Overexpression of a weed (Solanum americanum) proteinase inhibitor in transgenic tobacco results in increased glandular trichome density and enhanced resistance to Helicoverpa armigera and Spodoptera litura

International Journal of Molecular Sciences

Volumn 10, Issue 4, 2009, Pages 1896-1910

  Luo, Ming ^a   Wang, Zhaoyu ^a   Li, Huapeng ^a   Xia, Kuai Fei ^a   Cai, Yinpeng ^a   Xu, Zeng Fu ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Insect resistance; Lepidopteran pests; Protease inhibitor; Solanum americanum; Trichome

Indexed keywords

PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR 2A; UNCLASSIFIED DRUG;

ARMYWORM; ARTICLE; HELICOVERPA ARMIGERA; INSECT RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SOLANUM; SOLANUM AMERICANUM; TOBACCO; TRANSGENIC PLANT; TRICHOME; WORM;

INSECT RESISTANCE; LEPIDOPTERAN PESTS; PROTEASE INHIBITOR; SOLANUM AMERICANUM; TRICHOME;

ANIMALS; LARVA; LEPIDOPTERA; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEASE INHIBITORS; SOLANUM; SPODOPTERA; TOBACCO; TRICHOMES;

AGROBACTERIUM TUMEFACIENS; HELICOVERPA ARMIGERA; HEXAPODA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; SOLANUM AMERICANUM; SOLANUM NIGRUM; SPODOPTERA LITURA;

EID: 67149092180     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms10041896     Document Type: Article

References (59)

