RNA-Seq揭示Foc4在外源氧化胁迫(H_2O_2)下的基因表达及细胞代谢变化
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摘要
尖孢镰刀菌古巴专化型4号小种(Fusarium oxysporum f. sp. cubense race 4,Foc4)是香蕉枯萎病的强致病性病原菌。Foc4在侵染香蕉植株早期必须面对寄主的活性氧迸发。【目的】了解Foc4应对外源氧化胁迫的分子机制。【方法】利用Illumina 2500 RNA-Seq测序平台分析了经外源氧化胁迫(H_2O_2)处理的Foc4与对照在转录组水平的基因表达差异。【结果】在外源氧化胁迫条件下,Foc4的生长受到抑制。转录组测序获得了超过2千万条clean reads。进一步的差异基因表达分析以差异倍数FC (fold change)≥2且FDA值≤0.001为选择标准,发现496个基因表达上调,298个基因表达下调。GO功能富集分析显示,429个基因比对到GO功能分析数据库,在这些差异表达基因中,许多与代谢过程、生物调节、细胞过程和刺激应答有关。KEGG通路富集分析显示,有141个表达差异显著基因比对到KEGG中的50条代谢途径。其中,主要是各类氨基酸代谢途径、脂肪酸代谢途径。同时也包括与抗氧化胁迫直接相关的代谢途径,包括DNA的损伤修复、类胡萝卜素的生物合成、过氧化物酶体、谷胱甘肽代谢等。【结论】这些结果暗示,为了在强氧化胁迫环境下生存,Foc4细胞从包括直接应对氧化胁迫的信号调控途径在内的物质代谢和能量代谢均发生改变以应对环境变化的胁迫。
Fusarium oxysporum f. sp. cubense race 4(Foc4), the strong virulent pathogen of Banana Fusarium Wilt, must face to oxidative burst produced by the host in the early stage of infecting banana plants. [Objective] To study the molecular mechanism how Foc4 responses exogenous oxidative stress, [Methods] RNA-Seq was done between the wild type B2 strain of Foc4 treated by H_2O_2 and the control using Illumina 2500 sequencing platform, and differentially expression genes(DEGs) was analyzed. [Results] The growth of Foc4 was inhibited under exogenous oxidative stress, and more than 20 million clean reads were obtained after RNA-Seq. Compared with the control, a total of 496 genes were up-regulated and 298 genes were down-regulated, respectively, with FDA value≤0.001 and Fold Change(FC)≥2 used as the selection criteria. Gene ontology(GO) functional enrichment analysis showed that 429 genes were annotated in the GO functional analysis database. Many of them were related to metabolic processes, biological regulation, cellular processes and response to stimuli. Kyoto encyclopedia of genes and genomes(KEGG) pathway enrichment analysis showed that 141 DEGs were annotated in 50 metabolic pathways in KEGG. These metabolic pathways mainly include the metabolic pathway of various amino acids and fatty acid. It also includes metabolic pathways that are directly related to antioxidant stress, including damage repair of DNA, biosynthesis of carotenoids, peroxisome and glutathione metabolism. [Conclusion] Material metabolism, energy metabolism and signal regulation pathways directly dealing with oxidative stress must be changed in Foc4 cells to cope with environmental stress and to survive in strong oxidative stress environment.
