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Recent Studies on Development of Transgenic Plants Induced Root-Knot Nematode Resistance by RNA Interference Suppression of Nematode Genes and Nematode Prevention

뿌리혹선충 유전자의 RNA 간섭 억제에 의한 선충저항성 식물 개발 및 선충방제의 최근 연구 동향

  • Received : 2009.10.19
  • Published : 2010.04.01

Abstract

Root-knot nematodes cause billions of dollars in crop losses annually have a broad range of host over 2,000 species of plants. These nematodes are known as obligate, sedentary endo-parasites in a plant host to feed upon to complete their life cycle. To prevent the plant parasitic nematode, methyl bromide was widely applied as a soil fumigant. Other strategies to prevent or control nematodes involve RNAi-mediated suppression, R gene transformation, natural products or chemical treatments, the expression of peptide or proteins in susceptible plants, and others. Over the last decade, the entry in GenBank for Meloidogyne reveals 73,340 ESTs and recently two complete Meloidogyne spp. genomes sequences have simultaneously been presented by two groups. Recent works have demonstrated the effect of RNAi suppression to nematode target genes. These results will provide novel members of genes as a foundation for studies focused on understanding the function of M. incognita nematode genes as well as for the development of novel target genes for parasite control. Thus the successful development of biotechnology-derived plants with nematode resistance will result in large yield benefits for producers as well as environmental benefits and will accelerate the research related to pathogensresistant crops.

