Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses

Plant Biotechnology Journal

Volumn 12, Issue 4, 2014, Pages 503-515

  Chen, Peng Jen ^a   Senthilkumar, Rajendran ^a   Jane, Wann Neng ^b   He, Yong ^c   Tian, Zhihong ^c   Yeh, Kai Wun ^a,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^c YANGTZE UNIVERSITY   (China)

Author keywords

CeCPI; chitinase; Gene stacking; Plastid transformation; sporamin; Stress tolerance

Indexed keywords

ALTERNARIA ALTERNATA; COLOCASIA ESCULENTA; HEXAPODA; IPOMOEA BATATAS; NICOTIANA BENTHAMIANA; PAECILOMYCES JAVANICUS; PECTOBACTERIUM CAROTOVORUM SUBSP. CAROTOVORUM; SPODOPTERA EXIGUA; SPODOPTERA LITURA;

CHITINASE; MEMBRANE LIPID; PARAQUAT; PROTEINASE INHIBITOR; SODIUM CHLORIDE;

ALTERNARIA; ANIMAL; BIOASSAY; CROSS BREEDING; DISEASE RESISTANCE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC TRANSFORMATION; GENETICS; HERBIVORY; IMMUNOLOGY; INSECT; METABOLISM; MICROBIOLOGY; OXIDATIVE STRESS; PARASITOLOGY; PECTOBACTERIUM CAROTOVORUM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT LEAF; PLASTID; TOBACCO; TRANSGENIC PLANT; ULTRASTRUCTURE;

ALTERNARIA; ANIMALS; BIOLOGICAL ASSAY; CHITINASE; CROSSES, GENETIC; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC VECTORS; HERBIVORY; INSECTS; MEMBRANE LIPIDS; OXIDATIVE STRESS; PARAQUAT; PECTOBACTERIUM CAROTOVORUM; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROTEASE INHIBITORS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TOBACCO; TRANSFORMATION, GENETIC;

EID: 84899116969     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12157     Document Type: Article

References (64)