Fusarium oxysporum f. sp. cubense race 4(Foc4), the strong virulent pathogen of Banana Fusarium Wilt, must face to oxidative burst produced by the host in the early stage of infecting banana plants. [Objective] To study the molecular mechanism how Foc4 responses exogenous oxidative stress, [Methods] RNA-Seq was done between the wild type B2 strain of Foc4 treated by H_2O_2 and the control using Illumina 2500 sequencing platform, and differentially expression genes(DEGs) was analyzed. [Results] The growth of Foc4 was inhibited under exogenous oxidative stress, and more than 20 million clean reads were obtained after RNA-Seq. Compared with the control, a total of 496 genes were up-regulated and 298 genes were down-regulated, respectively, with FDA value≤0.001 and Fold Change(FC)≥2 used as the selection criteria. Gene ontology(GO) functional enrichment analysis showed that 429 genes were annotated in the GO functional analysis database. Many of them were related to metabolic processes, biological regulation, cellular processes and response to stimuli. Kyoto encyclopedia of genes and genomes(KEGG) pathway enrichment analysis showed that 141 DEGs were annotated in 50 metabolic pathways in KEGG. These metabolic pathways mainly include the metabolic pathway of various amino acids and fatty acid. It also includes metabolic pathways that are directly related to antioxidant stress, including damage repair of DNA, biosynthesis of carotenoids, peroxisome and glutathione metabolism. [Conclusion] Material metabolism, energy metabolism and signal regulation pathways directly dealing with oxidative stress must be changed in Foc4 cells to cope with environmental stress and to survive in strong oxidative stress environment.
引文
[1]Qi XZ,Guo LJ,Yang LY,Huang JS.Foatf1,a b ZIPtranscription factor of Fusarium oxysporum f.sp.cubense,is involved in pathogenesis by regulating the oxidative stress responses of Cavendish banana(Musa spp.).Physiological and Molecular Plant Pathology,2013,84:76-85.
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[3]Lamb C,Dixon RA.The oxidative burst in plant disease resistance.Annual Review of Plant Physiology and Plant Molecular Biology,1997,48:251-275.
[4]de Gara L,de Pinto MC,Tommasi F.The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction.Plant Physiology and Biochemistry,2003,41(10):863-870.
[5]Hückelhoven R,Kogel KH.Reactive oxygen intermediates in plant-microbe interactions:Who is who in powdery mildew resistance?Planta,2003,216(6):891-902.
[6]Orozco-Cárdenas ML,Narváez-Vásquez J,Ryan CA.Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding,systemin,and methyl jasmonate.The Plant Cell,2001,13(1):179-191.
[7]Wagner AM.A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells.FEBS Letters,1995,368(2):339-342.
[8]Nafie E,Hathout T,Mokadem AS Al.Jasmonic acid elicits oxidative defense and detoxification systems in Cucumis melo L.cells.Brazilian Journal of Plant Physiology,2011,23(2):161-174.
[9]Peroni LA,Ferreira RR,Figueira A,Machado MA,Stach-Machado DR.Expression profile of oxidative and antioxidative stress enzymes based on ESTs approach of citrus.Genetics and Molecular Biology,2007,30(3):872-880.
[10]Ahammed GJ,Yuan HL,Ogweno JO,Zhou YH,Xia XJ,Mao WH,Shi K,Yu JQ.Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato.Chemosphere,2012,86(5):546-555.
[11]Gupta AS,Heinen JL,Holaday AS,Burke JJ,Allen RD.Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase.Proceedings of the National Academy of Sciences of the United States of America,1993,90(4):1629-1633.
[12]Yoshioka H,Numata N,Nakajima K,Katou S,Kawakita K,Rowland Q,Jones JDG,Doke N.Nicotiana benthamiana gp91phox Homologs Nbrboh A and Nbrboh B participate in H2O2accumulation and resistance to Phytophthora infestans.Plant Cell,2003,15(3):706-718.
[13]Guo M,Chen Y,Du Y,Dong Y H,Guo W,Zhai S,Zhang HF,Dong SM,Zhang ZG,Wang YC,Wang P,Zheng XB.The b ZIP transcription factor Mo AP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae.PLo S Pathogens,2011,7(2):e1001302.
[14]Kavitha S,Chandra TS.Oxidative stress protection and glutathione metabolism in response to hydrogen peroxide and menadione in riboflavinogenic fungus Ashbya gossypii.Applied Biochemistry and Biotechnology,2014,174(6):2307-2325.
