Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Expression of BrD1, a Plant Defensin from Brassica rapa, Confers Resistance against Brown Planthopper (Nilaparvata lugens) in Transgenic Rices

  • Choi, Man-Soo (National Institute of Crop Science, Rural Development Administration) ;
  • Kim, Yul-Ho (National Institute of Crop Science, Rural Development Administration) ;
  • Park, Hyang-Mi (National Institute of Crop Science, Rural Development Administration) ;
  • Seo, Bo-Yoon (National Institute of Crop Science, Rural Development Administration) ;
  • Jung, Jin-Kyo (National Institute of Crop Science, Rural Development Administration) ;
  • Kim, Sun-Tae (Department of Plant Bioscience, Pusan National University) ;
  • Kim, Min-Chul (Division of Applied Life Science (Brain Korea 21 Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Shin, Dong-Bum (National Institute of Crop Science, Rural Development Administration) ;
  • Yun, Hong-Tai (National Institute of Crop Science, Rural Development Administration) ;
  • Choi, Im-Soo (National Institute of Crop Science, Rural Development Administration) ;
  • Kim, Chung-Kon (National Institute of Crop Science, Rural Development Administration) ;
  • Lee, Jang-Yong (National Academy of Agricultural Science, Rural Development Administration)
  • Received : 2009.06.24
  • Accepted : 2009.07.15
  • Published : 2009.08.31
⟨ Previous Next ⟩

Abstract

Plant defensins are small (5-10 kDa) basic peptides thought to be an important component of the defense pathway against fungal and/or bacterial pathogens. To understand the role of plant defensins in protecting plants against the brown planthopper, a type of insect herbivore, we isolated the Brassica rapa Defensin 1 (BrD1) gene and introduced it into rice (Oryza sativa L.) to produce stable transgenic plants. The BrD1 protein is homologous to other plant defensins and contains both an N-terminal endoplasmic reticulum signal sequence and a defensin domain, which are highly conserved in all plant defensins. Based on a phylogenetic analysis of the defensin domain of various plant defensins, we established that BrD1 belongs to a distinct subgroup of plant defensins. Relative to the wild type, transgenic rices expressing BrD1 exhibit strong resistance to brown planthopper nymphs and female adults. These results suggest that BrD1 exhibits insecticidal activity, and might be useful for developing cereal crop plants resistant to sap-sucking insects, such as the brown planthopper.

Keywords

Acknowledgement

Supported by : National Institute of Crop Science, Rural Development Administration