1. Ahmed, N.U., Park, J.I., Jung, H.J., Kang, K.K., Hur, Y., Lim, Y.P. and Nou, I.S. (2012) Molecular characterization of stress resistance-related chitinase genes of Brassica rapa. Plant Physiol. Biochem. 58, 106-115.
2. Amian, A.A., Papenbrock, J., Jacobsen, H.J. and Hassan, F. (2011) Enhancing transgenic pea (Pisum sativum L.) resistance against fungal diseases through stacking of two antifungal genes (chitinase and glucanase). GM crops, 2, 104-109.
3. Apel, W. and Bock, R. (2009) Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 151, 59-66.
4. Beyene, G., Foyer, C.H. and Kunert, K.J. (2006) Two new cysteine proteinases with specific expression patterns in mature and senescent tobacco (Nicotiana tabacum L.) leaves. J. Exp. Bot. 57, 1431-1443.
5. Bock, R. (2007) Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr. Opin. Biotechnol. 18, 100-106.
6. Bock, R. and Warzecha, H. (2010) Solar-powered factories for new vaccines and antibiotics. Trends Biotechnol. 28, 246-252.
7. Botelho-Junior, S., Siqueira-Junior, C.L., Jardim, B.C., Machado, O.L., Neves-Ferreira, A.G., Perales, J. and Jacinto, T. (2008) Trypsin inhibitors in passion fruit (Passiflora f. edulis flavicarpa) leaves: accumulation in response to methyl jasmonate, mechanical wounding, and herbivory. J. Agric. Food Chem. 56, 9404-9409.
8. Boyhan, D. and Daniell, H. (2011) Low-cost production of proinsulin in tobacco and lettuce chloroplasts for injectable or oral delivery of functional insulin and C-peptide. Plant Biotechnol. J. 9, 585-598.
9. Cai, D.G., Thurau, T., Tian, Y.Y., Lange, T., Yeh, K.W. and Jung, C. (2003) Sporamin-mediated resistance to beet cyst nematodes (Heterodera schachtii Schm.) is dependent on trypsin inhibitory activity in sugar beet (Beta vulgaris L.) hairy roots. Plant Mol. Biol. 51, 839-849.
10. Chakrabarti, S.K., Lutz, K.A., Lertwiriyawong, B., Svab, Z. and Maliga, P. (2006) Expression of the cry9Aa2 B.t. gene in tobacco chloroplasts confers resistance to potato tuber moth. Transgenic Res. 15, 481-488.
11. Chan, Y.L., Cai, D., Taylor, P.W.J., Chan, M.T. and Yeh, K.W. (2010a) Adverse effect of the chitinolytic enzyme PjCHI-1 in transgenic tomato on egg mass production and embryonic development of Meloidogyne incognita. Plant. Pathol. 59, 922-930.
12. Chan, Y.L., Yang, A.H., Chen, J.T., Yeh, K.W. and Chan, M.T. (2010b) Heterologous expression of taro cystatin protects transgenic tomato against Meloidogyne incognita infection by means of interfering sex determination and suppressing gall formation. Plant Cell Rep. 29, 231-238.
13. Chang, S., Puryear, J. and Cairney, J. (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11, 113-116.
14. Chang, I.F., Chen, P.J., Shen, C.H., Hsieh, T.J., Hsu, Y.W., Huang, B.L., Kuo, C.I., Chen, Y.T., Chu, H.A., Yeh, K.W. and Huang, L.C. (2010) Proteomic profiling of proteins associated with the rejuvenation of Sequoia sempervirens (D. Don) Endl. Proteome sci. 8, 64.
15. Chen, H.J., Wang, S.J., Chen, C.C. and Yeh, K.W. (2006) New gene construction strategy in T-DNA vector to enhance expression level of sweet potato sporamin and insect resistance in transgenic Brassica oleracea. Plant Sci. 171, 367-374.
16. Chen, C.C., Kumar, H.G., Kumar, S., Tzean, S.S. and Yeh, K.W. (2007) Molecular cloning, characterization, and expression of a chitinase from the entomopathogenic fungus Paecilomyces javanicus. Curr. Microbiol. 55, 8-13.
17. Christou, P., Capell, T., Kohli, A., Gatehouse, J.A. and Gatehouse, A.M. (2006) Recent developments and future prospects in insect pest control in transgenic crops. Trends Plant Sci. 11, 302-308.
18. Clarke, J.D. (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb. Protoc. 2009, pdb.prot5177.
19. Craig, W., Lenzi, P., Scotti, N., De Palma, M., Saggese, P., Carbone, V., McGrath Curran, N., Magee, A.M., Medgyesy, P., Kavanagh, T.A., Dix, P.J., Grillo, S. and Cardi, T. (2008) Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic Res. 17, 769-782.
20. Dana, M.D., Pintor-Toro, J.A. and Cubero, B. (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol. 142, 722-730.
