Skip to main content
SpringerLink
Log in

Molecular cloning, characterization, and antioxidant function of catalase in Lymantria dispar asiatic (Lepidoptera: Lymantriidae) under avermectin stress

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

The critical antioxidant catalase (CAT) breaks down hydrogen peroxide induced by environmental stresses. Here we cloned full length catalase cDNA from Lymantria dispar asiatic (LdCAT). Bioinformatic analyses showed that open reading frames of LdCAT contains 1524 bp, encoding 507 amino acids with molecular weight of 126.99 kDa, theoretical pI of 5.00, aliphatic index of 29.92, grand average of hydropathicity of 0.764, and instability index (II) of 46.56. Protein BLAST and multiple sequence alignment indicated that LdCAT had high identity with CAT from other insects, especially lepidopterans. In a phylogenetic analysis, LdCAT was most similar to CAT from Spodoptera litura and S. exigua. Quantitative real-time polymerase chain reaction showed that LdCAT transcripts in all instar larvae and the five tissues tested, verifying the ubiquity of LdCAT in L. disapr. Moreover, LdCAT of third instar larvae was significantly upregulated after they fed on avermectin at sublethal and LC10 doses. The highest relative transcript levels were found 2 h after an avermectin spray at LC90, and in the cuticula, rather than heads, fat bodies, malpighian tubes, and midguts after a spray avermectin at a sublethal concentration. The expression level of LdCAT under pesticide stresses here suggested that CAT is an important antioxidant enzyme of L. disapr defensing against pesticide stress and may be a good target for controlling this pest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bartos M, Falkinham OJIII, Pavlik I (2012) Mycobacterial catalases, peroxidases, and superoxide dismutases and their effects on virulence and isoniazid-susceptibility in mycobacteria–a review. Veterinární Medicína 49:161–170

    Google Scholar 

  • Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192–208

    CAS  PubMed  Google Scholar 

  • Chen L, Diao J, Zhang W, Zhang L, Wang Z, Li Y, Deng Y, Zhou Z (2019) Effects of beta-cypermethrin and myclobutanil on some enzymes and changes of biomarkers between internal tissues and saliva in reptiles (Eremias argus). Chemosphere 216:69–74

    CAS  PubMed  Google Scholar 

  • El-Gendy K, Radwan M, Gad A, Khamis A, Eshra E (2019) Use of multiple endpoints to investigate the ecotoxicological effects of abamectin and thiamethoxam on Theba pisana snails. Ecotox Environ Safe 167:242–249

    CAS  Google Scholar 

  • Fang S, Zhang Y, You X, Sun P, Qiu J, Kong F (2018) Lethal toxicity and sublethal metabolic interference effects of sulfoxaflor on the earthworm (Eisenia fetida). J Agr Food Chem 66:11902–11908

    CAS  Google Scholar 

  • Fateh R, Zaini F, Kordbacheh P, Falahati M, Rezaie S, Daie Ghazvini R, Borhani N, Safara M, Fattahi A, Kanani A, Farahyar S, Bolhassani M, Heidari M (2015) Identification and sequencing of Candida krusei aconitate hydratase gene using rapid amplification of cDNA ends method and phylogenetic analysis. Jundishapur J Microb 8:1–11

    Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem 29:187–197

    CAS  Google Scholar 

  • Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what’s in pROSpect? Plant, Cell Environ 39:951–964

    CAS  Google Scholar 

  • Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fridovich I (1978) The biology of oxygen radicals. Science 201:875–880

    CAS  PubMed  Google Scholar 

  • Gaetani G, Ferraris A, Rolfo M, Mangerini R, Arena J, Kirkman H (1994) Predominant role of catalase in the disposal of hydrogen peroxide within human erythrocytes. Blood 84:1595–1599

    Google Scholar 

  • Iummato MM, Sabatini SE, Cacciatore LC, Cochón AC, Cataldo D, Mdcr DM, Juárez ÁB (2018) Biochemical responses of the golden mussel Limnoperna fortunei under dietary glyphosate exposure. Ecotox Environ Safe 163:69–75

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kang Z, Liu F, Pang R, Tian H, Liu T (2018) Effect of sublethal doses of imidacloprid on the biological performance of aphid endoparasitoid Aphidius gifuensis (Hymenoptera: Aphidiidae) and influence on its related gene expression. Front Physiol 9:1–15

