Abstract
Digestive and detoxification enzyme activity and nutrient composition were examined in the body of fourth instar beet armyworms, Spodoptera exigua (Hübner), fed on transgenic Bacillus thuringiensis (Bt) and non-Bt cotton for different time periods. Nutrient composition and specific enzyme activities differed significantly between the S. exigua fed Bt vs. non-Bt cotton. At 1, 6 and 24 h, free fatty acid and glucose levels were significantly lower in S. exigua fed on Bt cotton than those fed on non-Bt cotton. S. exigua fed on Bt cotton had significantly higher trypsin and total superoxide dismutase (T-SOD) activities and significantly lower lipase, carboxylesterase and acetylcholinesterase activities than non-Bt fed worms for all feeding time periods. Differences were also observed among feeding times within each cotton variety group. Significantly lower free fatty acid and total amino acid were observed in S. exigua fed on Bt cotton for 24 h than in those fed for 1 h. Significantly lower activities of lipase and trypsin were detected in S. exigua fed on Bt cotton for 24 h than those for 1 and 4 h. However, carboxylesterase and acetylcholinesterase activities in S. exigua fed on Bt cotton for 24 h were significantly higher than those for 1, 4 and 6 h. The interaction between cotton variety and feeding time significantly affected the activities of lipase, trypsin, acetylcholinesterase and T-SOD enzymes in S. exigua. Measuring the temporal allocation of protection and detoxification enzyme activities in the body of S. exigua in response to B. thuringiensis can provide a meaningful evaluation on the metabolic tolerance of herbivorous insects under the continuous selection pressure of a toxic protein.
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References
Ferry N, Edwards M G, Gatehouse J, et al. Transgenic plants for insect pest control: A forward looking scientific perspective. Transgenic Res, 2006, 15:13–19, 1:CAS:528:DC%2BD28XhtlSqt70%3D, 16475006, 10.1007/s11248-005-4803-x
Mascarenhas V J, Graves J B, Leonard B R, et al. Susceptibility of field populations of beet armyworm (Lepidoptera: Noctuidae) to commercial and experimental insecticides. J Econ Entomol, 1998, 91:827–833, 1:CAS:528:DyaK1cXlslClurg%3D
James C. Global status of commercialized biotech/GM crops: 2006. ISAAA Briefs, No. 35. Ithaca: ISAAA, 2006
Zhang S Y, Li D M, Cui J, et al. Effects of Bt-toxin Cry1Ac on Propylaea japonica Thunberg (Col., Coccinellidae) by feeding on Bt-treated Bt-resistant Helicoverpa armigera (Hübner) (Lep., Noctuidae) larvae. J Appl Entomol, 2006, 130:206–212, 1:CAS:528:DC%2BD28XlvVyiurY%3D, 10.1111/j.1439-0418.2006.01049.x
Blumberg D, Navon A, Goldenberg S K S, et al. Interactions among Helicoverpa armigera (Lepidoptera: Noctuidae), its larval endoparasitoid Microplitis croceipes (Hymenoptera: Braconidae), and Bacillus thuringiensis. J Econ Entomol, 1997, 90:1181–1186
Wu G, Marvin K H, Guo J Y, et al. Response of multiple generations of beet armyworm, Spodoptera exigua (Hübner), feeding on transgenic Bt cotton. J Appl Entomol, 2008, 133:90–100, 10.1111/j.1439-0418.2008.01328.x
Schnepf E, Crickmore N, Van Rie J, et al. Revision of the nomencla ture for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol Mol Bio Rev, 1998, 62:775–806, 1:CAS:528:DyaK1cXmtFOju7w%3D
Kranthi K R, Naidu S, Dhawad C S, et al. Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera. Current Sci, 2005, 89:291–298, 1:CAS:528:DC%2BD2MXpvVWltLw%3D
Ma X M, Liu X X, Zhang Q W, et al. Assessment of cotton aphids, Aphis gossypii, and their natural enemies on aphid-resistant and aphid-susceptible wheat varieties in a wheat-cotton relay intercropping system. Entomol Exp Appl, 2006, 121:235–241, 10.1111/j.1570-8703.2006.00484.x
Shelton A, Zhao J Z, Roush R. Economic, ecological, food safety, and social consequences of the development of Bt transgenic plants. Ann Rev Entomol, 2002, 47:845–881, 1:CAS:528:DC%2BD38XnvVWluw%3D%3D, 10.1146/annurev.ento.47.091201.145309