References

  1. Alfonso-Rubi, J., Ortego, F., Castanera, P., Carbonero, P., and Diaz, I. (2003). Transgenic expression of trypsin inhibitor CMe from barley in indica and japonica rice, confers resistance to the rice weevil Sitophilus oryzae. Transgenic Res. 12, 23-31 https://doi.org/10.1023/A:1022176207180
  2. Bandyopadhyay, S., Roy, A., and Das, S. (2001). Binding of garlic (Allium sativum) leaf lectin to the gut receptors of homopteran pests is correlated to its insecticidal activity. Plant Sci. 161, 1025-1033 https://doi.org/10.1016/S0168-9452(01)00507-6
  3. Cha, Y.S., Ji, H., Yun, D.W., Ahn, B.O., Lee, M.C., Suh, S.C., Lee, C.S., Ahn, E.K., Jeon, Y.H., Jin, I.D., et al. (2008). Fine mapping of the rice Bph1 gene, which confers resistance to the brown planthopper (Nilaparvata lugens Stal), and development of STS markers for marker-assisted selection. Mol. Cells 26, 146-151
  4. Clarke, J.D. (2009). Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb. Protoc: doi:10.1101/pdb.prot5177
  5. Dutta, I., Saha, P., Majumder, P., Sarkar, A., Chakraborti, D., Banerjee, S., and Das, S. (2005a). The efficacy of a novel insecticidal protein, Allium sativum leaf lectin (ASAL), against homopteran insects monitored in transgenic tobacco. Plant Biotechnol. J. 3, 601-611 https://doi.org/10.1111/j.1467-7652.2005.00151.x
  6. Dutta, I., Majumder, P., Saha, P., Ray, K., and Das, S. (2005b). Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Sci. 169, 996-1007 https://doi.org/10.1016/j.plantsci.2005.05.016
  7. Epple, P., Apel, K., and Bohlmann, H. (1997). ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana. FEBS Lett. 400, 168-172 https://doi.org/10.1016/S0014-5793(96)01378-6
  8. Falk, B., and Tsai, T.H. (1998). Biology and molecular biology of viruses in the genus tenuiviruses. Annu. Rev. Phytopathol. 36, c https://doi.org/10.1146/annurev.phyto.36.1.139
  9. Foissac, X., Thi Loc, N., Christou, P., Gatehouse, A.M., and Gatehouse, J.A. (2000). Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglu-tinin; GNA). J. Insect Physiol. 46, 573-583 https://doi.org/10.1016/S0022-1910(99)00143-2
  10. Gallagher, K.D., Kenmore, P.E., and Sogawa, K. (1994). Judicial use of insecticides deter planthopper outbreaks and extend the life of resistant varieties in Southeast Asia rice. In: R.F. Denno and J.T. Perfect, eds., Planthoppers: Their ecology and management, (Chapman & Hall, New York) pp. 599-614
  11. Jang, I.C., Choi, W.B., Lee, K.H., Song, S.I., Nahm, B.H., and Kim, J.K. (2002). High-level and ubiquitous expression of the rice cytochrome c gene (OsCc1) and its promoter activity in transgenic plants provides a useful promoter for transgenesis of monocots. Plant Physiol. 129, 1473-1481 https://doi.org/10.1104/pp.002261
  12. Kim, S.M., and Shon, J.K. (2005). Identification of a rice gene (Bph 1) conferring resistance to brown planthopper (Nilaparvata Iugens Stal) using STS markers. Mol. Cells 20, 30-34
  13. Lay, F.T., and Anderson, M.A. (2005). Defensins--components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85-101 https://doi.org/10.2174/1389203053027575
  14. 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 (Nilapar-vata lugens Stal) in transgenic rice. Mol. Breed 5, 1-9 https://doi.org/10.1023/A:1009660712382
  15. Loc, N.T., Tinjuangjun, P., Gatehouse, A.M.R., Christou, P., and Gatehouse, J.A. (2002). Linear transgene constructs lacking vector backbone sequences generate transgenic rices which accumulate higher levels of proteins conferring insects resistance. Mol. Breed 9, 231-244 https://doi.org/10.1023/A:1020333210563
  16. Majumder, P., Banerjee, S., and Das, S. (2004). Identification of receptors responsible for binding of the mannose specific lectin to the gut epithelial membrane of the target insects. Glycoconj. J. 20, 525-530 https://doi.org/10.1023/B:GLYC.0000043288.72051.7c