[15]Walther A,Wendland J.Yap1-dependent oxidative stress response provides a link to riboflavin production in Ashbya gossypii.Fungal Genetics and Biology,2012,49(9):697-707.
[16]Qian W,Jia YT,Ren SX,He YQ,Feng JX,Lu LF,Sun QH,Ying G,Tang DJ,Tang H,Wu W,Hao P,Wang LF,Jiang BL,Zeng SY,Gu WY,Lu G,Rong L,Tian YC,Yao ZJ,Fu G,Chen BS,Fang RX,Qiang BQ,Chen Z,Zhao GP,Tang JL,He CU.Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv.campestris.Genome Research,2005,15(6):757-767.
[17]Wang ZX,Zhou XZ,Meng HM,Liu YJ,Zhou Q,Huang B.Comparative transcriptomic analysis of the heat stress response in the filamentous fungus Metarhizium anisopliae using RNA-Seq.Applied Microbiology and Biotechnology,2014,98(12):5589-5597.
[18]Rokas A,Gibbons JG,Zhou XF,Beauvais A,LatgéJP.The diverse applications of RNA-seq for functional genomic studies in Aspergillus fumigatus.Annals of the New York Academy of Sciences,2012,1273(1):25-34.
[19]Ries L,Pullan ST,Delmas S,Malla S,Blythe MJ,Archer DB.Genome-wide transcriptional response of Trichoderma reesei to lignocellulose using RNA sequencing and comparison with Aspergillus niger.BMC Genomics,2013,14:541.
[20]Soanes DM,Chakrabarti A,Paszkiewicz KH,Dawe AL,Talbot NJ.Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae.PLo S Pathogens,2012,8(2):e1002514.
[21]Grabherr MG,Haas BJ,Yassour M,Levin JZ,Thompson DA,Amit I,Adiconis X,Fan L,Raychowdhury R,Zeng QD,Chen ZH,Mauceli E,Hacohen N,Gnirke A,Rhind N,di Palma F,Birren BW,Nusbaum C,Lindblad-Toh K,Friedman N,Regev A.Full-length transcriptome assembly from RNA-Seq data without a reference genome.Nature Biotechnology,2011,29(7):644-652.
[22]Li B,Dewey CN.RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome.BMC Bioinformatics,2011,12:323.
[23]Young MD,Wakefield MJ,Smyth GK,Oshlack A.Gene ontology analysis for RNA-seq:accounting for selection bias.Genome Biology,2010,11(2):R14.
[24]Kanehisa M,Araki M,Goto S,Hattori M,Hirakawa M,Itoh M,Katayama T,Kawashima S,Okuda S,Tokimatsu T,Yamanishi Y.KEGG for linking genomes to life and the environment.Nucleic Acids Research,2008,36(S1):D480-D484.
[25]Mao XZ,Cai T,Olyarchuk JG,Wei LP.Automated genome annotation and pathway identification using the KEGGOrthology(KO)as a controlled vocabulary.Bioinformatics,2005,21(19):3787-3793.
[26]Skamnioti P,Henderson C,Zhang ZG,Robinson Z,Gurr SJ.A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea.Molecular Plant-Microbe Interactions,2007,20(5):568-580.
[27]Mc Kersie BD.Oxidative stress.http://www.plantstress.com/articles/oxidative%20stress.htm.2018-09-14.
[28]Isabelle M,Moreel X,GagnéJP,Rouleau M,Ethier C,GagnéP,Hendzel MJ,Poirier GG.Investigation of PARP-1,PARP-2,and PARG interactomes by affinity-purification mass spectrometry.Proteome Science,2010,8:22.
[29]Olsen LC,Aasland R,Wittwer CU,Krokan HE,Helland DE.Molecular cloning of human uracil-DNA glycosylase,a highly conserved DNA repair enzyme.The EMBO Journal,1989,8(10):3121-3125.
