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Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of the predatory mite, Neoseiulus cucumeris (Acari: Phytoseiidae)

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Abstract

Changes in temperature are known to cause a variety of physiological stress responses in insects and mites. Thermal stress responses are usually associated with the increased generation of reactive oxygen species (ROS), resulting in oxidative damage. In this study, we examined the time-related effect (durations for 1, 2, 3, and 5 h) of thermal stress conditions—i.e., relatively low (0, 5, 10, and 15 °C) or high (35, 38, 41, and 44 °C) temperatures—on the activities of antioxidant enzymes including catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), glutathione S-transferases (GSTs), and total antioxidant capacity (T-AOC) of the predatory mite Neoseiulus cucumeris. Also the lipid peroxidation (LPO) levels of the predatory mite were measured under thermal stress conditions. The results confirmed that thermal stress results in a condition of so-called oxidative stress and the four antioxidant enzymes play an important role in combating the accumulation of ROS in N. cucumeris. CAT and POX activity changed significantly when the mites were exposed to cold and heat shock, respectively. The elevated levels of SOD and GSTs activity, expressed in a time-dependent manner, may have an important role in the process of antioxidant response to thermal stress. However, the levels of LPO in N. cucumeris were high, serving as an important signal that these antioxidant enzyme-based defense mechanisms were not always adequate to counteract the surplus ROS. Thus, we hypothesize that thermal stress, especially extreme temperatures, may contribute much to the generation of ROS in N. cucumeris, and eventually to its death.

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References

  • Ahmad S, Duval DL, Weinhold LC, Pardini RS (1991) Cabbage looper antioxidant enzymes: tissue specificity. Insect Biochem 21:563–572

    Article  CAS  Google Scholar 

  • An MI, Choi CY (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comp Biochem Physiol B: Biochem Mol Biol 155:34–42

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Celino FT, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen E-H, Wei D, Wei D-D, Yuan G-R, Wang J-J (2013) The effect of dietary restriction on longevity, fecundity, and antioxidant responses in the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). J Insect Physiol 59:1008–1016

    Google Scholar 

  • Coombs MR, Bale JS (2013) Comparison of thermal activity thresholds of the spider mite predators Phytoseiulus macropilis and Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 59:435–445

    Article  PubMed  Google Scholar 

  • Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–328

    Article  PubMed  Google Scholar 

  • Easterbrook M, Fitzgerald J, Solomon M (2001) Biological control of strawberry tarsonemid mite Phytonemus pallidus and two-spotted spider mite Tetranychus urticae on strawberry in the UK using species of Neoseiulus (Amblyseius) (Acari: Phytoseiidae). Exp Appl Acarol 25:25–36

    Article  CAS  PubMed  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  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 Radic Biol Med 29:1106–1114

    Article  CAS  PubMed  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Sci-AAAS-Wkly Pap Ed 281:1309–1311

    CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Imai H, Nakagawa Y (2003) Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 34:145–169

    Article  CAS  PubMed  Google Scholar 

  • Jena K, Kumar Kar P, Kausar Z, Babu CS (2013) Effects of temperature on modulation of oxidative stress and antioxidant defences in testes of tropical tasar silkworm Antheraea mylitta. J Therm Biol 38:199–204

    Article  CAS  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). Fla Entomol 94:956–963

    Google Scholar 

  • Joanisse D, Storey K (1996) Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects. J Exp Biol 199:1483–1491

    CAS  PubMed  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. Comp Biochem Physiol B: Biochem Mol Biol 118:499–503

    Article  CAS  Google Scholar 

  • Kaur G, Alam MS, Athar M (2009) Cumene hydroperoxide debilitates macrophage physiology by inducing oxidative stress: possible protection by α-tocopherol. Chem Biol Interact 179:94–102

    Article  CAS  PubMed  Google Scholar 

  • Li M, Fu Y-G (2007) A study on life table of the laboratory population of Amblyseius cucumeris Oudemans. Plant Proc 33(2):84–87

    CAS  Google Scholar 

  • Livingstone D (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE Jr, Denlinger DL (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 Biochem Mol Biol 38:796–804

    Article  CAS  PubMed  Google Scholar 

  • Mahmud SA, Hirasawa T, Shimizu H (2010) Differential importance of trehalose accumulation in Saccharomyces cerevisiae in response to various environmental stresses. J Biosci Bioeng 109:262–266

    Article  CAS  PubMed  Google Scholar 

  • Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192:1–15

    Article  CAS  PubMed  Google Scholar 

  • McMurtry J, Croft B (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321

    Article  CAS  PubMed  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. J Insect Physiol 55:588–592

    Article  CAS  PubMed  Google Scholar 

  • Messelink GJ, Van Steenpaal SE, Ramakers PM (2006) Evaluation of phytoseiid predators for control of western flower thrips on greenhouse cucumber. Biocontrol 51:753–768

    Article  Google Scholar 

  • Montserrat M, Guzmán C, Sahún R, Belda J, Hormaza J (2013a) Pollen supply promotes, but high temperatures demote, predatory mite abundance in avocado orchards. Agric Ecosyst Environ 164:155–161