Keywords

References

  1. Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G, et al. 2008. Genome sequence of the metazoan plantparasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26: 909-915. https://doi.org/10.1038/nbt.1482
  2. Bakhetia, M., Charlton, W., Atkinson, H. J. and McPherson, M. J. 2005. RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol. Plant Microbe. Interact. 18: 1099-1106. https://doi.org/10.1094/MPMI-18-1099
  3. Baum, T. J., Hiatt, A., Parrott, W. A., Pratt, L. H. and Hussey, R. S. 1996. Expression in tobacco of a functional monoclonal antibody specific to stylet secretions of the root-knot nematode. Mol. Plant Microbe. Interact. 9: 382-387. https://doi.org/10.1094/MPMI-9-0382
  4. Bellafiore, S., Shen, Z., Rosso, M. N., Abad, P., Shih, P. and Briggs, S. P. 2008. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS. Pathog. 4: e1000192. https://doi.org/10.1371/journal.ppat.1000192
  5. Chen, R. G., Zhang, L. Y., Zhang, J. H., Zhang, W., Wang, X., Ouyang, B., Li, H. X. and Ye, Z. B. 2006. Functional characterization of Mi, a root-knot nematode resistance gene from tomato (Lycopersicon esculentum L.). J. Int. Plant Biol. 48: 1458-1465. https://doi.org/10.1111/j.1744-7909.2006.00354.x
  6. Chitwood, D. J. 2002. Phytochemical based strategies for nematode control. Annu. Rev. Phytopathol. 40: 221-249. https://doi.org/10.1146/annurev.phyto.40.032602.130045
  7. Dropkin, V. H. 1969. Cellular responses of plants to nematode infections. Annu. Rev. Phytopathol. 7: 101-122. https://doi.org/10.1146/annurev.py.07.090169.000533
  8. Dubreuil, G., Magliano, M., Deleury, E., Abad, P. and Rosso, M. N. 2007. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol. 176: 426-436. https://doi.org/10.1111/j.1469-8137.2007.02181.x
  9. Fairbaim, D. J., Cavallaro, A. S., Bernard, M., Mahalinga-Iyer, J., Graham, M. W. and Botella, J. R. 2007. Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta. 226: 1525-1533. https://doi.org/10.1007/s00425-007-0588-x
  10. Fanelli, E., Di Vito, M., Jones, J. T. and De Giorgi, C. 2005. Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene. 349: 87-95.
  11. Fioretti, L., Porter, A, Haydock, P. J. and Curtis, R. 2002. Monoclonal antibodies reactive with secreted-excreted products from the amphids and the cuticle surface of Globodera pallida affect nematode movement and delay invasion of potato roots. Int. J Parasitol. 32: 1709-1718. https://doi.org/10.1016/S0020-7519(02)00178-9
  12. Fosu-Nyarko, J., Jones, M. G. and Wang, Z. 2009. Functional characterization of transcripts expressed in early-stage Meloidogyne javanica-induced giant cells isolated by laser microdissection. Mol. Plant Pathol. 10: 237-248. https://doi.org/10.1111/j.1364-3703.2008.00526.x
  13. Gleason, C. A., Liu, Q. L. and Williamson, V. M. 2008. Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol. Plant Microbe Interact. 21: 576-585. https://doi.org/10.1094/MPMI-21-5-0576
  14. Goddijn, O. J., Lindsey, K., van der Lee, F. M., Klap, J. C. and Sijmons, P. C. 1993. Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter- gusA fusion constructs. Plant J. 4: 863-873. https://doi.org/10.1046/j.1365-313X.1993.04050863.x
  15. Goggin, F. L., Shah, G., Williamson, V. M. and Ullman, D. E. 2004. Instability of Mi-mediated nematode resistance in transgenic tomato plants. Mol. Breeding 13: 357-364. https://doi.org/10.1023/B:MOLB.0000034090.73857.b1
  16. Hannon, G. J. 2002. RNA interference. Nature 418: 244-251. https://doi.org/10.1038/418244a
  17. Hartman, K. M. and Sasser, J. N. 1985. Identification of Meloidogyne species on the basis of differential host test and perineal-pattern morphology. In: Barker, K. R., Carter, C. C. and Sasser, N. (Eds). An Advalued Treatise on Meloidogyne. Vol. II. Methodology, Raleigh, USA, North Carolina State University: 69-77.
  18. Huang, G., Allen, R., Davis, E. L., Baum, T. J. and Hussey, R. S. 2006. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential rootknot nematode parasitism gene. Proc. Natl. Acad. Sci. USA 103: 14302-14306. https://doi.org/10.1073/pnas.0604698103
  19. Huang, G., Gao, B., Maier, T., Allen, R., Davis, E. L., Baum, T. J. and 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. https://doi.org/10.1094/MPMI.2003.16.5.376
  20. Jacquet, M., Bongiovanni, M., Martinez, M., Verschave, P., Wajnberg, E. and Castagnone-Sereno, P. 2005. Variation in resistance to the root-knot nematode Meloidogyne incognita in tomato genotypes bearing the Mi gene. Plant Pathol. 54: 93-99. https://doi.org/10.1111/j.1365-3059.2005.01143.x
  21. Jaubert, S., Ledger, T. N., Laffaire, J. B., Piotte, C., Abad, P. and Rosso, M. N. 2002. Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol. Biochem. Parasitol. 121: 205-211. https://doi.org/10.1016/S0166-6851(02)00034-8