[30]Serre L,de Jésus KP,Boiteux S,Zelwer C,Castaing B.Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analogue-containing DNA.The EMBO Journal,2002,21(12):2854-2865.
[31]Burkovics P,Szukacsov V,Unk I,Haracska L.Human Ape2protein has a 3?-5?exonuclease activity that acts preferentially on mismatched base pairs.Nucleic Acids Research,2006,34(9):2508-2515.
[32]Ullah A,Chandrasekaran G,Brul S,Smits GJ.Yeast adaptation to weak acids prevents futile energy expenditure.Frontiers in Microbiology,2013,4:142.
[33]Coleman RA,Lewin TM,Muoio DM.Physiological and nutritional regulation of enzymes of triacylglycerol synthesis.Annual Review of Nutrition,2000,20:77-103.
[34]Harding HP,Zhang YH,Zeng H,Novoa I,Lu PD,Calfon M,Sadri N,Yun C,Popko B,Paules R,Stojdl DF,Bell JC,Hettmann T,Leiden JM,Ron D.An integrated stress response regulates amino acid metabolism and resistance to oxidative stress.Molecular Cell,2003,11(3):619-633.
[35]Lupo S,Aranda C,Olivera H,Riego L,González A,Miranda-Ham L,Servin L.Tyrosine is involved in protection from oxidative stress in Saccharomyces cerevisiae.Canadian Journal of Microbiology,1997,43(10):963-970.
[36]Fitzpatrick AM,Park Y,Brown LAS,Jones DP.Children with severe asthma have unique oxidative stress-associated metabolomic profiles.Journal of Allergy and Clinical Immunology,2014,133(1):258-261.e8.
[37]Lu JP,Cao HJ,Zhang LL,Huang PY,Lin FC.Systematic analysis of Zn2Cys6 transcription factors required for development and pathogenicity by High-throughput gene knockout in the rice blast fungus.PLo S Pathogens,2014,10(10):e1004432.
[38]Cummins I,Cole DJ,Edwards R.A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass.The Plant Journal,1999,18(3):285-292.
[39]Kobayashi M,Kakizono T,Naga S.Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga,Haematococcus pluvialis.Applied Environmental Microbiology,1993,59(3):867-873.
[40]Hartmann A,Hurek T.Effect of carotenoid overproduction on oxygen tolerance of nitrogen fixation in Azospirillum brasilense Sp7.Microbiology,1988,134(9):2449-2455.
[41]Singh S,Brocker C,Koppaka V,Chen Y,Jackson BC,Matsumoto A,Thompson DC,Vasiliou V.Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress.Free Radical Biology and Medicine,2013,56:89-101.
[42]Ohsawa I,Nishimaki K,Yasuda C,Kamino K,Ohta S.Deficiency in a mitochondrial aldehyde dehydrogenase increases vulnerability to oxidative stress in PC12 cells.Journal of Neurochemistry,2003,84(5):1110-1117.
[43]White WH,Skatrud PL,Xue ZX,Toyn JH.Specialization of function among aldehyde dehydrogenases:the ALD2 and ALD3 genes are required forβ-alanine biosynthesis in Saccharomyces cerevisiae.Genetics,2003,163(1):69-77.
[44]El Golli-Bennour E,Bach H.Hsp70 expression as biomarkers of oxidative stress:mycotoxins'exploration.Toxicology,2011,287(1/3):1-7.
[45]Ilbert M,Horst J,Ahrens S,Winter J,Graf PCF,Lilie H,Jakob U.The redox-switch domain of Hsp33 functions as dual stress sensor.Nature Structural&Molecular Biology,2007,14(6):556-563.
[2]Chung KR.Stress response and pathogenicity of the necrotrophic fungal pathogen Alternaria alternata.Scientifica,2012,2012:635431.
[3]Lamb C,Dixon RA.The oxidative burst in plant disease resistance.Annual Review of Plant Physiology and Plant Molecular Biology,1997,48:251-275.
