Identification and molecular characterization of a β-1,4-endoglucanase gene (Rr-eng-1) from Rotylenchulus reniformis

Journal of Nematology

Volumn 42, Issue 4, 2010, Pages 342-351

  Wubben, Martin J ^a,b   Ganji, Satish ^b   Callahan, Franklin E ^a  

^a CROP SCIENCE RESEARCH LABORATORY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

Cellulase; Endoglucanase; Host parasitic relationship; Molecular biology; Parasitism gene; Phylogenetics; Reniform nematode; Rotylenchulus reniformis

Indexed keywords

HETERODERA GLYCINES; NEMATODA; ROTYLENCHULUS RENIFORMIS;

EID: 80054731430     PISSN: 0022300X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Abad, P., et al. 2008. Genome sequence of the metazoan plantparasitic nematode Meloidogyne incognita. Nature Biotechnology 26:909-915.
2. Agudelo, P., Robbins, R. T., Stewart, J. M., Bell, A., and Robinson, A. F. 2005. Histological observations of Rotylenchulus reniformis on Gossypium longicalyx and interspecific cotton hybrids. Journal of Nematology 37:444-447. (Pubitemid 43863827)
3. Bakhetia, M., Urwin, P. E., and Atkinson, H.J. 2007. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular PlantMicrobe Interactions 20:306-312. (Pubitemid 46281157)
4. Bannai, H., Tamada, Y, Maruyama, O., Nakai, K., and Miyano, S. 2002. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298-305. (Pubitemid 34183107)
5. Baum, T.J., Hussey, R. S., and Davis, E. L. 2007. Root-knot and cyst nematode parasitism genes: The molecular basis of plant parasitism. Pp. 17-43 in Setlow, J. K., ed. Genetic Engineering Volume 28. Springer Science.
6. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340:783-795. (Pubitemid 38829638)
7. Bird, A. F. 1984. Growth and moulting in nematodes: Moulting and development of the hatched larva of Rotylenchulus reniformis. Parasitology 89:107-119.
8. Blin, N., and Stafford, D. W. 1976. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Research 3:2303-2308.
9. Bliimenthal, T., and Steward, K 1997. RNA processing and gene structure. Pp. 117-149 in Riddle, D. L., Blumenthal, T., Meyer, B. J., and Priess, j. R., eds. C. Elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
10. Chen, Q., Rehman, S., Smant, C, and Jones, J. T. 2005. Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Molecular Plant-Microbe Interactions 18:621-625. (Pubitemid 40832028)
11. Danchin, E. G. J., Rosso, M.-N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B., and Abad, P. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proceedings of the National Academy of Science of the United States of America 107:17651-17656.
12. Davis, E. L., Hussey, R. S., Mitchum, M. G., and Baum, T.J. 2008. Parasitism proteins in nematode-plant interactions. Current Opinion in Plant Biology 11:360-366.
13. De Meutter, J., Vanholme, B., Bauw, G., Tytgat, T., Gheysen, G., and Gheysen, G. 2001. Preparation and sequencing of secreted proteins from the pharyngeal glands of the plant parasitic nematode Heterodera schachlii Molecular Plant Pathology 2:297-301. (Pubitemid 33065926)
14. Elling, A. A., Mitreva, M., Gai, X., Martin, J., Recknor.J., Davis, E. L., Hussey, R. S., Nettleton, D., McCarter, J. P., and Baum, T. J. 2009. Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 10:58-74.
15. Gao, B., Allen, R., Maier, T., Davis, E. L., Baum, T. J., and Hussey, R. S. 2002. Identification of a new B-l,4-endoglucanase gene expressed in the esophageal gland cells of Heterodera glycines. Journal of Nematology 34:12-15. (Pubitemid 34881723)
16. Gao, B., Allen, R., Davis, E. L., Baum, T. J., and Hussey, R. S. 2004. Developmental expression and biochemical properties of a β-1,4endoglucanase family in the soybean cyst nematode, Heterodera glycines. Molecular Plant Pathology 5:93-104. (Pubitemid 38370324)
17. Gilkes, N. R., Henrissat, B., Kilburn, D. G., Miller, Jr., R. C., and Warren, R. A.J. 1991. Domains in microbial B-1,4-glycanases: Sequence conservation, function, and enzyme families. Microbiological Reviews 55:303-315. (Pubitemid 21895156)
18. Goellner, M., Smant, G., De Boer.J. M., Baum, T.J., and Davis, E. L. 2000. Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. Journal of Nematology 32:154-165.
19. Goellner, M., Wang, X., and Davis, E. L. 2001. Endo-β-1,4-glucanase expression in compatible plant-nematode interactions. The Plant Cell 13:2241-2255. (Pubitemid 33044952)
20. Haegeman, A., Jacob, J., VanHolme, B., Kyndt, T., and Gheysen, G. 2008. A family of GHF5 endo-1,4-beta-glucanases in the migratory plantparasitic nematode Radopholus similis. Plant Pathology 57:581-590. (Pubitemid 351691948)
21. Haegeman, A., Kyndt, T., and Gheysen, G. 2010. The role of pseudoendoglucanases in the evolution of nematode cell wall-modifying proteins. Journal of Molecular Evolution 70:441-452.