    Google Scholar 

  • Li G, Fan A, Peng G, Keyhani NO, Xin J, Cao Y, Xia Y (2017) A bifunctional catalase-peroxidase, MakatG1, contributes to virulence of Metarhizium acridum by overcoming oxidative stress on the host insect cuticle. Environ Microbiol 19:4365–4378

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, California) 25:402–408

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:200–203

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mcgillivray P, Ault R, Pawashe M, Kitchen R, Balasubramanian S, Gerstein M (2018) A comprehensive catalog of predicted functional upstream open reading frames in humans. Nucleic Acids Res 46:3326–3338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mermans C, Dermauw W, Geibel S, Van LT (2017) A G326E substitution in the glutamate-gated chloride channel 3 (GluCl3) of the two-spotted spider mite Tetranychus urticae abolishes the agonistic activity of macrocyclic lactones. Pest Manag Sci 73:2413–2418

    CAS  PubMed  Google Scholar 

  • Merzendorfer H (2006) Insect chitin synthases: a review. J Comp Physiol B 176:1–15

    CAS  PubMed  Google Scholar 

  • Qin J, Lu M, Zheng Y, Du Y (2016) Molecular cloning, characterization, and functional analysis of catalase in Frankliniella occidentalis (Thysanoptera: Thripidae). Ann Entomol Soc Am 110:212–220

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Santamaría ME, Arnaiz A, Velasco-Arroyo B, Grbic V, Diaz I, Martinez M (2018) Arabidopsis response to the spider mite Tetranychus urticae depends on the regulation of reactive oxygen species homeostasis. Sci Rep-Uk 8:1–13

    Google Scholar 

  • Shen Y, Li D, Tian P, Shen K, Zhu J, Feng M, Wan C, Yang T, Chen L, Wen F (2015) The catalase C-262T gene polymorphism and cancer risk: a systematic review and meta-analysis. Medicine 94:1–8

    Google Scholar 

  • Siddique S, Syed Q, Saleem Y, Adnan A, Qureshi FA (2015) Toxicity of avermectin B1b to earthworm and cockroaches. J Anim Plant Sci 25:844–850

    CAS  Google Scholar 

  • Song Y, Chen M, Zhou J (2017) Effects of three pesticides on superoxide dismutase and glutathione-S-transferase activities and reproduction of Daphnia magna. Arch Environ Prot 43:80–86

    Google Scholar 

  • Sun X, Song Q (2006) PKC-mediated USP phosphorylation is required for 20E-induced gene expression in the salivary glands of Drosophila melanogaster. Arch Insect Biochem Physiol 62:116–127

    CAS  PubMed  Google Scholar 

  • Sun L, Wang Z, Zou C, Cao C (2014) Transcription profiling of 12 Asian gypsy moth (Lymantria dispar) cytochrome P450 genes in response to insecticides. Arch Insect Biochem 85:181–194

    CAS  Google Scholar 

  • Tang Y, Wen M, Lian B, Cheng J, Wang K, Zhou B (2014) Detection, cloning, and sequencing of the enterotoxin gene of Clostridium perfringens type C isolated from goat. Turk J Vet Anim 36:153–158

    Google Scholar 

  • Tian X, Yang W, Wang D, Zhao Y, Yao R, Ma L, Ge C, Li X, Huang Z, He L (2018) Chronic brain toxicity response of juvenile Chinese rare minnows (Gobiocypris rarus) to the neonicotinoid insecticides imidacloprid and nitenpyram. Chemosphere 210:1006–1012

    CAS  PubMed  Google Scholar 

  • Vieira HLA, Pereira ACP, Carrondo MJT, Alves PM (2006) Catalase effect on cell death for the improvement of recombinant protein production in baculovirus-insect cell system. Bioproc Biosyst Eng 29:409–414

    CAS  Google Scholar 

  • Waltari E, Jia M, Jiang CS, Lu H, Huang J, Fernandez C, Finzi A, Kaufmann DE, Markowitz M, Tsuji M, Wu X (2018) 5′ rapid amplification of cDNA ends and illumina MiSeq reveals B cell receptor features in healthy adults, adults with chronic HIV-1 infection, cord blood, and humanized mice. Front Immunol 9:1–22

