The plant apoplasm is an important recipient compartment for nematode secreted proteins

Journal of Experimental Botany

Volumn 62, Issue 3, 2011, Pages 1241-1253

  Vieira, Paulo ^a   Danchin, Etienne G J ^a   Neveu, Cédric ^a,c   Crozat, Carine ^a   Jaubert, Stéphanie ^a,d   Hussey, Richard S ^b   Engler, Gilbert ^a   Abad, Pierre ^a   De Almeida Engler, Janice ^a   Castagnone Sereno, Philippe ^a   Rosso, Marie Noëlle ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF GEORGIA   (United States)

^c UR1282   (France)

^d AGROCAMPUS OUEST   (France)

Author keywords

Apoplasm; effector; giant cell; immunocytochemistry; intercellular migration; Meloidogyne incognita; plant parasitic nematode

Indexed keywords

HELMINTH PROTEIN;

ANIMAL; ARABIDOPSIS; ARTICLE; CELL WALL; FEMALE; HOST PARASITE INTERACTION; METABOLISM; NEMATODE; PARASITOLOGY; PLANT DISEASE; PLANT ROOT; PROTEIN TRANSPORT;

ANIMALS; ARABIDOPSIS; CELL WALL; FEMALE; HELMINTH PROTEINS; HOST-PARASITE INTERACTIONS; NEMATODA; PLANT DISEASES; PLANT ROOTS; PROTEIN TRANSPORT; TYLENCHOIDEA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MELOIDOGYNE INCOGNITA; NEMATODA;

EID: 79251515474     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq352     Document Type: Article

References (56)

