Protease inhibitor expression in soybean roots exhibiting susceptible and resistant interactions with soybean cyst nematode

Journal of Nematology

Volumn 40, Issue 2, 2008, Pages 138-146

  Rashed, Nahed A ^a,b   MacDonald, Margaret H ^a   Matthews, Benjamin F ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b DESERT RESEARCH CENTER   (Egypt)

Author keywords

Host parasitic relationship; Molecular biology; Protease inhibitors; Resistance; RT PCR; Soybean; Soybean cyst nematode

Indexed keywords

GLYCINE MAX; HETERODERA GLYCINES; NEMATODA;

EID: 56849109010     PISSN: 0022300X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Abdeen, A., Virgos, A., Olivella, E., Villanueva, J., Aviles, X., Gabarra, R., and Prat, S. 2005. Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Molecular Biology 57:189-202.
2. Alkharouf, N., Khan, R., and Matthews, B. F. 2004. Analysis of expressed sequence tags from roots of resistant soybean infected by the soybean cyst nematode. Genome 47:380-388.
3. Alkharouf, N. W., Klink, V., Chouikha, I. B., Beard, H. S., MacDonald, M. H., Meyer, S., Knap, H. T., Khan, R. and Matthews, B. F. 2006. Microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224:838-852.
4. Alkharouf, N., and Matthews, B. F. 2004. SGMD: The soybean genomics and microarray database. Nucleic Acids Research 32:D398-D400.
5. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25:3389-3402.
6. Ashida, Y., Matsushima, A., Tsuru, Y., Hirota, T., and Hirata, T. 2000. Isolation and sequencing of a cDNA clone encoding a 20-kDa protein with trypsin inhibitory activity. Bioscience, Biotechnology and Biochemistry 64:1305-1309.
7. Botella, M. A., Xu, Y., Prabha, T. N., Zhao, Y., Narasimhan, M. L., Wilson, K. A., Nielsen, S. S., Bressan, R. A., and Hasegawa, P. M. 1996. Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiology 112:1201-1210.
8. Boulter, D., Edwards, G. A., Gatehouse, A. M. R., Gatehouse, J. A., and Hilder, V. A. 1990. Additive effects of different plant-derived insect resistance genes in transgenic tobacco plants Crop Protection 9:351-354.
9. Duan, X., Li, X., Xue, Q., Ab-El-Saae, M., Xu, D., and Wu, R. 1996. Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant. Nature Biotechnology 14:494-498.
10. Endo, B.Y. 1965. Histological responses of resistant and susceptible soybean varieties, and background cross progeny to entry and development of Heterodera glycines. Phytopathology 55:375-381.
11. Endo, B. Y. 1991. Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines. Revue Nematologie 14:73-94.
12. Endo, B. Y., and Veech, J. A. 1970. Morphology and histochemistry of soybean roots infected with Heterodera glycines. Phytopathology 60: 1493-1498.
13. Farmer, E. E., Johnson, R. R., and Ryan, C. A. 1992. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiology 98:995-1002.
14. Ferry, N., Jouanin, L. Ceci, R., Mulligan, A., Emami, K., Gatehouse, A. and Gatehouse, A. M. R. 2004. Impact of oilseed rape expressing the insecticidal serine protease inhibitor, mustard trypsin inhibitor-2 on the beneficial predator Pterostichus madidus. Molecular Ecology 14:337-349.
15. Gatehouse, J. A. 2002. Tansley review no. 140 Plant resistance towards insect herbivores: A dynamic interaction. New Phytologist 156: 145-169.
16. Gipson, I., Kim, K. S., and Riggs, R. D. 1971. An ultrastructural study of syncytium development in soybean roots infected with Heterodera glycines. Phytopathology 61:347-353.
17. Gotor, C., Pintor-Toro, J. A., and Romero, L. C. 1995. Isolation of a new member of the soybean Kunitz-type proteinase inhibitors. Plant Physiology 107:1015-1016.