1. Boulter, D. Insect pest control by copying nature using genetically engineered crops. Phytochemistry 1993, 34, 1453-1466.
2. Mosolov, V.V.; Valueva, T.A. Proteinase inhibitors in plant biotechnology: A review. Appl. Biochem. Microbiol. 2008, 44, 233-240.
3. Ryan, C.A. Proteinase inhibitor gene families: Strategies for transformation to improve plant defenses against herbivores. Bioessays 1989, 10, 20-24.
4. Brzin, J.; Kidric, M. Proteinases and their inhibitors in plants: role in normal growth and in response to various stress conditions. Biotechnol. Genet. Eng. Rev. 1995, 13, 421-467.
5. Hilder, V.A.; Gatehouse, A.M.R.; Sheerman, S.E.; Barker, R.F.; Boulter, D. A novel mechanism of insect resistance engineered into tobacco. Nature 1987, 330, 160-163.
6. Johnson, R.; Narvaez, J.; An, G.; Ryan, C. Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc. Natl. Acad. Sci. USA 1989, 86, 9871-9875.
7. Yeh, K.W.; Lin, M.I.; Tuan, S.J.; Chen, Y.M.; Lin, C.J.; Kao, S.S. Sweet potato (Ipomoea batatas) trypsin inhibitors expressed in transgenic tobacco plants confer resistance against Spodoptera litura. Plant Cell Rep. 1997, 16, 696-699.
8. Charity, J.A.; Anderson, M.A.; Bittisnich, D.J.; Whitecross, M.; Higgins, T.J.V. Transgenic tobacco and peas expressing a proteinase inhibitor from Nicotiana alata have increased insect resistance. Mol. Breed. 1999, 5, 357-365.
9. Bown, D.P.; Wilkinson, H.S.; Gatehouse, J.A. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochem. Mol. Biol. 1997, 27, 625-638.
10. Haq, S.K.; Atif, S.M.; Khan, R.H. Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: Natural and engineered phytoprotection. Arch. Biochem. Biophys. 2004, 431, 145-159.
11. Leplé, J.C.; Bonadé-Bottino, M.; Augustin, S.; Pilate, G.; Lê Tan, V.D.; Delplanque, A.; Cornu, D.; Jouanin, L. Toxicity tochrysomela tremulae (Coleoptera: Chrysomelidae) of transgenic poplars expressing a cysteine proteinase inhibitor. Mol. Breed. 1995, 1, 319-328.
12. Altpeter, F.; Diaz, I.; McAuslane, H.; Gaddour, K.; Carbonero, P.; Vasil, I.K. Increased insect resistance in transgenic wheat stably expressing trypsin inhibitor CMe. Mol. Breed. 1999, 5, 53-63.
13. Lee, S.I.; Lee, S.H.; Koo, J.C.; Chun, H.J.; Lim, C.O.; Mun, J.H.; Song, Y.H.; Cho, M.J. Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Mol. Breed. 1999, 5, 1-9.
14. Vila, L.; Quilis, J.; Meynard, D.; Breitler, J.C.; Marfa, V.; Murillo, I.; Vassal, J.M.; Messeguer, J.; Guiderdoni, E.; San Segundo, B. 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 Biotechnol. J. 2005, 3, 187-202.
15. Jongsma, M.A.; Bolter, C. The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 1997, 43, 885-895.
16. Harsulkar, A.M.; Giri, A.P.; Patankar, A.G.; Gupta, V.S.; Sainani, M.N.; Ranjekar, P.K.; Deshpande, V.V. Successive use of non-host plant proteinase inhibitors required for effective inhibition of Helicoverpa armigera gut proteinases and larval growth. Plant Physiol. 1999, 121, 497-506.
17. Jongsma, M.A.; Bakker, P.L.; Peters, J.; Bosch, D.; Stiekema, W.J. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA 1995, 92, 8041-8045.
18. Wu, Y.; Llewellyn, D.; Mathews, A.; Dennis, E.S. Adaptation of Helicoverpa armigera (Lepidoptera: Noctuidae) to a proteinase inhibitor expressed in transgenic tobacco. Mol. Breed. 1997, 3, 371-380.
19. Girard, C.; Bonade-Bottino, M.; Pham-Delegue, M.H.; Jouanin, L. Two strains of cabbage seed weevil (Coleoptera : Curculionidae) exhibit differential susceptibility to a transgenic oilseed rape expressing oryzacystatin I. J. Insect Physiol. 1998, 44, 569-577.
20. Cloutier, C.; Jean, C.; Fournier, M.; Yelle, S.; Michaud, D. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 2000, 44, 69-81.