Chitkowski R L, Turnipseed S G, Sullivan M J, et al. Field and laboratory evaluations of transgenic cottons expressing one and two Bacillus thuringiensis var. kurstaki Berliner proteins for management of Noctuid (Lepidoptera) pests. J Econ Entomol, 2003, 96:755–762, 1:CAS:528:DC%2BD3sXlsVShsLg%3D, 12852613, 10.1603/0022-0493-96.3.755
Wu K M, Guo Y Y, Lv N, et al. Efficacy of transgenic cotton containing a Cry 1 Ac gene from Bacillus thuringiensis against Helicoverpa armigera (Lepidoptera: Noctuidae) in northern China. J Econ Entomol, 2003, 96:1322–1328, 1:CAS:528:DC%2BD3sXns1Knsr8%3D, 14503607, 10.1603/0022-0493-96.4.1322
Tabashnik B E. Evolution of resistance to Bacillus thuringiensis. Ann Rev Entomol, 1994, 39:47–49, 10.1146/annurev.en.39.010194.000403
Dingha B N, Moar W, Apple A G. Effects of Bacillus thuringiensis Cry 1C toxin on the metabolic rate of Cry 1C resistant and susceptible Spodoptera exigua (Lepidoptera: Noctuidae). Physiol Entomol, 2004, 29:409–418, 1:CAS:528:DC%2BD2MXjslSmtA%3D%3D, 10.1111/j.0307-6962.2004.00409.x
Adamczyk J J Jr., Holloway J W, Church G E, et al. Larval survival and development of the fall armyworm (Lepidoptera: Noctuidae) on normal and transgenic cotton expressing the Bacillus thuringiensis Cry1A(c)-endotoxin. J Econ Entomol, 1998, 91:539–545, 1:CAS:528:DyaK1cXjtFWjsbg%3D
Stewart S D, Adamczyk J J, Knighten K S, et al. Impact of Bt cotton expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. J Econ Entomol, 2001, 94:752–760, 1:CAS:528:DC%2BD3MXkvFegu70%3D, 11425033, 10.1603/0022-0493-94.3.752
Shi H, Zhang L F, Hua B Z, et al. Insecticidal activity of residual Bt protein at the second trophic level. Chin Sci Bull, 2006, 51:946–951, 1:CAS:528:DC%2BD28XktVejsr0%3D, 10.1007/s11434-006-0946-2
Guo T B, Ji B Z, Zhu G Q, et al. Effect of transgenic poplars on the activities of detoxification enzymes in Micromelalopha troglodyta larvae. Scientia Silvae Sinicae, 2007, 43:59–63, 1:CAS:528:DC%2BD2sXmvFOks7w%3D
Gutierrez A P, Adamczyk J J, Ponsard S, et al. Physiologically based demographics of Bt cotton-pest interactions II. Temporal refuges, natural enemy interactions. Ecol Model, 2006, 191:360–382, 10.1016/j.ecolmodel.2005.06.002
Dong H Z, Li W J. Variability of endotoxin expression in Bt transgenic cotton. J Agron Crop Sci, 2007, 193:21–29, 1:CAS:528:DC%2BD2sXjtF2itrk%3D, 10.1111/j.1439-037X.2006.00240.x
Li G H, Chen Q J, Pang Y. Studies of artificial diets for the beet armyworm, Spodoptera exigua. Acta Sci Nat Univ Sunyatseni, 1998, 37:1–5
Van Asperen K. A study of house fly esterase by means of a sensitive colourimetric method. J Insect Physiol, 1962, 8:401–416, 1:CAS:528:DyaF3sXkvVens7c%3D, 10.1016/0022-1910(62)90074-4
Bradford M M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein binding. Anal Biochem, 1976, 72:248–254, 1:CAS:528:DyaE28XksVehtrY%3D, 942051, 10.1016/0003-2697(76)90527-3
SAS Institute Inc. SAS/STAT software: Changes and enhancements through release 6. 12. Cary (NC): SAS Institute Inc. 1996
James C. Global review of commercialized transgenic crops: 1998. ISAAA Briefs, No. 8. Ithaca: ISAAA, 1998
Pray C, Ma D M, Huang J K, et al. Impact of Bt cotton in China. World Develop, 2001, 29:813–825, 10.1016/S0305-750X(01)00010-9
Wu K M, Guo Y Y. The evolution of cotton pest management practices in China. Ann Rev Entomol, 2005, 50:31–52, 1:CAS:528:DC%2BD2MXhtFOqt7w%3D, 10.1146/annurev.ento.50.071803.130349
Dutton A, Romeis J, Bigler F. Effects of Bt maize expressing Cry1Ab and Bt spray on Spodoptera littoralis. Entomol Exp Appl, 2005, 114:161–169, 1:CAS:528:DC%2BD2MXjtFeku74%3D, 10.1111/j.1570-7458.2005.00239.x
Liu X X, Zhang Q W, Zhao J Z, et al. Effects of the Cry1Ac toxin of Bacillus thuringiensis on Microplitis mediator, a parasitoid of the cotton bollworm, Helicoverpa armigera. Entomol Exp Appl, 2005a, 114:205–213, 1:CAS:528:DC%2BD2MXjtFeku7s%3D, 10.1111/j.1570-7458.2005.00248.x