18. Heibges, A., Glaczinski, H., Ballvora, A., Salamini, F., and Gebhardt, C. 2003. Structural diversity and organization of three gene families for Kunitz-type enzyme inhibitors from potato tubers (Solanum tuberosum L.). Molecular Genetics and Genomics 269:526-534
19. Hirata, T., Izumi, S., and Tsuji, S. 1999. A 20-kDa protein with the GTP and trypsin inhibitory activities from Glycine max. Bioscience, Biotechnology and Biochemistry 63:1816-1818.
20. Ithal, N., Recknor, J., Nettleton, D., Hearne, L., Maier, T., Baum, T.J., and Mitchum, M. G. 2007a. Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Molecular Plant Microbe Interactions 20:293-305.
21. Ithal, N., Recknor, J., Nettleton, D., Maier, T., Baum, T.J., and Mitchum, M. G. 2007b. Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Molecular Plant Microbe Interactions 20:510-525.
22. Johnson, R., Narvaez, J., An, G., and Ryan, C. A. 1989. Expression of proteinase inhibitors I and II in transgenic tobacco plants: Effects on natural defense against Manduca Sexta larvae. Proceedings of the National Academy of Science USA 86:9871-9875.
23. Jokufu, K. D., and Goldberg, R. B. 1989. Kunitz trypsin inhibitor genes are differentially expressed during the soybean life cycle and in transformed tobacco plants. The Plant Cell 1:1079-1093.
24. Jouanin, L., Bonade-Bottino, M., Girard, C., Morrot, G., and Giband, M. 1998. Transgenic plants for insect resistance. Plant Science 131:1-11.
25. Khan, R., Alkharouf, N., Beard, H. S., MacDonald, M., Chouikha, I., Meyer, S., Grefenstette, J., Knap, H., and Matthews, B. F. 2004. Resistance mechanisms in soybean: Gene expression profile at an early stage of soybean cyst nematode invasion. Journal of Nematology 36:241-248.
26. Kim, Y. H., Riggs, R. D., and Kim, K. S. 1987. Structural changes associated with resistance of soybean to Heterodera glycines. Journal of Nematology 19:177-187.
27. Klink, V. P., MacDonald, M. H., and Matthews, B. F. 2005. Gene expression in soybean syncytial cells formed by the soybean cyst nematode and isolated by laser-capture microdissection. Plant Molecular Biology. 59:969-983.
28. Klink, V. P., Overall, C. C., Alkharouf, N. W., MacDonald, M. H., and Matthews, B. F. 2007a. Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean roots infected by soybean cyst nematode (Heterodera glycines). Planta 226:1389-1409.
29. Klink, V. P., Overall, C. C., MacDonald, M. H., and Matthews, B. F. 2007b Changes in gene expression in soybean roots during the susceptible and resistant response to soybean cyst nematode (Heterodera glycines) infection. Planta 226:1423-1447.
30. Koiwa, H., Bressan, R. A., and Hasegawa, P. M. 1997. Regulation of protease inhibitors and plant defense. Trends in Plant Science 2:379-384.
31. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R, McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T.J., and Higgins, D. G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
32. Laskowski, M., and Kato, I. 1980. Protein inhibitors of proteinases. Annual Review of Biochemistry 49:593-626.
33. Lawrence, P. K., and Koundal, K. R. 2002. Plant protease inhibitors in control of phytophagous insects. Journal of Biotechnology 5: http://www.ejb.org/content/vol5/issue1/full/3
34. Lee, S. I., Lee, S. H., Koo, J. C., Chun, H. J., Lim, C. O., Mun, J. H., Song, Y. H., and Cho, M. J. 1999. Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Molecular Breeding 5:1-9.
35. -Delta;Delta;cT method. Methods 25:402-408.