[4]de Gara L,de Pinto MC,Tommasi F.The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction.Plant Physiology and Biochemistry,2003,41(10):863-870.
[5]Hückelhoven R,Kogel KH.Reactive oxygen intermediates in plant-microbe interactions:Who is who in powdery mildew resistance?Planta,2003,216(6):891-902.
[6]Orozco-Cárdenas ML,Narváez-Vásquez J,Ryan CA.Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding,systemin,and methyl jasmonate.The Plant Cell,2001,13(1):179-191.
[7]Wagner AM.A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells.FEBS Letters,1995,368(2):339-342.
[8]Nafie E,Hathout T,Mokadem AS Al.Jasmonic acid elicits oxidative defense and detoxification systems in Cucumis melo L.cells.Brazilian Journal of Plant Physiology,2011,23(2):161-174.
[9]Peroni LA,Ferreira RR,Figueira A,Machado MA,Stach-Machado DR.Expression profile of oxidative and antioxidative stress enzymes based on ESTs approach of citrus.Genetics and Molecular Biology,2007,30(3):872-880.
[10]Ahammed GJ,Yuan HL,Ogweno JO,Zhou YH,Xia XJ,Mao WH,Shi K,Yu JQ.Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato.Chemosphere,2012,86(5):546-555.
[11]Gupta AS,Heinen JL,Holaday AS,Burke JJ,Allen RD.Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase.Proceedings of the National Academy of Sciences of the United States of America,1993,90(4):1629-1633.
[12]Yoshioka H,Numata N,Nakajima K,Katou S,Kawakita K,Rowland Q,Jones JDG,Doke N.Nicotiana benthamiana gp91phox Homologs Nbrboh A and Nbrboh B participate in H2O2accumulation and resistance to Phytophthora infestans.Plant Cell,2003,15(3):706-718.
[13]Guo M,Chen Y,Du Y,Dong Y H,Guo W,Zhai S,Zhang HF,Dong SM,Zhang ZG,Wang YC,Wang P,Zheng XB.The b ZIP transcription factor Mo AP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae.PLo S Pathogens,2011,7(2):e1001302.
[14]Kavitha S,Chandra TS.Oxidative stress protection and glutathione metabolism in response to hydrogen peroxide and menadione in riboflavinogenic fungus Ashbya gossypii.Applied Biochemistry and Biotechnology,2014,174(6):2307-2325.
[15]Walther A,Wendland J.Yap1-dependent oxidative stress response provides a link to riboflavin production in Ashbya gossypii.Fungal Genetics and Biology,2012,49(9):697-707.
[16]Qian W,Jia YT,Ren SX,He YQ,Feng JX,Lu LF,Sun QH,Ying G,Tang DJ,Tang H,Wu W,Hao P,Wang LF,Jiang BL,Zeng SY,Gu WY,Lu G,Rong L,Tian YC,Yao ZJ,Fu G,Chen BS,Fang RX,Qiang BQ,Chen Z,Zhao GP,Tang JL,He CU.Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv.campestris.Genome Research,2005,15(6):757-767.
[17]Wang ZX,Zhou XZ,Meng HM,Liu YJ,Zhou Q,Huang B.Comparative transcriptomic analysis of the heat stress response in the filamentous fungus Metarhizium anisopliae using RNA-Seq.Applied Microbiology and Biotechnology,2014,98(12):5589-5597.
[18]Rokas A,Gibbons JG,Zhou XF,Beauvais A,LatgéJP.The diverse applications of RNA-seq for functional genomic studies in Aspergillus fumigatus.Annals of the New York Academy of Sciences,2012,1273(1):25-34.
[19]Ries L,Pullan ST,Delmas S,Malla S,Blythe MJ,Archer DB.Genome-wide transcriptional response of Trichoderma reesei to lignocellulose using RNA sequencing and comparison with Aspergillus niger.BMC Genomics,2013,14:541.