  22. Jones, M. G. and Northcote, D. H. 1972. Nematode-induced syncytium-a multinucleate transfer cell. J. Cell Sci. 10: 789-809.
  23. Jung, C., Cai, D. and Kleine, M. 1998. Engineering nematode resistance in crop species. Trends Plant Sci. 3: 266-271. https://doi.org/10.1016/S1360-1385(98)01247-3
  24. Kaplan, D. T. and Keen, N. T. 1980. Mechanisms conferring plant incompatibility to nematodes. Revue Nematol. 3: 123-134.
  25. Kawaji, H. and Hayashizaki, Y. 2008. Exploration of small RNAs. PLoS. Genet. 4: e22. https://doi.org/10.1371/journal.pgen.0040022
  26. Li, X. Q., Wei, J. Z., Tan, A. and Aroian, R. V. 2007. Resistance to root-knot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol. J. 5: 455-464. https://doi.org/10.1111/j.1467-7652.2007.00257.x
  27. Marban-Mendoza, N., Jeyaprakash, A., Jansson, H. B., Damon, R. A. and Zuckerman, B. M. 1987. Control of root-knot nematodes on tomato by lectins. J. Nematol. 19: 331-335.
  28. Marroquin, L. D., Elyassnia, D., Griffitts, J. S., Feitelson, J. S. and Aroian, R. V. 2000. Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155: 1693-1699.
  29. McCarter, J. P. 2009. "Molecular Approaches Toward Resistance to Plant-Parasitic Nematodes", Chapter in Cell Biology of Plant Nematode Parasitism, Berg, R. H. and C. G Taylor eds., Series: Plant Cell Monographs, Vol. 15, Springer-Verlag Press, Berlin.
  30. 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. and Waterston, R. H. 2003. Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol. 4: R26. https://doi.org/10.1186/gb-2003-4-4-r26
  31. Messeguer, R., Ganal, M., Devicente, M. C., Young, N. D., Bolkan, H. and Tanksley, S. D. 1991. High-resolution RFLP map around the root-knot nematode resistance gene (Mi) in tomato. Theor. Appl. Genet. 82: 529-536. https://doi.org/10.1007/BF00226787
  32. Milligan, S. B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Williamson, V. M. 1998. The root-knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307-1319. https://doi.org/10.1105/tpc.10.8.1307
  33. Nagaraj, S. H., Gasser, R. B. and Ranganathan, S. 2008. Needles in the EST Haystack: Large-Scale Identification and Analysis of Excretory-Secretory (ES) Proteins in Parasitic Nematodes Using Expressed Sequence Tags (ESTs). PLoS. Negl. Trop. Dis. 2: e301. https://doi.org/10.1371/journal.pntd.0000301
  34. Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J.,Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. 2008. Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proc. Natl. Acad. Sci. U.S.A. 105: 14802-14807. https://doi.org/10.1073/pnas.0805946105
  35. Pak, H. K., Sim, J. S., Rhee, Y., Ko, H. R., Ha, S. H., Yoon, M. S., Kang, C. H., Lee, S., Kim, Y. H. and Hahn, B. S. 2009. Hairy root induction in Oriental melon (Cucumis melo) by Agrobacterium rhizogenes and reproduction of the root-knot nematode (Meloidogyne incognita) Plant Cell Tiss. Organ Cult. 98: 219-228. https://doi.org/10.1007/s11240-009-9556-4
  36. Rasmann, S., Kollner, T, Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J. and Turlings, T. 2005. Recruitment of entomopathogenic nematodes by insectdamaged maize roots. Nature 434: 732-737. https://doi.org/10.1038/nature03451
  37. Rich, J. R., Keen, N. T. and Thomason, I. J. 1977. Association of coumestans with the hypersensitivity of lima bean roots to Pratylenchus scribneri. Physio. Plant Path. 10: 105-116. https://doi.org/10.1016/0048-4059(77)90014-5
  38. Ripoll, C., Favery, B., Lecomte, P., Van Damme, E., Peumans, W., Abad, P. and Jouanin, L. 2003. Evaluation of the ability of lectin from snowdrop (Galanthus nivalis) to protect plants against root-knot nematodes. Plant Sci. 164: 517-523. https://doi.org/10.1016/S0168-9452(02)00448-X
  39. Rossi, M., Goggin, F.L., Milligan, S. B., Kaloshian, I., Ullman, D. E. and Williamson, V. M. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad Sci. USA 95: 9750-9754. https://doi.org/10.1073/pnas.95.17.9750
  40. Rosso, M. N., Dubrana, M. P., Cimbolini, N., Jaubert, S. and Abad, P. 2005. Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Mol. Plant Microbe. Interact. 18: 615-620. https://doi.org/10.1094/MPMI-18-0615
  41. Rosso, M. N., Jones, J. T. and Abad, P. 2009. RNAi and Functional Genomics in Plant Parasitic Nematodes. Annu. Rev. Phytopathol. 47: 207-232. https://doi.org/10.1146/annurev.phyto.112408.132605
  42. Sasser, J. N. 1980. Root-knot nematodes: A global menace to crop production. Plant Dis. 64: 36-41. https://doi.org/10.1094/PD-64-36
  43. Sharon, E., Spiegel, Y, Salomon, R. and Curtis, R. H. C. 2002. Characterization of Meloidogyne javanica surface coat with antibodies and their effect on nematode behaviour. Parasitology 125: 177-185.
