烟粉虱MEAM1隐种磷脂氢谷胱甘肽过氧化物酶基因克隆与表达分析
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摘要
【目的】本研究旨在从烟粉虱Bemisia tabaci中东-小亚细亚1隐种(Middle East-Asia Minor 1, MEAM1)中克隆磷脂氢谷胱甘肽过氧化物酶(phospholipid hydroperoxide glutathione peroxidase, PHGPX)基因,鉴定其在烟粉虱不同发育阶段及吡虫啉处理不同时间后雌成虫体内的表达情况,明确其在烟粉虱应对外界环境压力中的功能。【方法】利用3′RACE克隆和测定烟粉虱MEAM1隐种内PHGPX基因的cDNA全长序列,并对其编码的氨基酸序列进行生物信息学分析;利用定量RT-PCR技术对该基因在烟粉虱MEAM1隐种不同发育阶段及吡虫啉处理不同时间后雌成虫体内的表达量进行分析。【结果】获得了烟粉虱MEAM1隐种两个磷脂氢谷胱甘肽过氧化物酶基因的全长cDNA序列,分别命名为BtB-PHGPX1(GenBank登录号:KY312116)和BtB-PHGPX2(GenBank登录号:KY312117)。序列分析表明,BtB-PHGPX1基因开放阅读框全长732 bp,编码243个氨基酸;BtB-PHGPX2基因开放阅读框全长567 bp,编码188个氨基酸。序列比对结果表明两基因的编码蛋白内均具有谷胱甘肽过氧化物酶保守的半胱氨酸、谷氨酰胺和色氨酸残基位点。BtB-PHGPX1在烟粉虱MEAM1隐种卵内表达量显著高于其在若虫、伪蛹、雌成虫和雄成虫内的表达量,BtB-PHGPX2在烟粉虱MEAM1隐种卵内的表达量显著低于其在若虫、伪蛹和雌成虫内的表达量(P<0.05)。BtB-PHGPX1和BtB-PHGPX2在雌成虫内的表达量均显著高于雄成虫内。吡虫啉处理雌成虫2 h时两基因的表达量均较对照显著提高(P<0.05),处理后5, 10和24 h时其表达量均较对照显著下降(P<0.01)。【结论】本研究克隆了烟粉虱MEAM1隐种两个PHGPX基因的序列全长,明确了其在不同发育阶段及吡虫啉处理不同时间后雌成虫体内的差异表达,推测PHGPX在烟粉虱抵御环境压力及杀虫剂胁迫时可能发挥着重要的防御作用。
【Aim】 The objective of this study is to clone phospholipid hydroperoxide glutathione peroxidase(PHGPX) genes from Bemisia tabaci MEAM1 cryptic species, to identify their expression levels in whiteflies at different developmental stages and in female adults treated with imidacloprid for different time, and to elucidate their function in the whitefly in response to environmental pressure. 【Methods】 The cDNAs of PHGPX genes were cloned by 3′RACE from B. tabaci MEAM1 cryptic species, and the putative amino acid sequences were analyzed by bioinformatics methods. The expression levels of PHGPX genes in the whitefly at different developmental stages and in female adults treated with imidacloprid for different time were analyzed by quantitative reverse transcription-polymerase chain reaction(qRT-PCR). 【Results】 The full-length cDNA sequences of two PHGPX genes were obtained from B. tabaci MEAM1 cryptic species, and named as BtB-PHGPX1(GenBank accession no.: KY312116) and BtB-PHGPX2(GenBank accession no.: KY312117), respectively. Sequence analysis indicated that the open reading frame of BtB-PHGPX1 is 732 bp in length encoding 243 amino acids, while that of BtB-PHGPX2 is 567 bp in length encoding 188 amino acids. Sequence alignment result showed that the encoded proteins of both genes have conserved cysteine, glutamine and tryptophan residues of glutathione peroxidase. The mRNA level of BtB-PHGPX1 in egg was significant higher than those in nymph, pseudopupa, female adult and male adult of the whitefly, while that of BtB-PHGPX2 in egg was significant lower than those in nymph, pseudopupa and female adult(P<0.05). The mRNA levels of both BtB-PHGPX1 and BtB-PHGPX2 in female adults were significant higher than those in male adults(P<0.05). Furthermore, the expression levels of BtB-PHGPX1 and BtB-PHGPX2 significantly increased in female adults at 2 h after treatment with imidacloprid as compared with their respective control(P<0.05), but decreased significantly at 5, 10 and 24 h after treatment(P<0.01). 【Conclusion】 In this study, the full-length sequences of two PHGPX genes were cloned from B. tabaci MEAM1 cryptic species, and their differential expression at different developmental stages and in female adults treated with imidacloprid for different time was clarified. It is speculated that PHGPX may play an important defense role in B. tabaci under environmental stress and insecticide treatment.