21. Xu, Z.F.; Qi, W.Q.; Ouyang, X.Z.; Yeung, E.; Chye, M.L. A proteinase inhibitor II of Solanum americanum is expressed in phloem. Plant Mol. Biol. 2001, 47, 727-738.
22. Wang, Z.Y.; Ding, L.W.; Ge, Z.J.; Wang, Z.; Wang, F.; Li, N.; Xu, Z.F. Purification and characterization of native and recombinant SaPIN2a, a plant sieve element-localized proteinase inhibitor. Plant Physiol. Biochem. 2007, 45, 757-766.
23. Fitt, G.P. The ecology of heliothis species in relation to agroecosystems. Annu. Rev. Entomol. 1989, 34, 17-52.
24. Ahmad, M.; Saleem, M.A.; Sayyed, A.H. Efficacy of insecticide mixtures against pyrethroid-and organophosphate-resistant populations of Spodoptera litura Lepidoptera: Noctuidae. Pest Manage. Sci. 2009, 65, 266-274.
25. Xu, Z.F.; Teng, W.L.; Chye, M.L. Inhibition of endogenous trypsin- and chymotrypsin-like activities in transgenic lettuce expressing heterogeneous proteinase inhibitor SaPIN2a. Planta 2004, 218, 623-629.
26. Xie, J.; Ouyang, X.Z.; Xia, K.F.; Huang, Y.F.; Pan, W.B.; Cai, Y.P.; Xu, X.P.; Li, B.J.; Xu, Z.F. Chloroplast-like organelles were found in enucleate sieve elements of transgenic plants overexpressing a proteinase inhibitor. Biosci. Biotech. Biochem. 2007, 71, 2759-2765.
27. Satoh, J.; Kato, K.; Shinmyo, A. The 5′-untranslated region of the tobacco alcohol dehydrogenase gene functions as an effective translational enhancer in plant. J. Biosci. Bioeng. 2004, 98, 1-8.
28. Sugio, T.; Satoh, J.; Matsuura, H.; Shinmyo, A.; Kato, K. The 5′-untranslated region of the Oryza sativa alcohol dehydrogenase gene functions as a translational enhancer in monocotyledonous plant cells. J. Biosci. Bioeng. 2008, 105, 300-302.
29. Dansako, T.; Kato, K.; Satoh, J.; Sekine, M.; Yoshida, K.; Shinmyo, A. 5′ Untranslated region of the HSP18.2 gene contributes to efficient translation in plant cells. J. Biosci. Bioeng. 2003, 95, 52-58.
30. Abdeen, A.; Virgos, A.; Olivella, E.; Villanueva, J.; Aviles, X.; Gabarra, R.; Prat, S. Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Mol. Biol. 2005, 57, 189-202.
31. Chye, M.L.; Sin, S.F.; Xu, Z.F.; Yeung, E.C. Serine proteinase inhibitor proteins: Exogenous and endogenous functions. In Vitro Cell. Dev. Biol. Plant. 2006, 42, 100-108.
32. Telang, M.; Srinivasan, A.; Patankar, A.; Harsulkar, A.; Joshi, V.; Damle, A.; Deshpande, V.; Sainani, M.; Ranjekar, P.; Gupta, G.; Birah, A.; Rani, S.; Kachole, M.; Giri, A.; Gupta, V. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry 2003, 63, 643-652.
33. Harsulkar, A.M.; Giri, A.P.; Gupta, V.S.; Sainani, M.N.; Deshpande, V.V.; Patankar, A.G.; Ranjekar, P.K. Characterization of Helicoverpa armigera gut proteinases and their interaction with proteinase inhibitors using gel X-ray film contact print technique. Electrophoresis 1998, 19, 1397-1402.
34. Bhattacharyya, A.; Mazumdar Leighton, S.; Babu, C.R. Bioinsecticidal activity of Archidendron ellipticum trypsin inhibitor on growth and serine digestive enzymes during larval development of Spodoptera litura. Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2007, 145, 669-677.
35. Tamhane, V.A.; Chougule, N.P.; Giri, A.P.; Dixit, A.R.; Sainani, M.N.; Gupta, V.S. In vivo and in vitro effect of Capsicum annum proteinase inhibitors on Helicoverpa armigera gut proteinases. Biochim. Biophys. Acta, Gen. Subj. 2005, 1722, 156-167.
36. Sin, S.F.; Chye, M.L. Expression of proteinase inhibitor II proteins during floral development in Solanum americanum. Planta 2004, 219, 1010-1022.
37. Sin, S.F.; Yeung, E.C.; Chye, M.L. Downregulation of Solanum americanum genes encoding proteinase inhibitor II causes defective seed development. Plant J. 2006, 45, 58-70.
38. Liu, J.; Xia, K.F.; Zhu, J.C.; Deng, Y.G.; Huang, X.L.; Hu, B.L.; Xu, X.; Xu, Z.F. The nightshade proteinase inhibitor IIb gene is constitutively expressed in glandular trichomes. Plant Cell Physiol. 2006, 47, 1274-1284.