36. Lopes, A. R., Juliano, M. A., Juliano, L., and Terra, W. R. 2004. Coevolution of insect trypsins and inhibitors. Archives of Insect Biochemistry and Physiology 55:140-152.
37. Mahalingam, R., and Skorupska, H. T. 1996. Cytological expression of early response to infection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:986-998.
38. Marchetti, S., Delledonne, M., Fogher, C., Chiaba, C., Chiesa, F., Savazzini, F., and Giordano, A. 2000. Soybean Kunitz, C-II and PI-IV inhibitor genes confer different levels of insect resistance to tobacco and potato transgenic plants. Theoretical and Applied Genetics 101: 519-526.
39. Matthews, B. F., Pilitt, K., and Klink, V. P. 2004. Molecular characterization of a soybean cyst nematode (Heterodera glycines) homolog of unc-87. Journal of Nematology 36:457-465.
40. McGurl, B., Mukherjee, S., Khan, M., and Ryan C. A. 1995. Characterization of two proteinase inhibitor (ATI) cDNAs from alfalfa leaves (Medicago saliva var. Vernema): The expression of ATI genes in response to wounding and soil microorganisms. Plant Molecular Biology 27:995-1001.
41. Mujer, C. V., Andrews, D. L., Manhart, J. R., Pierce, S. K., and Rumpho, M. E. 1996. Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proceedings of the National Academy of Science USA 93:12333-12338.
42. O'Callaghan, M., Glare, T. R., Burgess, E. P. J., and Malone, L. A. 2005 Effects of plants genetically modified for insect resistance on nontarget organisms. Annual Review of Entomology 50:271-292
43. Putoff, D. P., Ehrenfried, M. L., Vinyard, B. T., and Tucker, M. L. 2007. GeneChip profiling of transcriptional responses to soybean cyst nematode, Heterodera glycines, colonization of soybean roots. Journal of Experimental Botany 8:3405-3418.
44. Riggs, R. D., Kim, K. S., and Gipson, I. 1973. Ultrastructural changes in Peking soybeans infected with Heterodera glycines. Phytopathology 63:76-84.
45. Samac, D. A., and Smigocki, A. C. 2003. Expression of oryzacystatin I and II in alfalfa increases resistance to the root-lesion nematode. Phytopathology 93:799-804.
46. Sijmons, P. C., Atkinson, H. J., and Wyss, U. 1994. Parasitic strategies of root nematodes and associated host cell responses. Annual Review of Phytopathology 32:235-259.
47. Urwin, P. E., Atkinson, H. J., Waller, D. A., and McPherson, M. J. 1995. Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera pallida. The Plant Journal 8:121-131.
48. Urwin, P. E., McPherson, M. J., and Atkinson, H. J. 1998. Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta 204:472-479.
49. Vain, P., Worland, B., Clarke, M. C., Richard, G., Beavis, M., Liu, H., Kohli, A., Leech, M., Snape, J., Christou, P., and Atkinson, H. 1998. Expression of an engineered cysteine proteinase inhibitor (Oryzacystatin-IΔD86) for nematode resistance intransgenic rice plants. Theoretical and Applied Genetics 96:266-271.
50. Vila, L., Quilis, J., Meynard, D., Breitler, J. C., Marfa, V., Murillo, I., Vassal, J. M., Messeguer, J., Guideroni, E., and Segundo, B. S. 2005. Expression of the maize proteinase inhibitor (mpi) gene in rice plants enhances resistance against the striped stem borer (Chilo suppressalis): Effects on larval growth and insect gut proteinases. Plant Biotechnology Journal 3:187-202.
51. Wilson, R. F. 1987. Seed metabolism. Pp. 643-686 inJ. R. Wilcox, ed. Soybeans: Improvement, production, and uses. Madison, WI: American Society of Agronomy.
52. Wrather, J. A., and Koenning, S. R. 2006. Estimates of disease effects on soybean yields in the United States 2003 to 2005. Journal of Nematology 28:173-180.