Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T23:54:11.269Z Has data issue: false hasContentIssue false
  • English
  • Français

Response of antioxidant enzymes in Mythimna separata (Lepidoptera: Noctuidae) exposed to thermal stress

Published online by Cambridge University Press:  04 November 2016

A. Ali ,
M. A. Rashid ,
Q. Y. Huang ,
C. Wong  and
C.-L. Lei
A. Ali
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
M. A. Rashid
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
Q. Y. Huang
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
C. Wong
Affiliation:
Laboratory of Pesticide Toxicology, lowa State University, Ames, Iowa,USA
C.-L. Lei*
Affiliation:
Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China
*
*Author for correspondence Phone/Fax: +86 27 87287207 E-mail: ioir@mail.hzau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The oriental army worm Mythimna separata (Lepidoptera: Noctuidae) is a migratory pest in Eastern Asia and China. Seasonal high temperatures in Southern China and low temperatures in Northern China are pressures favouring the annual migration of this species, while cold tolerance determines the northern limit of its overwintering range. A number of physiological stress responses occur in insects as a result of variations in temperature. One reaction to thermal stress is the generation of reactive oxygen species (ROS), which can be harmful by causing oxidative damage. The time-related effects (durations of 1, 4 and 7 h) of thermal stress treatments of M. separata at comparatively low (5, 10, 15 and 20°C) and high (30, 35, 40 and 45°C) temperatures on the activities of antioxidant enzymes, including superoxide dismutase (SOD), catalase (CAT), peroxidase (POX) and glutathione S-transferases (GSTs), and total antioxidant capacity (T-AOC) were determined. Thermal stress resulted in significant elevation of the activities of SOD, CAT and GSTs, indicating that these enzymes contribute to defence mechanisms counteracting oxidative damage caused by an increase in ROS. However, at high-temperatures, POX and T-AOC were also found to contribute to scavenging ROS. Our results also indicate that extreme temperatures lead to elevated ROS production in M. separata. The present study confirms that thermal stress can be responsible for oxidative damage. To overcome such stress, antioxidant enzymes play key roles in diminishing oxidative damage in M. separata.

