Secrets in secretions: Genes that control nematode parasitism of plants

Brazilian Journal of Plant Physiology

Volumn 14, Issue 3, 2002, Pages 183-194

  Hussey, Richard S ^a   Davis, Eric L ^b   Baum, Thomas J ^c  

^a UNIVERSITY OF GEORGIA   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Esophageal gland cells; Nematode parasitism; Parasitism genes; Parasitome; Secretion

Indexed keywords

EMBRYOPHYTA; EUKARYOTA; NEMATODA;

EID: 0036991145     PISSN: 16770420     EISSN: None     Source Type: Journal    
DOI: 10.1590/S1677-04202002000300002     Document Type: Short Survey

References (72)

1. Anderson RV, Byers JR (1975) Ultrastructure of the esophageal procorpus in the plant parasitic nematode, Tylenchorhynchus dubius, and functional aspects in relation to feeding. Can. J. Zool. 53:1581-1595.
2. Atkinson HJ, Harris PD (1989) Changes in nematode antigens recognized by monoclonal antibodies during early infections of soya beans with the cyst nematode Heterodera glycines. Parasitology 98:479-487.
3. Baum TJ, Hiatt A, Parrott WA, Pratt LH, Hussey RS (1996) Expression in tobacco of a functional monoclonal antibody specific to stylet secretions of the root-knot nematode. Mol. Plant-Microbe Interac. 9: 382-387.
4. Bird AF (1971) Specialized adaptation of nematodes to parasitism. In: Zuckerman BM, Mai WF, Rohde RA (eds), Plant Parasitic Nematodes Vol. II, pp.35-49. Academic Press, New York, USA.
5. Bird AF (1983) Changes in the dimensions of the esophageal glands in root-knot nematodes during the onset of parasitism. Int. J. Parasitol. 13:343-348.
6. Bird DMcK (1996) Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 82:881-888.
7. Böckenhoff A, Grundler FMW (1994) Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology 109:249-254.
8. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:243-293.
9. Dautova M, Rosso M-N, Abad P, Gommers FJ, 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.
10. Davis EL, Allen R, Hussey RS (1994) Developmental expression of esophageal gland antigens and their detection in stylet secretions of Meloidogyne incognita. Fund. Appl. Nematol. 17:255-262.
11. Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, Rosso M-N, Abad P (2000) Nematode parasitism genes. Annu. Rev. Phytopath. 38:341-372.
12. de Boer JM, Yan Y, Bakker J, Davis EL, Baum TJ (1998) In situ hybridization to messenger RNA of Heterodera glycines. J. Nematol. 30:309-312.
13. de Boer JM, Yan Y, Wang X, Smant G, Hussey RS, Davis EL, Baum TJ (1999) Developmental expression of secretory β-1,4-endoglucanases in the subventral esophageal glands of Heterodera glycines. Mol. Plant-Microbe Interac. 12:663-669.
14. de Boer JM, McDermott JP, Davis EL, Hussey RS, Smant G, Baum TJ (2002a) Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. J. Nematol. 33:9-11.
15. de Boer JM, McDermott JP, Wang X, Maier T, Qui F, Hussey RS, Davis EL, Baum TJ (2002b) The use of DNA microarrays for the developmental expression analysis of cDNAs from the oesophageal gland cell region of Heterodera glycines. Mol. Plant Pathol. 3:261-270.
16. de Jaeger, G, de Wilde C, Eeckhout D, Fiers E, Depicker A (2002) The plantibody approach: expression of antibody genes in plants to modulate plant metabolism or to obtain pathogen resistance. Plant Mol. Biol. 43:419-428.
17. de Meutter J, Vanhomle B, Bauw G, Tytgat T, Gheysen G, Gheysen G (2001) Preparation and sequencing of secreted proteins from the pharyngeal glands of the plant parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 2: 297-301.
18. Ding X, Shields JP, Allen RI, Hussey RS (1998) A secretory cellulase-binding protein cDNA cloned from the root-knot nematode (Meloidogyne incognita). Mol. Plant-Microbe Interac. 11:952-959.
19. Ding X, Shields JP, Allen RI, Hussey RS (2000) Molecular cloning and characterization of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int. J. Parasitol. 30:77-81.
20. Doyle EA, Lambert KN (2002) Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol. Plant-Microbe Interac. 15:549-556.
21. Endo BY (1984) Ultrastructure of the esophagus of larvae of the soybean cyst nematode, Heterodera glycines. Proc. Helminth. Soc. Wash. 51:1-24.
22. Endo BY (1991) Ultrastructure of initial responses of susceptible and resistant soybean roots to infection by Heterodera glycines. Revue de Nematol. 14:73-94.