  44. Shingles, J., Lilley, C. J., Atkinson, H. J. and Urwin, P. E. 2007. Meloidogyne incognita: molecular and biochemical characterisation of a cathepsin L cysteine proteinase and the effect on parasitism following RNAi. Exp. Parasitol. 115: 114-120. https://doi.org/10.1016/j.exppara.2006.07.008
  45. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. and Fire, A. 2001. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476. https://doi.org/10.1016/S0092-8674(01)00576-1
  46. Sobczak, M., Avrova, A., Jupowicz, J., Phillips, M. S., Emst, K. and Kumar, A. 2005. Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Mol. Plant Microbe. Interact. 18: 158-168. https://doi.org/10.1094/MPMI-18-0158
  47. Soriano, I. R., Asenstorfer, R. E., Schmidt, O. and Riley, I. T. 2004a. Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes. Phytopathol. 94: 1207-1214. https://doi.org/10.1094/PHYTO.2004.94.11.1207
  48. Soriano. I. R., Riley, I.T., Potter, M. J. and Bowers, W.S. 2004b. Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J. Chem. Ecol. 30: 1885-1899. https://doi.org/10.1023/B:JOEC.0000045584.56515.11
  49. Timmons, L. and Fire, A. 1998. Specific interference by ingested dsRNA. Nature 395: 854. https://doi.org/10.1038/27579
  50. Urwin, P. E., Green, J. and Atkinson, H. J. 2003. Expression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistance. Mol. Breeding 12: 263-269. https://doi.org/10.1023/A:1026352620308
  51. 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. https://doi.org/10.1007/s004250050281
  52. Urwin, P. E., Troth, K. M., Zubko, E. I. and Atkinson, H. J. 2001. Effective transgenic resistance to Globodera pallida in potato field trials. Mol. Breeding 8: 95-101. https://doi.org/10.1023/A:1011942003994
  53. Urwin, P. E., Lilley, C. J., McPherson, M. J. and Atkinson, H. J. 1997. Resistance to both cyst and root-knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J. 12: 455-461. https://doi.org/10.1046/j.1365-313X.1997.12020455.x
  54. Vain, P., Worland, B., Clarke, M. C, Richard, G., Beavis, M., Liu, H., Kohli, A., Leech, M., Snape, J. W., Atkinson, H. and Christou, P. 1998. Expression of an engineered cysteine proteinase inhibitor (OC-I$\Delta$D86) for nematode resistance in transgenic rice plants. Theor. Appl. Genet. 96: 266-271. https://doi.org/10.1007/s001220050735
  55. Valette, C., Andary, C., Geiger, J. P., Sarah, J. L. and Nicole, M. 1998. Histochemical and cytochemical investigations of phenols in roots of banana infected by the burrowing nematode Radopholus similis. Phytopathol. 88: 1141-1148. https://doi.org/10.1094/PHYTO.1998.88.11.1141
  56. Veech, J. A. and McClure, M. A. 1977. Terpenoid aldehydes in cotton roots susceptible and resistant to the root-knot nematode, Meloidogyne incognita. J. Nematol. 9: 225-229.
  57. Vishnudasan, D., Tripathi, M. N., Rao, U. and Khurana, P. 2005. Assessment of nematode resistance in wheat transgenic plants expressing potato proteinase inhibitor (PIN2) gene. Transgenic Res. 14: 665-675. https://doi.org/10.1007/s11248-005-5696-4
  58. Vos, P., Simons, G, Jesse, T., Wijbrandi, J., Heinen, L., Hogers, R., Frijters, A., Groenendijk, J., Diergaarde, P., Reijans, M., Fierens-Onstenk, J., de Both, M., Peleman, J., Liharska, T., Hontelez, J. and Zabeau, M. 1998. The tomato Mi-I gene confers resistance to both root-knot nematodes and potato aphids. Nat. Biotechnol. 16: 1365-1369. https://doi.org/10.1038/4350
  59. Wei, J. -Z., Hale, K., Carta, L., Platzer, E., Wong, C., Fang, S.-C. and Aroian, R. V. 2003. Bacillus thuringiensis crystal proteins that target nematodes. Proc. Natl. Acad. Sci. USA 100: 2760-2765. https://doi.org/10.1073/pnas.0538072100
  60. Wider, T. L. and Abawi, G S. 2000. Mechanism of suppression of Meloidogyne hapla and its damage by a green manure of Sudan grass. Plant Dis. 84: 562-568. https://doi.org/10.1094/PDIS.2000.84.5.562
  61. Wiggers, R. J., Starr, J. L. and Price, H. J. 1990. DNA content and variation in chromosome number in plant cells affected by Meloidogyne incognita and M arenaria. Phytopathology, 80: 1391-1395. https://doi.org/10.1094/Phyto-80-1391
  62. Wylie, T., Martin, J., Abubucker, S., Yin, Y., Messina, D., Wang, Z., McCarter, J. P. and Mitreva, M. 2008. NemaPath: online exploration of KEGG-based metabolic pathways for nematodes. BMC Genomics. 9: 525. https://doi.org/10.1186/1471-2164-9-525
  63. Yadav, B. C., Veluthambi, K. and Subramaniam, K. 2006. Host-generated double stranded RNA induces RNAi in plantparasitic nematodes and protects the host from infection. Mol. Biochem. Parasitol. 148: 219-222. https://doi.org/10.1016/j.molbiopara.2006.03.013
  64. Yoon, Y., Kim, E., Hwang, Y. and Choi, C. 2004. Avermectin: biochemical and molecular basis of its biosynthesis and regulation. Appl. Microbiol. Biotechnol. 63: 626-634. https://doi.org/10.1007/s00253-003-1491-4

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