Keywords

thermal stressantioxidant enzymesoxidative stressMythimna separate
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 3 , June 2017 , pp. 382 - 390
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, S., Duval, D.L., Weinhold, L.C. & Pardini, R.S. (1991) Cabbage looper antioxidant enzymes: tissue specificity. Insect Biochemistry 21, 563–572.Google Scholar
Angilletta, M.J., Niewiarowski, P.H. & Navas, C.A. (2002) The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27, 249–268.Google Scholar
Aucoin, R., Guillet, G., Murray, C., Philogène, B.J. & Arnason, J.T. (1995) How do insect herbivores cope with the extreme oxidative stress of phototoxic host plants. Archives of Insect Biochemistry and Physiology 29, 211–226.Google Scholar
Board, P.G. & Menon, D. (2013) Glutathione transferases, regulators of cellular metabolism and physiology. Biochimica et Biophysica Acta 1830, 3267–3288.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google Scholar
Celino, F.T., Yamaguchi, S., Miura, C., Ohta, T., Tozawa, Y., Iwai, T. & Miura, T. (2011) Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase. PLoS ONE 6, e16938.Google Scholar
Chen, S.D. & Hu, B.H. (2000) Plant Protection in China in Fifty Years. Beijing, China, Agriculture Press.Google Scholar
Chen, R., Sun, Y., Wang, S., Zhai, B. & Bao, X. (1995) Mythimna Separata in East Asia in Relation to Weather and Climate. I. Northeastern China. Insect Migration: Tracking Resources through Space and Time. Cambridge, Cambridge University Press, pp. 93–104.Google Scholar
Chun, B.F. (1981) A new artificial diet for army worm. Acta Entomologica Sinica 24, 379–338.Google Scholar
Crespo, J.G., Vickers, N.J. & Goller, F. (2014) Male moths optimally balance take-off thoracic temperature and warm-up duration to reach a pheromone source quickly. Animal Behaviour 98, 79–85.Google Scholar
Dubovskiy, I., Martemyanov, V., Vorontsova, Y., Rantala, M., Gryzanova, E. & Glupov, V. (2008) Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). Comparative Biochemistry and Physiology C: Toxicology & Pharmacology 148, 1–5.Google Scholar
Felton, G.W. & Summers, C.B. (1995) Antioxidant systems in insects. Archives of Insect Biochemistry and Physiology 29, 187–197.Google Scholar
Ghiselli, A., Serafini, M., Natella, F. & Scaccini, C. (2000) Total antioxidant capacity as a tool to assess redox status: critical view and experimental data. Free Radical Biology and Medicine 29, 1106–1114.Google Scholar
Green, D.R. & Reed, J.C. (1998) Mitochondria and apoptosis. Science 281, 1309.Google Scholar
Howe, G.A. & Schilmiller, A.L. (2002) Oxylipin metabolism in response to stress. Current Opinion in Plant Biology 5, 230–236.CrossRefGoogle ScholarPubMed
Jena, K., Kar, P. K., Kausar, Z. & Babu, C.S. (2013) Effects of temperature on modulation of oxidative stress and antioxidant defenses in testes of tropical tasar silkworm Antheraea mylitta . Journal of Thermal Biology 38, 199–204.Google Scholar
Jia, F.X., Dou, W., Hu, F. & Wang, J.J. (2011) Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist 94, 956–963.Google Scholar
Jiang, X. (2004) The physiological and genetic characteristics of migratory behavior and genetic diversity, as determined by AFLP in the oriental armyworm, Mythimna separata (Walker). PhD dissertation, Chinese Academy of Agricultural Sciences, Beijing, China.Google Scholar
Jiang, X.F. & Luo, L.Z. (1997) Influence of temperature at pupal and adult stage on flight capacity of adult oriental armyworm, Mythimna separata (Walker). pp. 274–280 in Chen, X.F., Dai, X.F. & Hu, T. (Eds) Ecological Research Sustainable Development. Beijing, China, China Environmental Science Press.Google Scholar
Jiang, X.F., Luo, L.Z. & Hu, Y. (2000) Influences of rearing temperature on flight and reproductive capacity of adult oriental armyworm, Mythimna separata (Walker). Acta Ecologica Sinica 20, 288–292.Google Scholar
Jiang, X., Luo, L., Zhang, L., Sappington, T.W. & Hu, Y. (2011) Regulation of migration in Mythimna separata (Walker) in China: a review integrating environmental, physiological, hormonal, genetic, and molecular factors. Environmental Entomology 40, 516–533.Google Scholar
Jing, X.H., Wang, X.H. & Kang, L. (2005) Chill injury in the eggs of the migratory locust, Locusta migratoria (Orthoptera: Acrididae): the time temperature relationship with high temperature interruption. Insect Science 12, 171–178.CrossRefGoogle Scholar
Joanisse, D. & Storey, K. (1996) Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects. Journal of Experimental Biology 199, 1483–1491.Google Scholar
Joanisse, D.R. & Storey, K.B. (1998) Oxidative stress and antioxidants in stress and recovery of cold-hardy insects. Insect Biochemistry and Molecular Biology 28, 23–30.Google Scholar
Kashiwagi, A., Kashiwagi, K., Takase, M., Hanada, H. & Nakamura, M. (1997) Comparison of catalase in diploid and haploid Rana rugosa using heat and chemical inactivation techniques. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology 118, 499–503.Google Scholar
Kaur, G., Alam, M.S. & Athar, M. (2009) Cumene hydroperoxide debilitates macrophage physiology by inducing oxidative stress: possible protection by α-tocopherol. Chemico-Biological Interactions 179, 94–102.Google Scholar