  17. Mendez, E., Moreno, A., Colilla, F., Pelaez, F., Limas, G.G., Mendez, R., Soriano, F., Salinas, M., and de Haro, C. (1990). Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, gamma-hordothionin, from barley endosperm. Eur. J. Biochem. 194, 533-539 https://doi.org/10.1111/j.1432-1033.1990.tb15649.x
  18. Park, Y.S., Jeon, M.H., Lee, S.H., Moon, J.S., Cha, J.S., Kim, H.Y., and Cho, T.J. (2005). Activation of defense response in Chinese cabbage by a nonhost pathogene, Pseudomonas syringe pv. tomato. J. Biochem. Mol. Biol. 38, 748-754 https://doi.org/10.5483/BMBRep.2005.38.6.748
  19. Powell, K.S. (2001). Antifeedant effects of plant lectins towards nymphal stages of the planthoppers Tarophagous proserpina and Nilaparvata lugens. Entomol. Exp. Appl. 99, 71-77 https://doi.org/10.1023/A:1018948228640
  20. Ramesh, S., Nagadhara, D., Reddy, V.D., and Rao, K.V. (2004). Production of transgenic indica rice resistant to yellow stem borer and sap-sucking insects, using super-binary vectors of Agrobacterium tumefaciens. Plant Sci. 166, 1077-1085 https://doi.org/10.1016/j.plantsci.2003.12.028
  21. Roy-Barman, S., Sautter, C., and Chattoo, B.B. (2006). Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses. Transgenic Res. 15, 435-446 https://doi.org/10.1007/s11248-006-0016-1
  22. Saitoh, H., Kiba, A., Nishihara, M., Yamamura, S., Suzuki, K., and Terauchi, R. (2001). Production of antimicrobial defensin in Nicotiana benthamiana with a potato virus X vector. Mol. Plant-Microbe Interact. 14, 111-115 https://doi.org/10.1094/MPMI.2001.14.2.111
  23. Schuler, T.H., Poppy, G.M., Kerry, B.R., and Denholm, I. (1999). Insect-resistant transgenic plants. Trends Biotechnol. 16, 168-175 https://doi.org/10.1016/S0167-7799(97)01171-2
  24. Sohn, S.I., Kim, Y.H., Cho, J.H., Kim, J.G., and Lee, J.Y. (2006). An efficient selection scheme for Agrobacterium-mediated cotransformation of rice using two selectable marker genes hpt and var. Korean J. Breed 38, 173-179
  25. Tan, G.X., Weng, Q.M., Ren, X., Huang, Z., Zhu, L.L., and He, G.C. (2004). Two whitebacked planthopper resistance genes in rice share the same loci with those for brown planthopper resistance. Heredity 92, 211-217 https://doi.org/10.1038/sj.hdy.6800398
  26. Terras, F.R.G., Eggermont, K., Kovaleva, V., Raikhel, N.V., Osborn, R.W., Kester, A., Rees, S.B., Torrekens, S., Van Leuven, F., Vanderleyden, J., et al. (1995). Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7, 573-588 https://doi.org/10.1105/tpc.7.5.573
  27. Thevissen, K., Francois, I.E., Takemoto, J.Y., Ferket, K.K., Meert, E.M., and Cammue, B.P. (2003). DmAMP1, an antifungal plant defensin from dahlia (Dahlia merckii), interacts with sphingolipids from Saccharomyces cerevisiae. FEMS Microbiol. Lett. 226, 169-173 https://doi.org/10.1016/S0378-1097(03)00590-1
  28. Thevissen, K., Warnecke, D.C., Francois, I.E., Leipelt, M., Heinz, E., Ott, C., Zahringer, U., Thomma, B.P., Ferket, K.K., and Cammue, B.P. (2004). Defensins from insects and plants interact with fungal glucosylceramides. J. Biol. Chem.279, 3900-3905 https://doi.org/10.1074/jbc.M311165200
  29. Thomma, B.P., Cammue, B.P., and Thevissen, K. (2002). Plant defensins. Planta 16, 193-202 https://doi.org/10.1007/s00425-002-0902-6
  30. Wisniewski, M.E., Bassett, C.L., Artlip, T.S., Robert, P.W., Janisiewicz, W.J., Norelli, J.I., Goldway, M., and Droby, S. (2003). Characterization of a defensin in bark and fruit tissues of peach and antimicrobial activity of a recombinant defensin in the yeast, Pichia pastoris. Physiol. Plant 119, 563-572 https://doi.org/10.1046/j.1399-3054.2003.00204.x

