Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida

Molecular Plant Pathology

Volumn 10, Issue 6, 2009, Pages 815-828

  Jones, John T ^a   Kumar, Amar ^a,e   Pylypenko, Liliya A ^b   Thirugnanasambandam, Amarnath ^a   Castelli, Lydia ^a,f   Chapman, Sean ^a   Cock, Peter J A ^a   Grenier, Eric ^c   Lilley, Catherine J ^d   Phillips, Mark S ^a   Blok, Vivian C ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b Ukrainian Academy of Agrarian Sciences Kiev   (Ukraine)

^c AGROCAMPUS OUEST   (France)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e UNIVERSITY OF DELHI   (India)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HELMINTH PROTEIN;

ANIMAL; ARTICLE; BIOLOGY; EXPRESSED SEQUENCE TAG; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MOLECULAR GENETICS; NEMATODE; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; POTATO;

ANIMALS; COMPUTATIONAL BIOLOGY; EXPRESSED SEQUENCE TAGS; HELMINTH PROTEINS; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; SOLANUM TUBEROSUM; TYLENCHOIDEA;

GLOBODERA PALLIDA; SOLANUM TUBEROSUM;

EID: 70350231897     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00585.x     Document Type: Article

References (55)

1. Abad, P., Gouzy, J., Aury, J.-M., Castagnone-Sereno, P., Danchin, E.G.J., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V.C., Caillaud, M.-C., Coutinho, P.M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J.V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T.R., Markov, G.V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., Sallet, E., Segurens, B., Steinbach, D., Tytgat, T., Ugarte, E., van Ghelder, C., Veronico, P., Baum, T.J., Blaxter, M., Bleve-Zacheo, T., Davis, E.L., Ewbank, J.J., Favery, B., Grenier, E., Henrissat, B., Jones, J.T., Laudet, V., Maule, A.G., Quesneville, H., Rosso, M.N., Schiex, T., Smant, G., Weissenbach, J. Wincke, P. (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26, 909 915.
2. Barrett, J. Wright, D.J. (1998) Intermediary metabolism. In : The Physiology and Biochemistry of Free-Living and Plant-Parasitic Nematodes (Perry, R.N. Wright, D.J., eds), pp. 331 353. Oxford : CABI Publishing.
3. Bird, A.F. Bird, J. (1991) The Structure of Nematodes, 2nd edn. London : Academic Press.
4. Blanchard, A., Esquibet, M., Fouville, D. Grenier, E. (2005) Ranbpm homologues characterized in the cyst nematodes Globodera pallida and Globodera 'mexicana Physiol. Mol. Plant Pathol. 67, 15 22.
5. Chen, Q., Rehman, S., Smant, G. Jones, J.T. (2005) Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Mol. Plant-Microbe Interact. 18, 621 625.
6. Cock, P.J., Antao, T., Chang, J.T., Chapman, B.A., Cox, C.J., Dalke, A., Friedberg, I., Hamelryck, T., Kauff, F., Wilczynski, B. de Hoon, M.J. (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics, 25, 1422 1423.
7. Conesa, A., Gotz, S., Garcia-Gomez, M., Terol, J., Talon, M. Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674 3676.
8. Dautova, M., Rosso, M-N., Abad, P., Gommers, F.J., Bakker, J. Smant, G. (2001) Single pass cDNA sequencing - a powerful tool to analyse gene expression in preparasitic juveniles of the southern root-knot nematode Meloidogyne incognita. Nematology, 3, 129 139.
9. Davis, E.L., Hussey, R.S., Goellner-Mitchum, M. Baum, T.J. (2008) Parasitism proteins in nematode-plant interactions. Curr. Opin. Plant Biol. 11, 1 7.
10. Elling, A.A., Davis, E.L., Hussey, R.S. Baum, T.J. (2007) Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. Int. J. Parasitol. 37, 1269 1279.
11. Elling, A.A., Mitreva, M., Gai, X., Martin, J., Recknor, J., Davis, E.L., Hussey, R.S., Nettleton, D., McCarter, J.P. Baum, T.J. (2009) Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 10, 58.
12. Emmanuelsson, O., Brunak, S., von Heijne, G. Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953 971.
13. Furlanetto, C., Cardle, L., Brown, D.J.F. Jones, J.T. (2005) Analysis of expressed sequence tags from the ectoparasitic nematode Xiphinema index. Nematology, 7, 95 104.
14. Gao, B., Allen, R., Maier, T., Davis, E.L., Baum, T.J. Hussey, R.S. (2003) The parasitome of the phytonematode Heterodera glycines. Mol. Plant-Microbe Interact. 16, 720 726.