23. Endo BY, Wergin WP (1988) Ultrastructure of the second-stage juvenile of the root-knot nematode, Meloidogyne incognita. Proc. Helminth. Soc. Wash. 55:286-316.
24. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
25. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001a) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode, Heterodera glycines. Mol. Plant-Microbe Interac. 14:1247-1254.
26. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001b) Molecular characterization and expression of two venom allergen-like secretory proteins from the soybean cyst nematode, Heterodera glycines. Int. J. Parasitol. 31:1617-1625.
27. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2002a) Defining a plant-parasitic nematode: a profile of putative parasitism genes expressed in the esophageal gland cells of Heterodera glycines. Nematology 4:218 (abstr).
28. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2002b) Identification of a new β-1,4-endoglucanase gene expressed in the subventral gland cells of Heterodera glycines. J. Nematol. 33:12-15.
29. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2002c) Characterisation and developmental expression of a chitinase gene in Heterodera glycines. Int. J. Parasitol. 32:1293-1300.
30. Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu. Rev. Phytopathol. 40:124-168.
31. Goellner M, Smant G, deBoer JM, Baum TJ, Davis EL (2000) Isolation of beta-1,4-endoglucanase genes of Globodera tabacum and their expression during parasitism. J. Nematol. 32:154-165.
32. Goellner M, Wang X, Davis EL (2001) Endo-beta-1,4-glucanase expression in compatible plant-nematode interactions. Plant Cell 13:2241-2255.
33. Goverse A, Davis EL, Hussey RS (1994) Monoclonal antibodies to the esophageal glands and stylet secretions of Heterodera glycines. J. Nematol. 26:251-259.
34. Greenbaum D, Luscombe NM, Jansen R, Qian J, Gerstein M (2001) Interrelating different types of genomic data, from proteome to secretome: 'oming in on function. Genome Res. 11:1463-1468.
35. Hawdon JM, Narasimhan S, Hotez PJ (1999) Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Mol. Biochem. Parasitol. 99:149-165.
36. Huang G, Gao B, Maier T, Davis EL, Baum TJ, Hussey RS (2002) Identification of putative parasitism genes expressed in the esophageal gland cells of Meloidogyne incognita. Nematology 4:220 (abstr.).
37. Hussey RS (1989) Disease-inducing secretions of plant parasitic nematodes. Annu. Rev. Phytopath. 27:123-141.
38. Hussey RS, Mims CW (1990) Ultrastructure of esophageal glands and their secretory granules in the root-knot nematode Meloidogyne incognita. Protoplasma 156:9-18.
39. Hussey RS, Paguio OR, Seabury F (1990) Localization and purification of a secretory protein from the esophageal glands of Meloidogyne incognita with monoclonal antibodies. Phytopathology 80:709-714.
40. Hussey RS, Mims CW (1991) Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita. Protoplasma 162:99-107.
41. Hussey RS, Davis EL, Ray C (1994) Meloidogyne stylet secretions. In: Lamberti F, De Giorgi C, Bird D Mck (eds), Advances in Molecular Plant Nematology. pp.233-249. Plenum Press, New York.
42. Hussey RS, Grundler FMW (1998) Nematode parasitism of plants. In: Perry RN, Wright DJ, (eds), Physiology and biochemistry of free-living and plant parasitic nematodes, pp.213-243. CAB International Press, England.
43. Jaubert S, Laffaire JB, Abad P, Rosso M-N (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Letters 522:109-112.
44. Karrer EE, Lincoln JE, Hogenhout S, Bennett AB, Bostock RM, Martineau DB, Lucas WJ, Gilchrist D, Alexander D (1995) In situ isolation of mRNA from individual plant cells: Creation of cell-specific cDNA libraries. Proc. Natl. Acad. Sci. USA 92:3814-3818.
45. Keen NT, Roberts PA (1998) Plant parasitic nematodes: Digesting a page from the microbe book. Proc. Natl. Acad. Sci. USA 95:4789-4790.
46. Klein RD, Gu X, Goddard A, Rosenthal A (1996) Selection for genes encoding secreted proteins and receptors. Proc. Natl. Acad. Sci. USA 93:7108-7113.
47. Lambert KN, Allen KD, Sussex IM (1999) Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol. Plant-Microbe Interac. 12:328-336.