Kotak, S., Larkindale, J., Lee, U., Von Koskull-Döring, P., Vierling, E. & Scharf, K.D. (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310–316.Google Scholar
Lalouette, L., Williams, C., Hervant, F., Sinclair, B.J. & Renault, D. (2011) Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations. Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology 158, 229–234.Google Scholar
Lopez-Martinez, G., Elnitsky, M.A., Benoit, J.B., Lee, R.E. & Denlinger, D.L. (2008) High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochemistry and Molecular Biology 38, 796–804.Google Scholar
Mahmud, S.A., Hirasawa, T. & Shimizu, H. (2010) Differential importance of trehalose accumulation in Saccharomyces cerevisiae in response to various environmental stresses. Journal of Bioscience and Bioengineering 109, 262–266.Google Scholar
Mangel, M. & Munch, S.B. (2005) A life history perspective on short and long term consequences of compensatory growth. The American Naturalist 166, E155–E176.Google Scholar
McCord, J.M. & Fridovich, I. (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry 244, 6049–6055.Google Scholar
Meng, J.Y., Zhang, C.Y., Zhu, F., Wang, X.P. & Lei, C.L. (2009) Ultraviolet light-induced oxidative stress: effects on antioxidant response of Helicoverpa armigera adults. Journal of Insect Physiology 55, 588–592.Google Scholar
Monaghan, P., Metcalfe, N.B. & Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12, 75–92.Google Scholar
Nabizadeh, P. & Kumar, T.J. (2011) Fat body catalase activity as a biochemical index for the recognition of thermotolerant breeds of mulberry silkworm, Bombyx mori L . Journal of Thermal Biology 36, 1–6.Google Scholar
Nguyen, T.M., Bressac, C. & Chevrier, C. (2013) Heat stress affects male reproduction in a parasitoid wasp. Journal of Insect Physiology 59, 248–254.Google Scholar
Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37, 637–669.Google Scholar
Rosa, R., Pimentel, M.S., Boavida, P.J., Teixeira, T., Trübenbach, K. & Diniz, M. (2012) Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid. PLoS ONE 7, e38282.Google Scholar
Ruilo, C. & Ziangshi, B. (1987) Research on the migration of oriental armyworm in China and a discussion of management strategy. International Journal of Tropical Insect Science 8, 571–572.Google Scholar
Rui-Lu, C., Xiang-zhe, B., Drake, V., Farrow, R., Su-Yun, W., Ya-Jie, S. & Bao-Ping, Z. (1989) Radar observations of the spring migration into northeastern China of the oriental armyworm moth, Mythimna separata, and other insects. Ecological Entomology 14, 149–162.Google Scholar
Sashidhara, K.V., Singh, S.P., Srivastava, A. & Puri, A. (2011) Identification of the antioxidant principles of Polyalthia longifolia var. pendula using TEAC assay. Natural Product Research 25, 918–926.Google Scholar
Sohal, R., Arnold, L. & Orr, W.C. (1990) Effect of age on superoxide dismutase, catalase, glutathione reductase, inorganic peroxides, TBA-reactive material, GSH/GSSG, NADPH/NADP+ and NADH/NAD+ in Drosophila melanogaster . Mechanisms of Ageing and Development 56, 223–235.Google Scholar
Wang, Y., Oberley, L.W. & Murhammer, D.W. (2001) Antioxidant defense systems of two lipidopteran insect cell lines. Free Radical Biology and Medicine 30, 1254–1262.Google Scholar
Wang, G.P., Zhang, Q.W., Ye, Z.H. & Luo, L.Z. (2006) The role of nectar plants in severe outbreaks of armyworm Mythimna separata (Lepidoptera: Noctuidae) in China. Bulletin of Entomological Research 96, 445–455.Google Scholar
Xinfu, J., Yueqiu, L. & Lizhi, L. (1998) Effects of high temperature on the immature stages of the oriental armyworm Mythimna separata Walker. Journal of Beijing Agricultural College (China) 13, 20–26.Google Scholar
Yang, L.H., Huang, H. & Wang, J.J. (2010) Antioxidant responses of citrus red mite, Panonychus citri (McGregor) (Acari: Tetranychidae), exposed to thermal stress. Journal of Insect Physiology 56, 1871–1876.Google Scholar
Zaman, K., MacGill, R.S., Johnson, J.E., Ahmad, S. & Pardini, R.S. (1995) An insect model for assessing oxidative stress related to arsenic toxicity. Archives of Insect Biochemistry and Physiology 29, 199–209.Google Scholar
Zhang, L., Luo, L.Z., Jiang, X.F. & Hu, Y. (2006) Influences of starvation on the first day after emergence on ovarian development and flight potential in adults of the oriental armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae). Acta Entomologica Sinica 49, 895–902.Google Scholar
Zhang, L., Jiang, X.F. & Luo, L.Z. (2008) Determination of sensitive stage for switching migrant oriental armyworms into residents. Environmental Entomology 37, 1389–1395.Google Scholar
Zhang, G.H., Liu, H., Wang, J.J. & Wang, Z.Y. (2014) Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of the predatory mite, Neoseiulus cucumeris (Acari: Phytoseiidae). Experimental and Applied Acarology 64, 73–85.Google Scholar
Zhang, S., Fu, W., Li, N., Zhang, F. & Liu, T.X. (2015) Antioxidant responses of Propylaea japonica (Coleoptera: Coccinellidae) exposed to high temperature stress. Journal of Insect Physiology 73, 47–52.Google Scholar