15. Gheysen, G. Jones, J.T. (2006) Molecular aspects of plant-nematode interactions. In : Plant Nematology (Perry, R.N. Moens, M., eds), pp. 234 254. Wallingford : CABI Publishing.
16. Harcus, Y.M., Parkinson, J., Fernandez, C., Daub, J., Selkirk, M., Blaxter, M.L. Maizels, R.M. (2004) Signal sequence analysis of expressed sequence tags from the nematode Nippostrongylus brasiliensis and the evolution of secreted proteins in parasites. Genome Biol. 5, R39.
17. Huang, G., Gao, B., Maier, T., Allen, R., Davis, E.L., Baum, T.J. Hussey, R.S. (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 16, 376 381.
18. Huang, X. Madan, A. (1999) CAP3: a DNA sequence assembly program. Genome Res. 9, 868 877.
19. Hussey, R.S. Mims, C.W. (1990) Ultrastructure of oesophageal glands and their secretory granules in the root knot nematode Meloidogyne incognita. Protoplasma, 165, 9 18.
20. Jacob, J., Mitreva, M., Vanholme, B. Gheysen, G. (2008) Exploring the transcriptome of the burrowing nematode Radopholus similis. Mol. Gen. Genom. 280, 1 17.
21. Jasmer, D.P., Roth, J. Myler, P.J. (2001) Cathepsin B-like cysteine proteases and Caenorhabditis elegans homologues dominate gene products expressed in adult Haemonchus contortus intestine. Mol. Biochem. Parasitol. 116, 159 169.
22. Jaubert, S., Laffaire, J.B., Abad, P. Rosso, M-N. (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 522, 109 112. (Pubitemid 34722507)
23. Johnstone, I.L. Barry, J.D. (1996) Temporal reiteration of a precise gene expression pattern during nematode development. EMBO J. 15, 3633 3639.
24. Jones, J.T., Furlanetto, C., Bakker, E., Banks, B., Blok, V.C., Chen, Q. Prior, A. (2003) Characterisation of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol. Plant Pathol. 4, 43 50.
25. Jones, J.T., Smant, G. Blok, V.C. (2000) SXP/RAL2 proteins of the potato cyst nematode Globodera rostochiensis: secreted proteins of the hypodermis and amphids. Nematology, 2, 887 893.
26. Kennedy, M.W. (2000) The nematode polyprotein allergens/antigens. Parasitol. Today, 16, 373 380.
27. Kikuchi, T., Aikawa, T., Kosaka, H., Ogura, N. Jones, J.T. (2007) EST analysis of the pine wood nematodes Bursaphelenchus xylophilus and B. mucronatus. Mol. Biochem. Parasitol. 155, 9 17.
28. Kikuchi, T., Jones, J.T., Aikawa, T., Kosaka, H. Ogura, N. (2004) A family of GHF45 cellulases from the pine wood nematode Bursaphelenchus xylophilus. FEBS Lett. 572, 201 205.
29. Kikuchi, T., Shibuya, H., Aikawa, T. Jones, J.T. (2006) Cloning and characterization of pectate lyases secreted by the pine wood nematode Bursaphelenchus xylophilus. Mol. Plant-Microbe Interact. 19, 280 287.
30. Kikuchi, T., Shibuya, H. Jones, J.T. (2005) Molecular and biochemical characterization of an endo-β-1,3-glucanase from the pine wood nematode Bursaphelenchus xylophilus. Biochem. J. 389, 117 125.
31. Kramer, J.M. (1997) Extracellular matrix. In : C. elegans II (Riddle, D.L., Blumenthal, T., Meyer, B.J. Priess, J.R., eds), pp. 471 500. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
32. Krogh, A., Larsson, G., von Heijne, G. and Sonnhammer, E.L.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567 580.
33. Lambert, K.N., Allen, K.D. Sussex, I.M. (1999) Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol. Plant-Microbe Interact. 12, 328 336.
34. Liu, Y., Schiff, M., Marathe, R. Dinesh-Kumar, S.P. (2002) Tobacco Rar1, EDS1, and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415 429.
35. McCarter, J.P., Mitreva, M.D., Martin, J., Dante, M., Wylie, T., Rao, U., Pape, D., Bowers, Y., Theising, B., Murphy, C.V., Kloek, A.P., Chiapelli, B.J., Clifton, S.W., Bird, D.M. Waterston, R.H. (2003) Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol. 4, R26.
36. Minnis, S.T., Haydock, P.P.J., Ibrahim, S.K., Grove, I.G., Evans, K. Russell, M.D. (2002) Potato cyst nematodes in England and Wales - occurrence and distribution. Ann. Appl. Biol. 140, 187 195.
37. Mitreva, M., Blaxter, M.L., Bird, D.M. McCarter, J.P. (2005) Comparative genomics of nematodes. Trends Genet. 21, 573 581.