39. Berger, D.; Altmann, T. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev. 2000, 14, 1119-1131.
40. Tanaka, H.; Onouchi, H.; Kondo, M.; Hara-Nishimura, I.; Nishimura, M.; Machida, C.; Machida, Y. A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 2001, 128, 4681-4689.
41. Von Groll, U.; Berger, D.; Altmann, T., The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during arabidopsis stomatal development. Plant Cell 2002, 14, 1527-1539.
42. Wagner, G.J. Secreting glandular trichomes: more than just hairs. Plant physiol. 1991, 96, 675-679.
43. Amme, S.; Rutten, T.; Melzer, M.; Sonsmann, G.; Vissers, J.P.; Schlesier, B.; Mock, H.P. A proteome approach defines protective functions of tobacco leaf trichomes. Proteomics 2005, 5, 2508-2518.
44. Peter, A.J.; Shanower, T.G.; Romeis, J. The role of plant trichomes in insect resistance: a selective review. Phytophaga (Madras) 1995, 7, 41-64.
45. Neal, J.J.; Steffens, J.C.; Tingey, W.M. Glandular trichomes of Solanum berthaultii and resistance to the Colorado potato beetle. Entomol. Exp. Appl. 1989, 51, 133-140.
46. Lai, A.; Cianciolo, V.; Chiavarini, S.; Sonnino, A. Effects of glandular trichomes on the development of Phytophthora infestans infection in potato (S. tuberosum). Euphytica 2000, 114, 165-174.
47. Ascensao, L.; Marques, N.; Pais, M.S. Glandular trichomes on vegetative and reproductive organs of Leonotis leonurus (Lamiaceae). Ann. Bot. 1995, 75, 619-626.
48. Fernandez-Munoz, R.; Salinas, M.; Alvarez, M.; Cuartero, J. Inheritance of resistance to two-spotted spider mite and glandular leaf trichomes in wild tomato Lycopersicon pimpinellifolium (Jusl.) Mill. J. Am. Soc. Hortic. Sci. 2003, 128, 188-195.
49. Simmons, A.T.; Gurr, G.M.; McGrath, D.; Nicol, H.I.; Martin, P.M. Trichomes of Lycopersicon spp. and their effect on Myzus persicae (Sulzer) (Hemiptera : Aphididae). Aust. J. Entomol. 2003, 42, 373-378.
50. Simmons, A.T.; Gurr, G.M.; McGrath, D.; Martin, P.M.; Nicol, H.I. Entrapment of Helicoverpa armigera (Hubner) (Lepidoptera : Noctuidae) on glandular trichomes of Lycopersicon species. Aust. J. Entomol. 2004, 43, 196-200.
51. Saeidi, Z.; Mallik, B.; Kulkarni, R.S. Inheritance of glandular trichomes and two-spotted spider mite resistance in cross Lycopersicon esculentum "Nandi" and L pennellii "LA2963". Euphytica 2007, 154, 231-238.
52. Aruna, R.; Rao, D.M.; Reddy, L.J.; Upadhyaya, H.D.; Sharma, H.C. Inheritance of trichomes and resistance to pod borer (Helicoverpa armigera) and their association in interspecific crosses between cultivated pigeonpea (Cajanus cajan) and its wild relative C-scarabaeoides. Euphytica 2005, 145, 247-257.
53. Gregory, P.; Tingey, W.M.; Ave, D.A.; Bouthyette, P.Y. Potato glandular trichomes: a physic chemical defense mechanism against insects. ACS Symp. Ser. 1986, 296, 160-167.
54. Wagner, G.J.; Wang, E.; Shepherd, R.W. New approaches for studying and exploiting an old protuberance, the plant trichome. Ann. Bot. 2004, 93, 3-11.
55. Mcmanus, M.T.; White, D.W.R.; Mcgregor, P.G. Accumulation of a Chymotrypsin Inhibitor in Transgenic Tobacco Can Affect the Growth of Insect Pests. Transgenic Res. 1994, 3, 50-58.
56. Jefferson, R.A.; Kavanagh, T.A.; Bevan, M.W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987, 6, 3901-3907.
57. Hofgen, R.; Willmitzer, L. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 1988, 16, 9877.
58. Horsch, R.B.; Fry, J.E.; Hoffmann, N.L.; Eichholtz, D.; Rogers, S.G.; Fraley, R.T. A simple and general method for transferring genes into plants. Science 1985, 227, 1229-1231.
59. Doyle, J.J.; Doyle, J.L. Isolation of plant DNA from fresh tissue. Focus 1990, 12, 13-15.