21. Davarpanah, S.J., Jung, S.H., Kim, Y.J., Park, Y.I., Min, S.R., Liu, J.R. and Jeong, W.J. (2009) Stable plastid transformation in Nicotiana benthamiana. J. Plant Biol. 52, 244-250.
22. Davoodi-Semiromi, A., Schreiber, M., Nalapalli, S., Verma, D., Singh, N.D., Banks, R.K., Chakrabarti, D. and Daniell, H. (2010) Chloroplast-derived vaccine antigens confer dual immunity against cholera and malaria by oral or injectable delivery. Plant Biotechnol. J. 8, 223-242.
23. DeGray, G., Rajasekaran, K., Smith, F., Sanford, J. and Daniell, H. (2001) Expression of an antimicrobial peptide via the chloroplast genome to control phytopathogenic bacteria and fungi. Plant Physiol. 127, 852-862.
24. Dudas, B., Jenes, B., Kiss, G.B. and Maliga, P. (2012) Spectinomycin resistance mutations in the rrn16 gene are new plastid markers in Medicago sativa. Theor. Appl. Genet. 125, 1517-1523.
25. Dufourmantel, N., Pelissier, B., Garcon, F., Peltier, G., Ferullo, J.M. and Tissot, G. (2004) Generation of fertile transplastomic soybean. Plant Mol. Biol. 55, 479-489.
26. Hanson, M.R., Gray, B.N. and Ahner, B.A. (2013) Chloroplast transformation for engineering of photosynthesis. J. Exp. Bot. 64, 731-742.
27. Jin, S., Zhang, X. and Daniell, H. (2012) Pinellia ternata agglutinin expression in chloroplasts confers broad spectrum resistance against aphid, whitefly, Lepidopteran insects, bacterial and viral pathogens. Plant Biotechnol. J. 10, 313-327.
28. Kanagaraj, A.P., Verma, D. and Daniell, H. (2011) Expression of dengue-3 premembrane and envelope polyprotein in lettuce chloroplasts. Plant Mol. Biol. 76, 323-333.
29. Kanamoto, H., Yamashita, A., Asao, H., Okumura, S., Takase, H., Hattori, M., Yokota, A. and Tomizawa, K. (2006) Efficient and stable transformation of Lactuca sativa L. cv. Cisco (lettuce) plastids. Transgenic Res. 15, 205-217.
30. Kumar, S., Dhingra, A. and Daniell, H. (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiol. 136, 2843-2854.
31. Kumar, S., Hahn, F.M., Baidoo, E., Kahlon, T.S., Wood, D.F., McMahan, C.M., Cornish, K., Keasling, J.D., Daniell, H. and Whalen, M.C. (2012) Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metab. Eng. 14, 19-28.
32. Kwon, K.-C., Nityanandam, R., New, J.S. and Daniell, H. (2013a) Oral delivery of bioencapsulated exendin-4 expressed in chloroplasts lowers blood glucose level in mice and stimulates insulin secretion in beta-TC6 cells. Plant Biotechnol. J. 11, 77-86.
33. Kwon, K.-C., Verma, D., Singh, N.D., Herzog, R. and Daniell, H. (2013b) Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv. Drug Deliv. Rev. 65, 782-799.
34. Lakshmi, P.S., Verma, D., Yang, X., Lloyd, B. and Daniell, H. (2013) Low cost tuberculosis vaccine antigens in capsules: expression in chloroplasts, bio-encapsulation, stability and functional evaluation in vitro. PLoS ONE, 8, e54708.
35. Lee, S.B., Li, B., Jin, S. and Daniell, H. (2011) Expression and characterization of antimicrobial peptides Retrocyclin-101 and Protegrin-1 in chloroplasts to control viral and bacterial infections. Plant Biotechnol. J. 9, 100-115.
36. 2K-type dehydrin VrDhn1 from Vigna radiata. Plant Cell Physiol. 53, 930-942.
37. Liu, C.W., Lin, C.C., Chen, J.J. and Tseng, M.J. (2007) Stable chloroplast transformation in cabbage (Brassica oleracea L. var. capitata L.) by particle bombardment. Plant Cell Rep. 26, 1733-1744.
38. Lu, Y., Rijzaani, H., Karcher, D., Ruf, S. and Bock, R. (2013) Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc. Natl Acad. Sci. USA, 110, E623-E632.
39. Maliga, P. and Bock, R. (2011) Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol. 155, 1501-1510.
40. Martinez, M., Abraham, Z., Gambardella, M., Echaide, M., Carbonero, P. and Diaz, I. (2005) The strawberry gene Cyf1 encodes a phytocystatin with antifungal properties. J. Exp. Bot. 56, 1821-1829.
41. Maximova, S.N., Marelli, J.P., Young, A., Pishak, S., Verica, J.A. and Guiltinan, M.J. (2006) Overexpression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta, 224, 740-749.