    Article  Google Scholar 

  • Montserrat M, Sahún RM, Guzmán C (2013b) Can climate change jeopardize predator control of invasive herbivore species? A case study in avocado agro-ecosystems in Spain. Exp Appl Acarol 59:27–42

    Article  PubMed  Google Scholar 

  • Morewood WD (1993) Diapause and cold hardiness of phytoseiid mites (Acarina: Phytoseiidae). Eur J Entomol 90:3

    Google Scholar 

  • Nabizadeh P, Jagadeesh Kumar T (2011) Fat body catalase activity as a biochemical index for the recognition of thermotolerant breeds of mulberry silkworm, Bombyx mori L. J Therm Biol 36:1–6

    Article  CAS  Google Scholar 

  • Nair PMG, Choi J (2011) Identification, characterization and expression profiles of Chironomus riparius glutathione S-transferase (GST) genes in response to cadmium and silver nanoparticles exposure. Aquat Toxicol 101:550–560

    Article  CAS  PubMed  Google Scholar 

  • Ozawa R, Nishimura O, Yazawa S, Muroi A, Takabayashi J, Arimura G (2012) Temperature-dependent, behavioural, and transcriptional variability of a tritrophic interaction consisting of bean, herbivorous mite, and predator. Mol Ecol 21:5624–5635

    Article  PubMed  Google Scholar 

  • Rosa R, Pimentel MS, Boavida-Portugal 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roy M, Brodeur J, Cloutier C (2003) Effect of temperature on intrinsic rates of natural increase (rm) of a coccinellid and its spider mite prey. Biocontrol 48:57–72

    Article  Google Scholar 

  • Rudneva I (1999) Antioxidant system of black sea animals in early development. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 122:265–271

    CAS  Google Scholar 

  • Sawicki R, Singh S, Mondal A, Benes H, Zimniak P (2003) Cloning, expression and biochemical characterization of one Epsilon-class (GST-3) and ten Delta-class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem J 370:661–669

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh SP, Coronella JA, Beneš H, Cochrane BJ, Zimniak P (2001) Catalytic function of Drosophila melanogaster glutathione S-transferase Dmgsts1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur J Biochem 268:2912–2923

    Article  CAS  PubMed  Google Scholar 

  • Sohal R, Arnold L, Orr WC (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. Mech Ageing Dev 56:223–235

    Article  CAS  PubMed  Google Scholar 

  • Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Storey KB (1997) Organic solutes in freezing tolerance. Comp Biochem Physiol A Physiol 117:319–326

    Article  CAS  PubMed  Google Scholar 

  • van Houten YM, van Rijn PCJ, Tanigoshi LK, van Stratum P, Bruin J (1995) Preselection of predatory mites to improve year-round biological control of western flower thrips in greenhouse crops. Entomol Exp Appl 74:225–234

    Article  Google Scholar 

  • Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bährmann R, Fabian B, Heinrich W, Köhler G, Lichter D (2003) Trophic levels are differentially sensitive to climate. Ecology 84:2444–2453

    Article  Google Scholar 

  • Wang H-S, Kang L (2005) Effect of cooling rates on the cold hardiness and cryoprotectant profiles of locust eggs. Cryobiology 51:220–229

    Article  CAS  PubMed  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. J Insect Physiol 56:1871–1876

    Google Scholar 

  • Zhang Y-X, Zhang Z-Q, Lin J-Z, JI J (2000) Potential of Amblyseius cucumeris (Acari: Phytoseiidae) as a biocontrol agent against Schizotetranychus nanjingensis (Acari: Tetranychidae) in Fujian, China. Syst Appl Acarol Spec Publ 4:109–124

    Google Scholar 

  • Zhang Y-X, Jian-Zhen L, Jie J, Xie C, Yu-Mei K (2004) Analyses of numerical responses and main life parameters for determining the suppression of Amblyseius cucumeris on Panonychus citri. Sci Agric Sin 37:1866–1873 (In Chinese with English Abstract)

    Google Scholar 

  • Zhu M, Hou B-H, Wu W-N, Fang X-D, Guo M-F (2010) Mites of tea plantation and releasing of Amblyseius cucumeris (Acari: Phytoseiidae) for control of Brevipalpus obovatus (Acari: Tenuipalpidae). J Environ Entomol 32:204–209

    Google Scholar 

  • Zilahi-Balogh G, Shipp J, Cloutier C, Brodeur J (2007) Predation by Neoseiulus cucumeris on western flower thrips, and its oviposition on greenhouse cucumber under winter vs. summer conditions in a temperate climate. Biol Control 40:160–167

    Article  Google Scholar 

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Acknowledgments

This study was supported by the National Public Benefit Industry (Agriculture) Research Projects, the Ministry of Agriculture, (200903032).

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  1. Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing, 400715, China

    Guo-Hao Zhang, Huai Liu, Jin-Jun Wang & Zi-Ying Wang

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  1. Guo-Hao Zhang
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  2. Huai Liu
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  4. Zi-Ying Wang
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Correspondence to Huai Liu.

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Zhang, GH., Liu, H., Wang, JJ. et al. Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of the predatory mite, Neoseiulus cucumeris (Acari: Phytoseiidae). Exp Appl Acarol 64, 73–85 (2014). https://doi.org/10.1007/s10493-014-9806-y

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