38. Mitreva, M., Elling, A.A., Dante, M., Kloek, A.P., Kalyanaraman, A., Aluru, S., Clifton, S.W., Bird, D.M., Baum, T.J. McCarter, J.P. (2004) A survey of SL-1 spliced transcripts from the root lesion nematode Pratylenchus penetrans. Mol. Gen. Genom. 272, 138 148.
39. Mulvenna, J., Hamilton, B., Nagaraj, S.H., Smyth, D., Loukas, A. Gorman, J.J. (2009) Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm Ancylostoma caninum. Mol. Cell. Proteom. 8, 109 121.
40. Parkinson, J., Anthony, A., Wasmuth, J., Schmid, R., Hedley, A. Blaxter, M.L. (2004a) PartiGene - constructing partial genomes. Bioinformatics, 20, 1398 1404.
41. Parkinson, J., Mitreva, M., Whitton, C., Thomson, M., Daub, J., Martin, J., Schmid, R., Hall, N., Barrell, B., Waterston, R.H., McCarter, J.P. Blaxter, M.L. (2004b) A transcriptomic analysis of the Phylum Nematoda. Nat. Genet. 36, 1259 1267.
42. Popeijus, H., Blok, V.C., Cardle, L., Bakker, E., Phillips, M.S., Helder, J., Smant, G. Jones, J.T. (2000a) Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and G. pallida using the expressed sequence tag approach. Nematology, 2, 567 574.
43. Popeijus, H., Overmars, H., Jones, J.T., Blok, V.C., Goverse, A., Helder, J., Bakker, J., Schots, A. Smant, G. (2000b) Non-symbiotic degradation of plant cell walls by animals. Nature, 406, 36 37.
44. Prior, A.E., Jones, J.T., Blok, V.C., Beauchamp, J., McDermott, L., Cooper, A. Kennedy, M.W. (2001) A surface-associated retinol- and fatty acid-binding protein (GpLBP20) from the potato cyst nematode Globodera pallida - lipid binding activities, structural analysis and expression pattern. Biochem. J. 356, 387 394.
45. Qin, L., Kudla, U., Roze, E., Goverse, A., Popeijus, H., Nieuwland, J., Overmars, H., Jones, J.T., Schots, A., Smant, G., Bakker, J. Helder, J. (2004) Identification of a functional expansin, a non-enzymatic, cell wall-loosening agent, from the plant parasitic nematode Globodera rostochiensis. Nature, 427, 30.
46. Qin, L., Overmars, B., Helder, J., Popeijus, H., Van der Voort, J.R., Groenink, W., Van Koert, P., Schots, A., Bakker, J. Smant, G. (2000) An efficient cDNA-AFLP-based strategy for the identification of putative pathogenicity factors from the potato cyst nematode Globodera rostochiensis. Mol. Plant-Microbe Interact. 13, 830 836.
47. Rehman, S., Postma, W., Tytgat, T., Prins, P., Qin, L., Overmars, H., Vosson, J., Spiridon, L.N., Petrescu, A.J., Goverse, A., Bakker, J. Smant, G. (2009) A secreted SPRY domain-containing protein from the plant parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Mol. Plant-Microbe Interact. 22, 330 340.
48. Roze, E., Hanse, B., Mitreva, M., Vanholme, B., Bakker, J. Smant, G. (2008) Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol. Plant Pathol. 9, 1 10.
49. Sacco, M.A., Koropacka, K., Grenier, E., Jaubert, M.J., Blanchard, A., Goverse, A., Smant, G. Moffett, P. (2009) The cyst nematode SPRYSEC protein RBP-I elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathogens. 5 (8 e1000564.
50. Scholl, E.H., Thorne, J.L., McCarter, J.P. Bird, D.M. (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol. 4, R39.
51. Tytgat, T., Vanholme, B., De Meutter, J., Claeys, M., Couvreur, M., Vanhoutte, I., Gheysen, G., Van Criekinge, W., Borgonie, G., Coomans, A. Gheysen, G. (2004) A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic nematodes. Mol. Plant-Microbe Interact. 17, 846 852.
52. Valentine, T., Shaw, J., Blok, V.C., Phillips, M.S., Oparka, K.J. Lacomme, C. (2004) Efficient virus-induced gene silencing in roots using a modified tobacco rattle virus vector. Plant Physiol. 136, 3999 4009.
53. Vanholme, B., Mitreva, M., Van Criekinge, W., Logghe, M., Bird, D., McCarter, J. Gheysen, G. (2006) Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii. Parasitol. Res. 98, 414 424.
54. Vercauteren, I., Geldhof, P., Peelaers, I., Claerebout, E., Berx, G. Vercruysse, J. (2003) Identification of excretory-secretory products of larval and adult Ostertagia ostertagi by immunoscreening of cDNA libraries. Mol. Biochem. Parasitol. 126, 201 208.
55. Wang, X., Allen, R., Ding, X., Goellner, M., Maier, T., de Boer, J.M., Baum, T.J., Hussey, R.S. Davis, E.L. (2001) Signal peptide selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 14, 536 544. (Pubitemid 32235585)