    Google Scholar 

  • Wan NF, Li X, Guo L, Ji XY, Zhang H, Chen YJ, Jiang JX (2018) Phytochemical variation mediates the susceptibility of insect herbivores to entomoviruses. J Appl Entomol 142:705–715

    CAS  Google Scholar 

  • Wann KT (2010) The cellular actions of the avermectins. Phytother Res 1:143–150

    Google Scholar 

  • Wei P, Che W, Wang J, Xiao D, Wang R, Luo C (2018) RNA interference of glutamate-gated chloride channel decreases abamectin susceptibility in Bemisia tabaci. Pestic Biochem Physiol 145:1–7

    CAS  PubMed  Google Scholar 

  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Method Mol Bio (Clifton, NJ) 112:531

    CAS  Google Scholar 

  • Xu ZF, Shi L, Peng JF, Shen GM, Wei P, Wu Q, He L (2016) Analysis of the relationship between P-glycoprotein and abamectin resistance in Tetranychus cinnabarinus (Boisduval). Pestic Biochem Phys 129:75–82

    CAS  Google Scholar 

  • Xu J, Lu M, Huang D, Du Y (2017) Molecular cloning, characterization, genomic structure and functional analysis of catalase in Chilo suppressalis. J Asia-Pac Entomol 20:331–336

    Google Scholar 

  • Zeng J, Zhang F, Wu Y, Zhang T, Zhang G (2018) Synergistic mechanism of combined using insecisides abamectin plus triflumuron for control larvae of Lymantria dispar (Lepidoptera: Lymantriidae). Sci Sil Sin 54: (accept, waiting for publication)

  • Zhang W, Chen W, Li Z, Ma L, Yu J, Wang H, Liu Z, Xu B (2018) Identification and characterization of three new cytochrome P450 genes and the Use of RNA interference to evaluate their roles in antioxidant defense in Apis cerana cerana fabricius. Front Physiol 9:1–16

    Google Scholar 

  • Zhao H, Sun X, Xue M, Zhang X, Li Q (2016a) Antioxidant enzyme responses induced by whiteflies in tobacco plants in defense against aphids: catalase may play a dominant role. PLoS ONE 11:1–17

    Google Scholar 

  • Zhao Y, Sun Q, Hu K, Ruan J, Yang X (2016b) Isolation, characterization, and tissue-specific expression of GABA A receptor α1 subunit gene of Carassius auratus gibelio after avermectin treatment. Fish Physiol Biochem 42:1–10

    CAS  Google Scholar 

  • Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD (2001) Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques 30:892–897

    CAS  PubMed  Google Scholar 

  • Zou C, Lv C, Wang Y, Cao C, Zhang G (2017) Larvicidal activity and insecticidal mechanism of Chelidonium majus on Lymantria dispar. Pestic Biochem Physiol 142:123–132

    CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

    Authors and Affiliations

    1. School of Forest, Northeast Forestry University, Harbin, 150040, People’s Republic of China

      Jianyong Zeng, Bowen Zhang, Thi Minh Dien Vuong, Tingting Zhang, Jing Yang & Guocai Zhang

    2. Vietnam Academy of Agricultural Sciences, Hanoi, 100803, Vietnam

      Thi Minh Dien Vuong

    Authors
    1. Jianyong Zeng
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Bowen Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Thi Minh Dien Vuong
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Tingting Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jing Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Guocai Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Guocai Zhang.

    Ethics declarations

    Conflict of interest

    The authors declare they have no conflict of interest.

    Additional information

    Publisher's Note

    Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

    Project funding: This research was funded by the Fundamental Research Funds for Chinese Central Universities (Grant Nos. 2572017AA18 and 2572018AA09), the Chinese Central Financial Forest Science and Technology Extension Demonstration Fund Project (Grant No. JLT[2016]13).

    The online version is available at http://www.springerlink.com

    Corresponding editor: Ruihai Chai.

    Jianyong Zeng and Bowen Zhang contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zeng, J., Zhang, B., Vuong, T.M.D. et al. Molecular cloning, characterization, and antioxidant function of catalase in Lymantria dispar asiatic (Lepidoptera: Lymantriidae) under avermectin stress. J. For. Res. 31, 2563–2570 (2020). https://doi.org/10.1007/s11676-019-01008-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11676-019-01008-6

    Keywords

    Search

    Navigation