1. Abad P, Gouzy J, Aury JM, et al. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909-915.
2. Adam MAM, Phillips MA, Tzortzakakis EA, Blok VC. 2009. Characterisation of mjap genes encoding novel secretd proteins from the root-knot nematode, Meloidogyne javanica. Nematology 11, 253-265.
3. Bakhetia M, Urwin PE, Atkinson HJ. 2007. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular Plant-Microbe Interactions 20, 306-312.
4. Barcala M, García A, Cabrera J, Casson S, Lindsey K, Favery B, García-Casado G, Solano R, Fenoll C, Escobar C. 2010. Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. The Plant Journal 61, 698-712.
5. Bellafiore S, Briggs SP. 2010. Nematode effectors and plant responses to infection. Current Opinion in Plant Biology 13, 442-448.
6. Bird DM, Bird A. 2001. Plant-parasitic nematodes. In: Kennedy MW, Harnett W, eds. Parasitic nematodes. Wallinford, UK: CAB International, 139-166.
7. Brinkworth RI, Harrop SA, Prociv P, Brindley PJ. 2000. Host specificity in blood feeding parasites: a defining contribution by haemoglobin-degrading enzymes? International Journal for Parasitology 30, 785-790.
8. Caillaud M-C, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida Engler J, Abad P, Rosso M-N, Favery B. 2008. Root-knot nematodes manipulate plant cell functions during a compatible interaction. Journal of Plant Physiology 165, 104-113.
9. Castagnone-Sereno P, Semblat JP, Castagnone C. 2009. Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Molecular Genetics and Genomics 282, 547-554.
10. Chen Q, Rehman S, Smant G, Jones JT. 2005. Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Molecular Plant-Microbe Interactions 18, 621-625.
11. Curtis RHC. 1996. Identification and in situ and in vitro characterization of secreted proteins produced by plant-parasitic nematodes. Parasitology 113, 589-597.
12. Davis EL, Aron LM, Pratt LH, Hussey RS. 1992. Novel immunization procedures used to develop monoclonal antibodies that bind to specific structures in Meloidogyne spp. Phytopathology 82, 1244-1250.
13. Davis E, Hussey R, Mitchum M, Baum T. 2008. Parasitism proteins in nematode-plant interactions. Current Opinion in Plant Biology 11, 360-666.
14. De Almeida Engler J, Favery B, Engler G, Abad P. 2005. Loss of susceptibility as an alternative for nematode resistance. Current Opinion in Biotechnology 16, 112-117.
15. Ding X, Shields J, Allen R, Hussey RS. 1998. A secretory cellulose-binding protein cDNA cloned from the root-knot nematode (Meloidogyne incognita). Molecular Plant-Microbe Interactions 11, 952-959.
16. Dowen R, Engel J, Shao F, Ecker J, Dixon J. 2009. A family of bacterial cysteine protease type III effectors utilizes acylation-dependent and -independent strategies to localize to plasma membranes. Journal of Biological Chemistry 284, 15867-15879.
17. Doyle E, Lambert K. 2002. Cloning and characterisation of an esophageal-gland specific pectate lyase from the root-knot nematode Meloidogyne javanica. Molecular Plant-Microbe Interactions 15, 549-556.
18. Doyle EA, Lambert KN. 2003. Meloidogyne javanica chorismate mutase 1 alters plant cell development. Molecular Plant-Microbe Interactions 16, 123-131.
19. Elling A, Davis E, Hussey R, Baum T. 2007. Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. International Journal for Parasitology 37, 1269-1279.
20. Ellis J, Rafiqi M, Gan P, Chakrabarti A, Dodds P. 2009. Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens. Current Opinion in Plant Biology 12, 399-405.
21. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP, and related tools. Nature Protocols 2, 953-971.
22. Fragoso RR, Lourencxo IT, Batista JAN, Oliveira-Neto OB, Silva MCM, Rocha TL, Coutinho MV, Grossi-de-Sa MF. 2009. Meloidogyne incognita: molecular cloning and characterization of a cDNA encoding a cathepsin D-like aspartic proteinase. Experimental Parasitology 121, 115-123.
23. Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ. 2008. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. The Plant Cell 20, 3080-3093.
24. Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ. 2009. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiology 152, 968-984.
25. Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S. 2009. Emerging concepts in effector biology of plant-associated organisms. Molecular Plant-Microbe Interactions 22, 115-122.
26. Huang G, Dong R, Allen R, Davis E, Baum T, Hussey R. 2005. Developmental expression and molecular analysis of two Meloidogyne incognita pectate lyase genes. International Journal for Parasitology 35, 685-692.
27. Huang GZ, Dong RH, Allen R, Davis EL, Baum TJ, Hussey RS. 2006. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Molecular Plant-Microbe Interactions 19, 463-470.
28. Hussey RS. 1989. Disease-inducing secretions of plant-parasitic nematodes. Annual Review of Phytopathology 27, 123-141.
29. James KE, Asgian JL, Li ZZ, Ekici OD, Rubin JR, Mikolajczyk J, Salvesen GS, James CP. 2004. Design, synthesis, and evaluation of aza-peptide epoxides as selective and potent inhibitors of caspases-1, -3, -6, and -8. Journal of Medicinal Chemistry 47, 1553-1574.
30. Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette M-L, Renou JP, Abad P, Favery B. 2005. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. The Plant Journal 44, 447-458.
31. Jaubert S, Milac AL, Petrescu J, de Almeida-Engler J, Abad P, Rosso MN. 2005. In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Molecular Plant-Microbe Interactions 18, 1277-1284.
32. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park S-Y, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. The Plant Cell 22, 1388-1403.
33. Kronenberger J, Desprez T, Höfte H, Caboche M, Traas J. 1993. A methacrylate embedding procedure developed for immunolocalization on plant tissues is also compatible with in situ hybridization. Cell Biology International 17, 1013-1021.
34. Lopez de Mendoza ME, Abrantes IMO, Rowe J, Gowen S, Curtis RHC. 2002. Immunolocalisation in planta of secretions from parasitic stages of Meloidogyne incognita and M. hispanica. International Journal of Nematology 12, 149-154.
35. Marchler-Bauer A, Bryant SH. 2004. CD-Search: protein domain annotations on the fly. Nucleic Acids Research. 32, W327-W331.
36. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B. 2009. Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. The Plant Cell 21, 1273-1290.
37. Neveu C, Jaubert S, Abad P, Castagnone-Sereno P. 2003. A set of genes differentially expressed between avirulent and virulent Meloidogyne incognita near-isogenic lines encode secreted proteins. Molecular Plant-Microbe Interactions 16, 1077-1084.
38. Orion D, Franck A. 1990. An electron microscopy study of cell wall lysis by Meloidogyne javanica gelatinous matrix. Revue de Nématologie 13, 105-107.
39. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, Baum TJ, Mitchum MG, Davis EL. 2010. A nematode effector protein similar to annexins in host plants. Journal of Experimental Botany 61, 235-248.
40. Perry R. 1996. Chemoreception in plant-parasitic nematodes. Annual Review of Phytopathology 34, 181-199.
41. Pollastri G, Martin AJM, Mooney C, Vullo A. 2007. Accurate prediction of protein secondary structure and solvent accessibility by consensus combiners of sequence and structure information. BMC Bioinformatics 8, 201.
42. Rafiqi M, Gan PHP, Ravensdale M, Lawrence GJ, Elli JG, Jones DA, Hardham AR, Dodds PN. 2010. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. The Plant Cell 22, 2017-2032.
43. Rehman S, Postma W, Tytgat T, et al. 2009. A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Molecular Plant-Microbe Interactions 22, 330-340.
44. Rosso M-N, Favery B, Piotte C, Arthaud L, De Boer JM, Hussey RS, Bakker J, Baum TJ, Abad P. 1999. Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Molecular Plant-Microbe Interactions 12, 585-591.
45. Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, Goverse A, Smant G, Moffett P. 2009. The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathogens 5, e1000564.
46. Semblat JP, Rosso MN, Hussey RS, Abad P, Castagnone-Sereno P. 2001. Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 14, 72-79.
47. Sijmons PC, Grundler FMW, Von Mende N, Burrows PR, Wyss U. 1991. Arabidopsis thaliana as a new model host for plantparasitic nematodes. The Plant Journal 1, 245-254.
48. Sobczak M, Golinowski W, Grundler F. 1999. Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1, 363-374.
49. Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M, Vanhoutte I, Gheysen G, Van Criekinge W, Borgonie G, Coomans A. 2004. A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant parasitic cyst nematodes. Molecular Plant-Microbe Interactions 17, 846-852.
50. Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey R, Baum T, Davis E, Wang X, Mitchum M. 2010. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytologist 187, 1003-1017.
51. Wang X, Meyers D, Yan Y, Baum T, Smant G, Hussey R, Davis E. 1999. In planta localization of a b-1,4-endoglucanase secreted by Heterodera glycines. Molecular Plant-Microbe Interactions 12, 64-67.
52. Williamson V, Hussey R. 1996. Nematode pathogenesis and resistance in plants. The Plant Cell 8, 1735-1745.
53. Williamson AL, Brindley PJ, Knox DP, Hotez PJ, Loukas A. 2003. Digestive proteases of blood-feeding nematodes. Trends in Parasitology 19, 417-423.
54. Wyss U, Grundler FMW. 1992. Feeding behavior of sedentary plant parasitic nematodes. European Journal of Plant Pathology 98, 165-173.
55. Zdobnov EM, Apweiler R. 2001. InterProScan an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847-848.
56. Zhang Q, Bat G, Yang W, Li H, Xiong H. 2006. Pathogenic cellulase assay of pine wilt disease and immunological localization. Bioscience, Biotechnology, and Biochemistry 70, 2727-2732.