Liu X D, Zhai B P, Zhang X X, et al. Impact of transgenic cotton plants on a non-target pest, Aphis gossypii Glover. Ecol Entomol, 2005b, 30:307–315, 10.1111/j.0307-6946.2005.00690.x
Dutton A, Klein H, Romeis J, et al. Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol Entomol, 2002, 27:441–447, 10.1046/j.1365-2311.2002.00436.x
Wu K M, Guo Y Y, Lv N, et al. Resistance monitoring of Helicoverpa armigera (Lepidoptera: Noctuidae) to Bacillus thuringiensis insecticidal protein in China. J Econ Entomol, 2002, 95:826–831, 12216827, 10.1603/0022-0493-95.4.826
Coviella C E, Trumble J T. Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conserv Biol, 1999, 13:700–712, 10.1046/j.1523-1739.1999.98267.x
Tabashnik B E, Liu Y B, Dennehy T J, et al. Inheritance of resistance to Bt toxin Cry1Ac in a field-derived strain of pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol, 2002, 95:1018–1026, 1:CAS:528:DC%2BD38XoslCgtro%3D, 12403429, 10.1603/0022-0493-95.5.1018
Wilson W D, Flint H M, Deaton R W, et al. Resistance of cotton lines containing a Bacillus thuringiensis toxin to pink bollworm (Lepidoptera: Gelechiidae) and other insects. J Entomol Sci, 1992, 34:415–425
Cui J J, Xia J Y. Effects of Bt (Bacillus thuringiensis) transgenic cotton on the dynamics of pest population and their enemies. Acta Phytophyl Sin, 2000, 27:141–145
Chen F J, Wu G, Parajulee M N, et al. Long-term impacts of elevated carbon dioxide and transgenic Bt cotton on performance and feeding of three generations of cotton bollworm. Entomol Exp Appl, 2007, 124:27–35, 10.1111/j.1570-7458.2007.00563.x
Groeters F R, Tabashnik B E, Finson N, et al. Resistance to Bacillus thuringiensis affects mating success of diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol, 1993, 86:1035–1039
Groeters F R, Tabashnik B E, Finson N J, et al. Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution, 1994, 48:197–201, 10.2307/2410015
Carriere Y, Ellers-Kirk C, Patin A L, et al. Over wintering cost associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol, 2001, 94:935–941, 1:CAS:528:DC%2BD3MXnt1SqsLk%3D, 11561855, 10.1603/0022-0493-94.4.935
Zhang Y J, Wu K M, Guo Y Y. On the spatio-temporal expressing of the contents of Bt insecticidal protein and the resistance of Bt transgenic cotton to cotton bollworm. Acta Phytophysiol Sin, 2001, 28:1–6
Luo K, Adang M J. Removal of adsorbed toxin fragments that modify Bacillus thuringiensis Cry1C delta-endotoxin iodination and binding by sodium dodecyl sulfate treatment and renaturation. Appl Environ Microbiol, 1994, 60:2905–2910, 1:CAS:528:DyaK2cXlt1OksrY%3D, 16349357
Stapel J O, Waters D J, Ruberson J R, et al. Development and behavior of Spodoptera exigua (Lepidoptera: Noctuidae) larvae in choice tests with food substrates containing toxins of Bacillus thuringiensis. Biol Control, 1998, 11:29–37, 10.1006/bcon.1997.0576
Ashfaq A, Young S Y, McNew R W. Development of Spodoptera exigua and Helicoverpa zea (Lepidoptera: Noctuidae) on transgenic cotton containing Cry1Ac insecticidal protein. J Entomol Sci, 2000, 35:360–372
Moar W J, Pusztai-Carey M, Van Faassen H, et al. Development of Bacillus thuringiensis Cry1C resistance by Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Appl Environ Microbiol, 1995, 61:2086–2092, 1:CAS:528:DyaK2MXlvFOgsbk%3D, 16535038
Berdegue M, Trumble J T, Moar W J. Effect of Cry1C toxin from Bacillus thuringiensis on larval feeding behavior of Spodoptera exigua. Entomol Exp Appl, 1996, 80:389–401, 1:CAS:528:DyaK28XlsVamtLs%3D
Huang F N. Detection and monitoring of insect resistance to transgenic Bt crops. Insect Sci, 2006, 13:73–84, 1:CAS:528:DC%2BD28XlvV2qur4%3D
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Guo, J., Wu, G. & Wan, F. Temporal allocation of metabolic tolerance to transgenic Bt cotton in beet armyworm, Spodoptera exigua (Hübner). Sci. China Life Sci. 54, 152–158 (2011). https://doi.org/10.1007/s11427-010-4133-y
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DOI: https://doi.org/10.1007/s11427-010-4133-y