plants expressing 10A06 exhibited elevated SPDS2 mRNA abundance, significantly higher spermidine content, and increased polyamine oxidase (PAO) activity. Furthermore, the SPDS2 promoter was strongly activated in the nematode-induced syncytia, and transgenic plants overexpressing SPDS2 showed enhanced plant susceptibility to H. schachtii. In addition, in planta expression of 10A06 or SPDS2 increased mRNA abundance of a set of antioxidant genes upon nematode infection. These data lend strong support to a model in which the cyst nematode effector 10A06 exerts its function through the interaction with SPDS2, thereby increasing spermidine content and subsequently PAO activity. Increasing PAO activity results in stimulating the induction of the cellular antioxidant machinery in syncytia. Furthermore, we observed an apparent disruption of salicylic acid defense signaling as a function of 10A06. Most likely, increased antioxidant protection and interruption of salicylic acid signaling are key aspects of 10A06 function in addition to other physiological and morphological changes caused by altered polyamines, which are potent plant signaling molecules.Sedentary plant-parasitic nematodes are obligate biotrophs that meet their nutritional requirements solely from modified, but living, root cells of their host plants. The most economically important plantparasitic nematodes are the sedentary endoparasitic root-knot nematodes (Meloidogyne spp.) and cyst nematodes (Heterodera and Globodera spp.). The soybean cyst nematode (Heterodera glycines) and the closely related sugar beet cyst nematode (Heterodera schachtii) are of particular importance in U.S. agriculture.Cyst nematode infection involves the penetration of second-stage juveniles (J2) into host roots followed by intracellular migration to the vasculature, where the nematodes initiate specialized feeding structures called syncytia. Feeding site initiation and formation are characterized by complex morphological and physiological changes of the parasitized plant root cells. This process includes endoreduplication, cell wall modification and dissolution leading to cell fusion, disappearance of large vacuoles, inc...

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Section: Discussionmentioning

confidence: 99%

Arabidopsis Spermidine Synthase Is Targeted by an Effector Protein of the Cyst Nematode Heterodera schachtii

et al. 2009

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“…Four proteins identified in this study, GAPDH, enolase, peroxiredoxin, and elongation factor, are known to be secreted in spite of their lack of a signal peptide. For example, peroxiredoxin was immunolocalised to the extracellular surface of the potato cyst nematode despite lack of an apparent signal peptide [44]. Similarly, Edwards et al [45] immunolocalised enolase to Saccharomyces cerevisiae cell wall.…”

Section: Contamination or Alternative Secretory Pathway?mentioning

confidence: 97%

Proteomic analysis of the Arabidopsis thaliana cell wall

et al. 2002

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With the completion of the Arabidopsis genome, many hypothetical proteins have been predicted without any information on their expression, subcellular localisation and function. We have performed proteomic analysis of proteins sequentially extracted from enriched Arabidopsis cell wall fractions and separated by two-dimensional gel electrophoresis (2-DE). The proteins were identified by peptide mass fingerprinting using matrix-assisted laser desorption/ionisation-time of flight (MALDI-TOF) mass spectrometry and genomic database searches. This is part of a targeted exercise to establish the entire Arabidopsis secretome database. We report evidence for new proteins of unknown function whose existence had been predicted from genomic sequences and, furthermore, localise them to the cell wall. In addition, we observed an unexpected presence in the cell wall preparations of proteins whose known biochemical activity has never been associated with this compartment hitherto. We discuss the implications of these findings and present results suggesting a possible involvement of cell wall kinases in plant responses to pathogen attack.

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“…Those cell-wall degrading enzymes have been identiWed in numerous plantparasitic nematodes (Ledger et al 2006;Smant et al 1998) and these were extensively studied in the light of parasitism. Other unigenes putatively encode enzymes that can neutralize reactive oxygen (ROS) species, produced by the host as a defense mechanism in response to infection by the nematode (Dubreuil et al 2007;Jones et al 2004;Robertson et al 2000). Further, three unigenes show homology to fatty acid-and retinoid-binding proteins of parasitic nematodes.…”

Section: Unigenes Putatively Involved In Parasitismmentioning

confidence: 99%

Exploring the transcriptome of the burrowing nematode Radopholus similis

et al. 2008

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Radopholus similis is an important nematode pest on fruit crops in the tropics. Unraveling the transcriptome of this migratory plant-parasitic nematode can provide insight in the parasitism process and lead to more eYcient control measures. For the Wrst high throughput molecular characterization of this devastating nematode, 5,853 expressed sequence tags from a mixed stage population were generated. Adding 1,154 tags from the EST division of GenBank for subsequent analysis, resulted in a total of 7,007 ESTs, which represent approximately 3,200 genes. The mean G + C content of the nucleotides at the third codon position (GC3%) was calculated to be as high as 64.8%, the highest for nematodes reported to date. BLAST-searches resulted in about 70% of the clustered ESTs having homology to (DNA and protein) sequences from the GenBank database, whereas one-third of them did not match to any known sequence. Roughly 40% of these latter sequences are predicted to be coding, representing putative novel protein coding genes. Functional annotation of the sequences by GO annotation revealed the abundance of genes involved in reproduction and development, which reXects the nematode population biology. Genes with a role in the parasitism process are identiWed, as well as genes essential for nematode survival, providing information useful for parasite control. No evidence was found for the presence of trans-spliced leader sequences commonly occurring in nematodes, despite the use of various approaches. In conclusion, we found three diVerent sources for the EST sequences: the majority has a nuclear origin, approximately 1% of the EST sequences are derived from the mitochondrial transcriptome, and interestingly, 1% of the tags are with high probability derived from Wolbachia, providing the Wrst molecular indication for the presence of this endosymbiont in a plant-parasitic nematode.Keywords Expressed sequence tag analysis · Trans-spliced leader · Parasitism · G + C content · Wolbachia · Endoparasitic migratory nematode

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Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis

Cited by 102 publications

References 21 publications

Arabidopsis Spermidine Synthase Is Targeted by an Effector Protein of the Cyst Nematode Heterodera schachtii

Arabidopsis Spermidine Synthase Is Targeted by an Effector Protein of the Cyst Nematode Heterodera schachtii

Proteomic analysis of the Arabidopsis thaliana cell wall

Exploring the transcriptome of the burrowing nematode Radopholus similis

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