【Aim】 The objective of this study is to clone phospholipid hydroperoxide glutathione peroxidase(PHGPX) genes from Bemisia tabaci MEAM1 cryptic species, to identify their expression levels in whiteflies at different developmental stages and in female adults treated with imidacloprid for different time, and to elucidate their function in the whitefly in response to environmental pressure. 【Methods】 The cDNAs of PHGPX genes were cloned by 3′RACE from B. tabaci MEAM1 cryptic species, and the putative amino acid sequences were analyzed by bioinformatics methods. The expression levels of PHGPX genes in the whitefly at different developmental stages and in female adults treated with imidacloprid for different time were analyzed by quantitative reverse transcription-polymerase chain reaction(qRT-PCR). 【Results】 The full-length cDNA sequences of two PHGPX genes were obtained from B. tabaci MEAM1 cryptic species, and named as BtB-PHGPX1(GenBank accession no.: KY312116) and BtB-PHGPX2(GenBank accession no.: KY312117), respectively. Sequence analysis indicated that the open reading frame of BtB-PHGPX1 is 732 bp in length encoding 243 amino acids, while that of BtB-PHGPX2 is 567 bp in length encoding 188 amino acids. Sequence alignment result showed that the encoded proteins of both genes have conserved cysteine, glutamine and tryptophan residues of glutathione peroxidase. The mRNA level of BtB-PHGPX1 in egg was significant higher than those in nymph, pseudopupa, female adult and male adult of the whitefly, while that of BtB-PHGPX2 in egg was significant lower than those in nymph, pseudopupa and female adult(P<0.05). The mRNA levels of both BtB-PHGPX1 and BtB-PHGPX2 in female adults were significant higher than those in male adults(P<0.05). Furthermore, the expression levels of BtB-PHGPX1 and BtB-PHGPX2 significantly increased in female adults at 2 h after treatment with imidacloprid as compared with their respective control(P<0.05), but decreased significantly at 5, 10 and 24 h after treatment(P<0.01). 【Conclusion】 In this study, the full-length sequences of two PHGPX genes were cloned from B. tabaci MEAM1 cryptic species, and their differential expression at different developmental stages and in female adults treated with imidacloprid for different time was clarified. It is speculated that PHGPX may play an important defense role in B. tabaci under environmental stress and insecticide treatment.
引文
Agrawal GK, Rakwal R, Jwa NS, Agrawal VP, 2002. Effects of signaling molecules, protein phosphatase inhibitors and blast pathogen (Magnaporthe grisea) on the mRNA level of a rice (Oryza sativa L.) phospholipid hydroperoxide glutathione peroxidase (OsPHGPx) gene in seedling leaves. Gene, 283: 227-236.
Bae YA, Cai GB, Kim SH, Zo YG, Kong Y, 2009. Molecular evolution of glutathione peroxidase genes in association with different biochemical properties of their encoded proteins in invertebrate animals. BMC Evol. Biol., 9: 72.
Carmel-Harel O, Storz G, 2000. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol., 54: 439-461.
Chen YI, Wei PC, Hsu JL, Su FY, Lee WH, 2016. NPGPx (GPx7): a novel oxidative stress sensor/transmitter with multiple roles in redox homeostasis. Am. J. Transl. Res., 8(4): 1626-1640.