22. Heald, C. M. 1975. Pathogenicity and histopathology of Rotylenchulus reniformis infecting cantaloup. Journal of Nematology 7:149-152.
23. Henrissat, B. 1991. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal 280:309-316.
24. Henrissat, B., Claeyssens, M., Tomme, P., Lemesle, L., and Mornon, J.-P. 1989. Cellulase families revealed by hydrophobic cluster analysis. Gene 81:83-95. (Pubitemid 19227537)
25. Hussey, R. S., and Barker, K. R. 1973. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Reporter 57:1025-1028.
26. Jenkins, W. R. 1964. A rapid centifugal-floatation technique for separating nematodes from soil. Plant Disease Reporter 48:692.
27. Keen, N. T., and Roberts, P. A. 1998. Plant parasitic nematodes: Digesting a page from the microbe book. Proceedings of the National Academy of Science of the United States of America 95:4789-4790. (Pubitemid 28208501)
28. Kyndt, T., Haegeman, A., and Gheysen, G. 2008. Evolution of GHF5 endoglucanase gene structure in plant-parasitic nematodes: no evidence for an early domain shuffling event. BMC Evolutionary Biology 8:305-320.
29. Ledger, T. N., Jaubert, S., Bosselut, N., Abad, P., and Rosso, M.-N. 2006. Characterization of a new β-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 382:121-128. (Pubitemid 44566437)
30. Liepman, A. H., Wightman, R., Geshi, N., Turner, S. R., and Serieller, H. V. 2010. Arabidopsis - a powerful model system for plant cell wall research. The Plantjournal 61:1107-1121.
31. Nakasono, K. 1973. Studies on post-embryonic development of the reniform nematode, Rotylenchulus reniformis Linford and Oliveira (Nematoda: Rotylenchulidae) I. Morphological changes of the molting larva of a parthenogenetic population. Applied Entomology and Zoology 8:83-96.
32. Rebois, R. V, Madden, P. A., and Eidridge, B.J. 1975. Some ultrastructural changes induced in resistant and susceptible soybean roots following infection by Rotylenchulus reniformis. Journal of Nematology 7:122-139.
33. Rehman, S., Butterbach, P., Popeijus, H., Overmars, H., Davis, E. L., Jones.J. T., Goverse, A., Bakker, J., and Smant, G. 2009. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis. Phytopathology 99:194-202.
34. Robinson, A. F., Inseria, R. N., Caswell-Chen, E. P., Vovlas, N., and Troccoli, A. 1997. Rotylenchulus species: Identification, distribution, host ranges, and crop plant resistance. Nematropica 27:127-180. (Pubitemid 127462416)
35. Rosso, M.-N., Favery, B., Piotte, C., Arthattd, L., De Boer, J. M., Hussey, R. S., Bakker, J., Baum, T. J., and Abad, P. 1999. Isolation of a cDNA encoding a β-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Molecular Plant-Microbe Interactions 12:585-591. (Pubitemid 29291951)
36. Smant, C, Stokkermans, J. P. W. G., Yan, Y, De Boer, J. M., Baum, T. J., Wang, X., Hussey, R. S., Gommers, F. J., Henrissat, B., Davis, E. L., Helder, J., Schots, A., and Bakker, J. 1998. Endogenous cellulases in animals: Isolation of 6-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proceedings of the National Academy of Science of the United States of America 95:4906-4911. (Pubitemid 28208523)
37. Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599. (Pubitemid 47236692)
38. Uehara, T., Kushida, A., and Momota, Y 2001. PCR-based cloning of two beta-1,4-endoglucanases from the root-lesion nematode Pratylenchus penetrans. Nematology 3:335-341. (Pubitemid 32996787)
39. Vovlas, N., and Lamberti, F. 1990. Histological alterations induced by Rotylenchulus reniformis on Coffea arabica roots. Nematologia Mediterranea 18:77-81.
40. Wang, X., Meyers, D., Yan, Y, Baum, T., Smant, C, Hussey, R., and Davis, E. 1999. In planta localization of a β-l,4-endoglucanase secreted by Heterodera glycines. Molecular Plant-Microbe Interactions 12:64-67. (Pubitemid 29015140)
41. Williamson, V M., and Hussey, R. S. 1996. Nematode pathogenesis and resistance in plants. The Plant Cell 8:1735-1745. (Pubitemid 27012401)
42. Wubben, M.J., Callahan, F. E., Hayes, R. W, andjenkins, J. N. 2008. Molecular characterization and temporal expression analyses indicate that the MIC (Meloidogyne Induced Cotton) gene family represents a novel group of root-specific defense-related genes in upland cotton (Gossypium hirsutum L.). Planta 228:111-123.
43. Wubben, M. J., Callahan, F. E., and Scheffler, B. E. 2010. Transcript analysis of sedentary parasitic females of the semi-endoparasitic nematode Rotylenchulus reniformis. Molecular and Biochemical Parasitology 172:31-40.
44. Yan, Y, Smant, G., Stokkermans, J., Qin, L., Hélder,J., Baum, T., Schots, A., and 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. (Pubitemid 28470323)
45. Yan, Y, Smant, G., and Davis, E. 2001. Functional screening yields a new β-1,4-endoglucanase gene from Heterodera glycines that may be the product of recent gene duplication. Molecular Plant-Microbe Interactions 14:63-71.