48. Maggenti AR (1987) Adaptive biology of nematode parasites. In: Veech JA, Dickson DW, (eds), Vistas on Nematology, pp. 188-195. Hyattsville: Society of Nematologists.
49. Mazarei M, Ying Z, Houtz RL (1998) Functional analysis of the rubisco large subunit N-methyltransferase promoter from tobacco and its regulation by light in soybean hairy roots. Plant Cell Rep. 17:907-912.
50. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24:34-35.
51. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
52. Popeijus H, Blok V, Cardle L, Bakker E, Phillips MS, Helder J, Smant G, Jones J (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.
53. Popeijus HE, Overmars H, Jones J, Blok V, Goverse A, Helder J, Schots A, Bakker J, Smant G (2000b). Degradation of plant cell walls by nematodes. Nature 406:36-37.
54. Qin L, Overmars H, Helder J, Popeijus H, van der Voort JR, Groenink W, van P. Koert, 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 Interac. 13:830-836.
55. Qin L, Smant G, Bakker J, Helder J (2002) The identity and function of cyst nematode-secreted proteins in pathogenesis. In: Leong SA, Allen C, Tripplet E, (eds), Biology of Plant-Microbe Interactions, Vol. 3, pp.212-216, APS Press, St. Paul, MN.
56. Rebois RV (1980) Ultrastructure of a feeding peg and tube associated with Rotylenchulus reniformis in cotton. Nematologica 26:396-405.
57. Reed JD, Edwards DL, Gonzalez CF (1997) Synthetic peptide combinatorial libraries: a method for the identification of bioactive peptides against phytopathogenic fungi. Mol. Plant-Microbe Interac. 10:537-549.
58. Rosso M-N, Schouten A, Roosien J, Borst-Vrenssen T, Hussey RS, Gommers FJ, Bakker J, Schots A, Abad P (1996) Expression and functional characterization of a single-chain FV antibody directed against secretions involved in plant nematode infection process. Biochem. Biophys. Res. Commun. 220:255-263.
59. Rosso M-N, Piotte C, Favery B, Arthaud L, Hussey RS, de Boer JM, Baum TJ, Abad P (1999) Isolation of a cDNA encoding a β-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita during plant parasitism. Mol. Plant-Microbe Interac. 12:585-591.
60. Shields JP, Ding X, Hussey RS (1998) Microaspiration of esophageal gland contents from plant-parasitic nematodes. J. Nematol. 30:515 (Abstr.).
61. Shpigel E, Roiz L, Goren R, Shoseyov O (1998) Bacterial cellulose-binding domain modulates in vitro elongation of different plant cells. Plant Physiol. 117:1185-94
62. Smant G, Goverse A, Stokkermans JWPG, de Boer JM, Pomp H, Zilverentant JF, Overmars HA, Helder J, Schots A, Bakker J (1997) Potato root diffusate-induced secretion of soluble, basic proteins originating from the subventral esophageal glands of potato cyst nematodes. Phytopathology 87:839-845.
63. Smant G, Yan Y, Stokkermans JWPG, de Boer JM, Davis EL, Pomp H, Zilverentant JF, Overmars HA, Helder J, Hussey RS, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. USA 95:4906-4911.
64. Uehara T, Kushida A, Momota Y (2001) PCR-based cloning of two β-1,4-endoglucanases from the root-lesion nematode Pratylenchus penetrans. Nematology 3:335-341.
65. Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant-Microbe Interact. 15:747-752.
66. Von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.
67. Wang X, Meyers D, Yan Y, Baum T, Smant G, Hussey RS, Davis EL (1999) In planta localization of a β-1,4-endoglucanase secreted by Heterodera glycines. Mol. Plant-Microbe Interac. 12:64-67.
68. Wang X, Allen R, Ding X, Goellner M, Maier T, de Boer JM, Baum TJ, Hussey RS, Davis EL (2001) Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode, Heterodera glycines. Mol. Plant-Microbe Interac. 14: 536-544.
69. Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735-1745.
70. Yan Y, Smant G, Stokkermans J, Qin L, Helder J, Baum T, Schots A, Davis E (1998) Genomic organization of four β-1,4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications. Gene 220:61-70.
71. Yan Y, Smant G, Davis EL (2001) Functional screening yields a new β-1,4-endo glucanase gene from Heterodera glycines that may be the product of a recent gene duplication. Mol. Plant-Microbe Interac. 14:63-71.
72. Yan Y, Davis EL (2002) Characterisation of guanylyl cyclase genes in the soybean cyst nematode, Heterodera glycines. Int. J. Parasitol. 32:65-72.