Chu D, Zhang YJ, Brown JK, Cong B, Xu BY, Wu QJ, Zhu GR, 2006. The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Fla. Entomol., 89(2): 168-174.
Cossío-Bayúgar R, Miranda E, Holman PJ, 2005. Molecular cloning of a phospholipid hydroperoxide glutathione peroxidase gene from the tick, Boophilus microplus (Acari: Ixodidae). Insect Biochem. Molec. Biol., 35(12): 1378-1387.
De Barro PJ, Driver F, 1997. Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Austral. J. Entomol., 36: 149-152.
De Barro PJ, Liu SS, Boykin LM, Dinsdale AB, 2011. Bemisia tabaci: a statement of species status. Annu. Rev. Entomol., 56: 1-19.
Guo L, Huang XY, Liang YP, Liu XX, Chu D, 2018. Identification of cryptic species and detection of the susceptibility to cyantraniliprole and flupyradifurone of field populations of Bemisia tabaci (Hemiptera: Aleyrodidae) in Hainan, southern China. Acta Entomol. Sin., 61(2): 209-217. [郭磊, 黄新意, 梁延坡, 刘想想, 褚栋, 2018. 海南烟粉虱田间种群隐种鉴定及对溴氰虫酰胺和氟吡呋喃酮的敏感性检测. 昆虫学报, 61(2): 209-217]
Hermesz E, Ferencz á, 2009. Identification of two phospholipid hydroperoxide glutathione peroxidase (gpx4) genes in common carp. Comp. Biochem. Physiol. C, 150(1): 101-106.
Holland D, Ben-Hayyim G, Faltin Z, Camoin L, Strosberg AD, Eshdat Y, 1993. Molecular characterization of salt stress-associated protein in citrus: protein and cDNA sequence homology to mammalian glutathione peroxidases. Plant Mol. Biol., 21(5): 923-927.
Hu J, De Barro P, Zhao H, Wang J, Nardi F, Liu SS, 2011. An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE, 6(1): e16061.
Hu ZG, Lee KS, Choo YM, Yoon HJ, Kim I, Wei YD, Gui ZZ, Zhang GZ, Sohn HD, Jin BR, 2010. Molecular characterization of a phospholipid hydroperoxide glutathione peroxidase from the bumblebee Bombus ignitus. Comp. Biochem. Physiol. Part B, 155(1): 54-61.
Jiu M, Hu J, Wang LJ, Dong JF, Song YQ, Sun HZ, 2017. Cryptic species identification and composition of Bemisia tabaci (Hemiptera: Aleyrodidae) complex in Henan province, China. J. Insect Sci., 17(3): 78.
Jiu M, Li JM, Gao XL, Wang LJ, Wang XW, Liu SS, 2015. Identification and characterization of two phospholipid hydroperoxide glutathione peroxidase genes from the Mediterranean species of the whitefly Bemisia tabaci complex. Arch. Insect Biochem. Physiol., 89(1): 54-67.
Jiu M, Zhou XP, Tong L, Xu J, Yang X, Wan FH, Liu SS, 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE, 2(1): e182.
Li D, Blasevich F, Theopold U, Schmidt O, 2003. Possible function of two insect phospholipid-hydroperoxide glutathione peroxidases. J. Insect Physiol., 49(1): 1-9.
Li HR, Liu X, Liu XL, Li CY, Shen CP, Tao YL, Chu D, 2015. Widespread displacement of the exotic whitefly species Bemisia tabaci B by Bemisia tabaci Q in fields in Shandong, China. Acta Entomol. Sin., 58(7): 811-816. [李洪冉, 刘馨, 刘小龙, 李长友, 沈长朋, 陶云荔, 褚栋, 2015. 田间系统调查表明山东省农区烟粉虱优势种为Q隐种. 昆虫学报, 58(7): 811-816]
Li WJ, Feng H, Fan JH, Zhang RQ, Zhao NM, Liu JY, 2000. Molecular cloning and expression of a phospholipid hydroperoxide glutathione peroxidase homolog in Oryza sativa. Biochim. Biophys. Acta, 1493: 225-230.
Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, Wan FH, 2007. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science, 318(5857): 1769-1772.
Luo C, Yao Y, Wang RJ, Yan FM, Hu DX, Zhang ZL, 2002. The use of mitochondrial cytochrome oxidase I (mt COI) gene sequences for the identification of biotypes of Bemisia tabaci (Gennadius) in China. Acta Entomol. Sin., 45(6): 759-763. [罗晨, 姚远, 王戎疆, 闫凤鸣, 胡敦孝, 张芝利, 2002. 利用mtDNA COI基因序列鉴定我国烟粉虱的生物型. 昆虫学报, 45(6): 759-763]
Maiorino M, Roveri A, Ursini F, Gregolin C, 1985. Enzymatic determination of membrane lipid peroxidation. J. Free Radic. Biol. Med., 1(3): 203-207.
Mittapalli O, Neal JJ, Shukle RH, 2007. Antioxidant defense response in a galling insect. Proc. Natl. Acad. Sci. USA, 104(6): 1889-1894.
Pan HP, Chu D, Ge DQ, Wang SL, Wu QJ, Xie W, Jiao XG, Liu BM, Yang X, Yang N, Su Q, Xu BY, Zhang YJ, 2011. Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. J. Econ. Entomol., 104(3): 978-985.
Rao Q, Luo C, Zhang H, Guo X, Devine GJ, 2011. Distribution and dynamics of Bemisia tabaci invasive biotypes in central China. Bull. Entomol. Res., 101(1): 81-88.
Seth V, Banerjee BD, Bhattacharya A, Chakravorty AK, 2000. Lipid peroxidation, antioxidant enzymes, and glutathione redox system in blood of human poisoning with propoxur. Clin. Biochem., 33(8): 683-685.
Seth V, Banerjee BD, Chakravorty AK, 2001. Lipid peroxidation, free radical scavenging enzymes, and glutathione redox system in blood of rats exposed to propoxur. Pestic. Biochem. Physiol., 71: 133-139.
Sreenivasulu N, Miranda M, Prakash HS, Wobus U, Weschke W, 2004. Transcriptome changes in foxtail millet genotypes at high salinity: identification and characterization of a PHGPX gene specifically up-regulated by NaCl in a salt-tolerant line. J. Plant Physiol., 161(4): 467-477.
Sugimoto M, Furui S, Suzuki Y, 1997. Molecular cloning and characterization of a cDNA encoding putative phospholipid hydroperoxide glutathione peroxidase from spinach. Biosci. Biotechnol. Biochem., 61(8): 1379-1381.
Tian CB, Zhang GH, Li YY, Liu H, 2017. Identification of two putative phospholipid hydroperoxide glutathione peroxidase genes and the induction of three environmental stresses in Neoseiulus barkeri (Acari: Phytoseiidae). J. Asia-Pac. Entomol., 20(1): 261-267.
Ursini F, Maiorino M, Valente M, Ferri L, Gregolin C, 1982. Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides. Biochim. Biophys. Acta, 710(2): 197-211.
Wang M, Kang MJ, Guo XQ, Xu BH, 2010. Identification and characterization of two phospholipid hydroperoxide glutathione peroxidase genes from Apis cerana cerana. Comp. Biochem. Physiol. Part C, 152(1): 75-83.
Zhang Y, He Y, He L, Zong HY, Cai GB, 2015. Molecular cloning and characterization of a phospholipid hydroperoxide glutathione peroxidase gene from a blood fluke Schistosoma japonicum. Mol. Biochem. Parasitol., 203: 5-13.
Bae YA, Cai GB, Kim SH, Zo YG, Kong Y, 2009. Molecular evolution of glutathione peroxidase genes in association with different biochemical properties of their encoded proteins in invertebrate animals. BMC Evol. Biol., 9: 72.