42. Minocha, R., Martinez, G., Lyons, B. and Long, S. (2009) Development of a standardized methodology for quantifying total chlorophyll and carotenoids from foliage of hardwood and conifer tree species. Can. J. For. Res. 39, 849-861.
43. Munger, A., Coenen, K., Cantin, L., Goulet, C., Vaillancourt, L.P., Goulet, M.C., Tweddell, R., Sainsbury, F. and Michaud, D. (2012) Beneficial 'unintended effects' of a cereal cystatin in transgenic lines of potato, Solanum tuberosum. BMC Plant Biol. 12, 198.
44. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
45. Nakamura, T., Ishikawa, M., Nakatani, H. and Oda, A. (2008) Characterization of cold-responsive extracellular chitinase in bromegrass cell cultures and its relationship to antifreeze activity. Plant Physiol. 147, 391-401.
46. Outchkourov, N.S., de Kogel, W.J., Wiegers, G.L., Abrahamson, M. and Jongsma, M.A. (2004) Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Franklinielia occidentalis) in greenhouse trials. Plant Biotechnol. J. 2, 449-458.
47. Quesada-Vargas, T., Ruiz, O.N. and Daniell, H. (2005) Characterization of heterologous multigene operons in transgenic chloroplasts: transcription, processing, and translation. Plant Physiol. 138, 1746-1762.
48. Ruf, S., Hermann, M., Berger, I.J., Carrer, H. and Bock, R. (2001) Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nat. Biotechnol. 19, 870-875.
49. Ruhlman, T., Verma, D., Samson, N. and Daniell, H. (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol. 152, 2088-2104.
50. Senthilkumar, R., Cheng, C.P. and Yeh, K.W. (2010) Genetically pyramiding protease-inhibitor genes for dual broad-spectrum resistance against insect and phytopathogens in transgenic tobacco. Plant Biotechnol. J. 8, 65-75.
51. Sidorov, V.A., Kasten, D., Pang, S.Z., Hajdukiewicz, P.T., Staub, J.M. and Nehra, N.S. (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J. 19, 209-216.
52. Svab, Z., Hajdukiewicz, P. and Maliga, P. (1990) Stable transformation of plastids in higher plants. Proc. Natl Acad. Sci. USA, 87, 8526-8530.
53. Valkov, V.T., Gargano, D., Manna, C., Formisano, G., Dix, P.J., Gray, J.C., Scotti, N. and Cardi, T. (2011) High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5' and 3' regulatory sequences. Transgenic Res. 20, 137-151.
54. Verma, D. and Daniell, H. (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol. 145, 1129-1143.
55. Verma, D., Samson, N.P., Koya, V. and Daniell, H. (2008) A protocol for expression of foreign genes in chloroplasts. Nat. Protoc. 3, 739-758.
56. Wang, K.-M., Kumar, S., Cheng, Y.-S., Venkatagiri, S., Yang, A.-H. and Yeh, K.-W. (2008) Characterization of inhibitory mechanism and antifungal activity between group-1 and group-2 phytocystatins from taro (Colocasia esculenta). FEBS J. 275, 4980-4989.
57. Wurbs, D., Ruf, S. and Bock, R. (2007) Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. Plant J. 49, 276-288.
58. Yang, A.H. and Yeh, K.W. (2005) Molecular cloning, recombinant gene expression, and antifungal activity of cystatin from taro (Colocasia esculenta cv. Kaosiung no. 1). Planta, 221, 493-501.
59. Yeh, K.W., Chen, J.C., Lin, M.I., Chen, Y.M. and Lin, C.Y. (1997a) Functional activity of sporamin from sweet potato (Ipomoea batatas Lam.): a tuber storage protein with trypsin inhibitory activity. Plant Mol. Biol. 33, 565-570.
60. Yeh, K.W., Lin, M.I., Tuan, S.J., Chen, Y.M., Lin, C.Y. and Kao, S.S. (1997b) Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Rep. 16, 696-699.
61. Zhang, J., Tan, W., Yang, X.H. and Zhang, H.X. (2008a) Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Rep. 27, 1113-1124.
62. Zhang, X., Liu, S. and Takano, T. (2008b) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol. Biol. 68, 131-143.
63. Zhang, G., Chen, M., Li, L., Xu, Z., Chen, X., Guo, J. and Ma, Y. (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 60, 3781-3796.
64. Zhang, J., Ruf, S., Hasse, C., Childs, L., Scharff, L.B. and Bock, R. (2012) Identification of cis-elements conferring high levels of gene expression in non-green plastids. Plant J. 72, 115-128.