Cited by

  1. Four plant defensins from an indigenous South African Brassicaceae species display divergent activities against two test pathogens despite high sequence similarity in the encoding genes vol.4, pp.None, 2011, https://doi.org/10.1186/1756-0500-4-459
  2. The expression pattern of the Picea glauca Defensin 1 promoter is maintained in Arabidopsis thaliana, indicating the conservation of signalling pathways between angiosperms and gymnosperms vol.63, pp.2, 2009, https://doi.org/10.1093/jxb/err303
  3. Constitutive expression of transgenes encoding derivatives of the synthetic antimicrobial peptide BP100: impact on rice host plant fitness vol.12, pp.None, 2009, https://doi.org/10.1186/1471-2229-12-159
  4. Overexpression of a Broccoli Defensin Gene BoDFN Enhances Downy Mildew Resistance vol.11, pp.7, 2009, https://doi.org/10.1016/s2095-3119(12)60107-5
  5. Defensin (TvD1) from Tephrosia villosa exhibited strong anti-insect and anti-fungal activities in transgenic tobacco plants vol.86, pp.2, 2009, https://doi.org/10.1007/s10340-012-0467-5
  6. Constitutive expression of a fusion gene comprising Trigonella foenum-graecum defensin (Tfgd2) and Raphanus sativus antifungal protein (RsAFP2) confers enhanced disease and insect resistance in transg vol.115, pp.3, 2013, https://doi.org/10.1007/s11240-013-0363-6
  7. Rice Bran Expressing a Shrimp Antimicrobial Peptide Confers Delayed Spoilage of Fish Feed and Resistance of Tilapia to Aeromonas hydrophila vol.45, pp.3, 2009, https://doi.org/10.1111/jwas.12121
  8. Insect antimicrobial peptides and their applications vol.98, pp.13, 2009, https://doi.org/10.1007/s00253-014-5792-6
  9. Surveying the potential of secreted antimicrobial peptides to enhance plant disease resistance vol.6, pp.None, 2009, https://doi.org/10.3389/fpls.2015.00900
  10. Omics-Based Comparative Transcriptional Profiling of Two Contrasting Rice Genotypes during Early Infestation by Small Brown Planthopper vol.16, pp.12, 2009, https://doi.org/10.3390/ijms161226128
  11. Antimicrobial Activities of Novel Peptides Derived from Defensin Genes of Brassica hybrid cv Pule vol.22, pp.1, 2009, https://doi.org/10.1007/s10989-015-9488-2
  12. The recombinant pea defensin Drr230a is active against impacting soybean and cotton pathogenic fungi from the genera Fusarium , Colletotrichum and Phakopsora vol.6, pp.1, 2016, https://doi.org/10.1007/s13205-015-0320-7
  13. Functional characterization of Rorippa indica defensin and its efficacy against Lipaphis erysimi vol.5, pp.1, 2009, https://doi.org/10.1186/s40064-016-2144-2
  14. Overexpression of biologically safe Rorippa indica defensin enhances aphid tolerance in Brassica juncea vol.246, pp.5, 2009, https://doi.org/10.1007/s00425-017-2750-4
  15. Antimicrobial activity of LFchimera synthetic peptide against plant pathogenic bacteria vol.50, pp.19, 2017, https://doi.org/10.1080/03235408.2017.1411173
  16. The toxic effect of Vu-Defr, a defensin from Vigna unguiculata seeds, on Leishmania amazonensis is associated with reactive oxygen species production, mitochondrial dysfunction, and plasma membrane pe vol.64, pp.7, 2009, https://doi.org/10.1139/cjm-2018-0095
  17. Identification and characterization of defensin genes conferring Phytophthora infestans resistance in tomato vol.103, pp.None, 2009, https://doi.org/10.1016/j.pmpp.2018.04.003
  18. Plant defensins: types, mechanism of action and prospects of genetic engineering for enhanced disease resistance in plants vol.9, pp.5, 2009, https://doi.org/10.1007/s13205-019-1725-5
  19. Evaluation of Antibacterial Properties of Chimeric Bovine Lactoferrin Peptide for Inhibition of Food and Plant Pathogens vol.7, pp.2, 2009, https://doi.org/10.5812/iji.104594
  20. Recent advances in genomics‐assisted breeding of brown planthopper (Nilaparvata lugens) resistance in rice (Oryza sativa) vol.139, pp.6, 2020, https://doi.org/10.1111/pbr.12851
  21. Antimicrobial Peptides from Plants: A cDNA-Library Based Isolation, Purification, Characterization Approach and Elucidating Their Modes of Action vol.22, pp.16, 2021, https://doi.org/10.3390/ijms22168712