Carmel-Harel O, Storz G, 2000. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol., 54: 439-461.
Chen YI, Wei PC, Hsu JL, Su FY, Lee WH, 2016. NPGPx (GPx7): a novel oxidative stress sensor/transmitter with multiple roles in redox homeostasis. Am. J. Transl. Res., 8(4): 1626-1640.
Chu D, Zhang YJ, Brown JK, Cong B, Xu BY, Wu QJ, Zhu GR, 2006. The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Fla. Entomol., 89(2): 168-174.
Cossío-Bayúgar R, Miranda E, Holman PJ, 2005. Molecular cloning of a phospholipid hydroperoxide glutathione peroxidase gene from the tick, Boophilus microplus (Acari: Ixodidae). Insect Biochem. Molec. Biol., 35(12): 1378-1387.
De Barro PJ, Driver F, 1997. Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Austral. J. Entomol., 36: 149-152.
De Barro PJ, Liu SS, Boykin LM, Dinsdale AB, 2011. Bemisia tabaci: a statement of species status. Annu. Rev. Entomol., 56: 1-19.
Guo L, Huang XY, Liang YP, Liu XX, Chu D, 2018. Identification of cryptic species and detection of the susceptibility to cyantraniliprole and flupyradifurone of field populations of Bemisia tabaci (Hemiptera: Aleyrodidae) in Hainan, southern China. Acta Entomol. Sin., 61(2): 209-217. [郭磊, 黄新意, 梁延坡, 刘想想, 褚栋, 2018. 海南烟粉虱田间种群隐种鉴定及对溴氰虫酰胺和氟吡呋喃酮的敏感性检测. 昆虫学报, 61(2): 209-217]
Hermesz E, Ferencz á, 2009. Identification of two phospholipid hydroperoxide glutathione peroxidase (gpx4) genes in common carp. Comp. Biochem. Physiol. C, 150(1): 101-106.
Holland D, Ben-Hayyim G, Faltin Z, Camoin L, Strosberg AD, Eshdat Y, 1993. Molecular characterization of salt stress-associated protein in citrus: protein and cDNA sequence homology to mammalian glutathione peroxidases. Plant Mol. Biol., 21(5): 923-927.
Hu J, De Barro P, Zhao H, Wang J, Nardi F, Liu SS, 2011. An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE, 6(1): e16061.
Hu ZG, Lee KS, Choo YM, Yoon HJ, Kim I, Wei YD, Gui ZZ, Zhang GZ, Sohn HD, Jin BR, 2010. Molecular characterization of a phospholipid hydroperoxide glutathione peroxidase from the bumblebee Bombus ignitus. Comp. Biochem. Physiol. Part B, 155(1): 54-61.
Jiu M, Hu J, Wang LJ, Dong JF, Song YQ, Sun HZ, 2017. Cryptic species identification and composition of Bemisia tabaci (Hemiptera: Aleyrodidae) complex in Henan province, China. J. Insect Sci., 17(3): 78.
Jiu M, Li JM, Gao XL, Wang LJ, Wang XW, Liu SS, 2015. Identification and characterization of two phospholipid hydroperoxide glutathione peroxidase genes from the Mediterranean species of the whitefly Bemisia tabaci complex. Arch. Insect Biochem. Physiol., 89(1): 54-67.
Jiu M, Zhou XP, Tong L, Xu J, Yang X, Wan FH, Liu SS, 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE, 2(1): e182.
Li D, Blasevich F, Theopold U, Schmidt O, 2003. Possible function of two insect phospholipid-hydroperoxide glutathione peroxidases. J. Insect Physiol., 49(1): 1-9.
Li HR, Liu X, Liu XL, Li CY, Shen CP, Tao YL, Chu D, 2015. Widespread displacement of the exotic whitefly species Bemisia tabaci B by Bemisia tabaci Q in fields in Shandong, China. Acta Entomol. Sin., 58(7): 811-816. [李洪冉, 刘馨, 刘小龙, 李长友, 沈长朋, 陶云荔, 褚栋, 2015. 田间系统调查表明山东省农区烟粉虱优势种为Q隐种. 昆虫学报, 58(7): 811-816]
Li WJ, Feng H, Fan JH, Zhang RQ, Zhao NM, Liu JY, 2000. Molecular cloning and expression of a phospholipid hydroperoxide glutathione peroxidase homolog in Oryza sativa. Biochim. Biophys. Acta, 1493: 225-230.
Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, Wan FH, 2007. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science, 318(5857): 1769-1772.
Luo C, Yao Y, Wang RJ, Yan FM, Hu DX, Zhang ZL, 2002. The use of mitochondrial cytochrome oxidase I (mt COI) gene sequences for the identification of biotypes of Bemisia tabaci (Gennadius) in China. Acta Entomol. Sin., 45(6): 759-763. [罗晨, 姚远, 王戎疆, 闫凤鸣, 胡敦孝, 张芝利, 2002. 利用mtDNA COI基因序列鉴定我国烟粉虱的生物型. 昆虫学报, 45(6): 759-763]
Maiorino M, Roveri A, Ursini F, Gregolin C, 1985. Enzymatic determination of membrane lipid peroxidation. J. Free Radic. Biol. Med., 1(3): 203-207.
Mittapalli O, Neal JJ, Shukle RH, 2007. Antioxidant defense response in a galling insect. Proc. Natl. Acad. Sci. USA, 104(6): 1889-1894.
Pan HP, Chu D, Ge DQ, Wang SL, Wu QJ, Xie W, Jiao XG, Liu BM, Yang X, Yang N, Su Q, Xu BY, Zhang YJ, 2011. Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. J. Econ. Entomol., 104(3): 978-985.
Rao Q, Luo C, Zhang H, Guo X, Devine GJ, 2011. Distribution and dynamics of Bemisia tabaci invasive biotypes in central China. Bull. Entomol. Res., 101(1): 81-88.
Seth V, Banerjee BD, Bhattacharya A, Chakravorty AK, 2000. Lipid peroxidation, antioxidant enzymes, and glutathione redox system in blood of human poisoning with propoxur. Clin. Biochem., 33(8): 683-685.
Seth V, Banerjee BD, Chakravorty AK, 2001. Lipid peroxidation, free radical scavenging enzymes, and glutathione redox system in blood of rats exposed to propoxur. Pestic. Biochem. Physiol., 71: 133-139.
Sreenivasulu N, Miranda M, Prakash HS, Wobus U, Weschke W, 2004. Transcriptome changes in foxtail millet genotypes at high salinity: identification and characterization of a PHGPX gene specifically up-regulated by NaCl in a salt-tolerant line. J. Plant Physiol., 161(4): 467-477.
Sugimoto M, Furui S, Suzuki Y, 1997. Molecular cloning and characterization of a cDNA encoding putative phospholipid hydroperoxide glutathione peroxidase from spinach. Biosci. Biotechnol. Biochem., 61(8): 1379-1381.
Tian CB, Zhang GH, Li YY, Liu H, 2017. Identification of two putative phospholipid hydroperoxide glutathione peroxidase genes and the induction of three environmental stresses in Neoseiulus barkeri (Acari: Phytoseiidae). J. Asia-Pac. Entomol., 20(1): 261-267.
Ursini F, Maiorino M, Valente M, Ferri L, Gregolin C, 1982. Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides. Biochim. Biophys. Acta, 710(2): 197-211.
Wang M, Kang MJ, Guo XQ, Xu BH, 2010. Identification and characterization of two phospholipid hydroperoxide glutathione peroxidase genes from Apis cerana cerana. Comp. Biochem. Physiol. Part C, 152(1): 75-83.
Zhang Y, He Y, He L, Zong HY, Cai GB, 2015. Molecular cloning and characterization of a phospholipid hydroperoxide glutathione peroxidase gene from a blood fluke Schistosoma japonicum. Mol. Biochem. Parasitol., 203: 5-13.