[20]Soanes DM,Chakrabarti A,Paszkiewicz KH,Dawe AL,Talbot NJ.Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae.PLo S Pathogens,2012,8(2):e1002514.
[21]Grabherr MG,Haas BJ,Yassour M,Levin JZ,Thompson DA,Amit I,Adiconis X,Fan L,Raychowdhury R,Zeng QD,Chen ZH,Mauceli E,Hacohen N,Gnirke A,Rhind N,di Palma F,Birren BW,Nusbaum C,Lindblad-Toh K,Friedman N,Regev A.Full-length transcriptome assembly from RNA-Seq data without a reference genome.Nature Biotechnology,2011,29(7):644-652.
[22]Li B,Dewey CN.RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome.BMC Bioinformatics,2011,12:323.
[23]Young MD,Wakefield MJ,Smyth GK,Oshlack A.Gene ontology analysis for RNA-seq:accounting for selection bias.Genome Biology,2010,11(2):R14.
[24]Kanehisa M,Araki M,Goto S,Hattori M,Hirakawa M,Itoh M,Katayama T,Kawashima S,Okuda S,Tokimatsu T,Yamanishi Y.KEGG for linking genomes to life and the environment.Nucleic Acids Research,2008,36(S1):D480-D484.
[25]Mao XZ,Cai T,Olyarchuk JG,Wei LP.Automated genome annotation and pathway identification using the KEGGOrthology(KO)as a controlled vocabulary.Bioinformatics,2005,21(19):3787-3793.
[26]Skamnioti P,Henderson C,Zhang ZG,Robinson Z,Gurr SJ.A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea.Molecular Plant-Microbe Interactions,2007,20(5):568-580.
[27]Mc Kersie BD.Oxidative stress.http://www.plantstress.com/articles/oxidative%20stress.htm.2018-09-14.
[28]Isabelle M,Moreel X,GagnéJP,Rouleau M,Ethier C,GagnéP,Hendzel MJ,Poirier GG.Investigation of PARP-1,PARP-2,and PARG interactomes by affinity-purification mass spectrometry.Proteome Science,2010,8:22.
[29]Olsen LC,Aasland R,Wittwer CU,Krokan HE,Helland DE.Molecular cloning of human uracil-DNA glycosylase,a highly conserved DNA repair enzyme.The EMBO Journal,1989,8(10):3121-3125.
[30]Serre L,de Jésus KP,Boiteux S,Zelwer C,Castaing B.Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analogue-containing DNA.The EMBO Journal,2002,21(12):2854-2865.
[31]Burkovics P,Szukacsov V,Unk I,Haracska L.Human Ape2protein has a 3?-5?exonuclease activity that acts preferentially on mismatched base pairs.Nucleic Acids Research,2006,34(9):2508-2515.
[32]Ullah A,Chandrasekaran G,Brul S,Smits GJ.Yeast adaptation to weak acids prevents futile energy expenditure.Frontiers in Microbiology,2013,4:142.
[33]Coleman RA,Lewin TM,Muoio DM.Physiological and nutritional regulation of enzymes of triacylglycerol synthesis.Annual Review of Nutrition,2000,20:77-103.
[34]Harding HP,Zhang YH,Zeng H,Novoa I,Lu PD,Calfon M,Sadri N,Yun C,Popko B,Paules R,Stojdl DF,Bell JC,Hettmann T,Leiden JM,Ron D.An integrated stress response regulates amino acid metabolism and resistance to oxidative stress.Molecular Cell,2003,11(3):619-633.
[35]Lupo S,Aranda C,Olivera H,Riego L,González A,Miranda-Ham L,Servin L.Tyrosine is involved in protection from oxidative stress in Saccharomyces cerevisiae.Canadian Journal of Microbiology,1997,43(10):963-970.
[36]Fitzpatrick AM,Park Y,Brown LAS,Jones DP.Children with severe asthma have unique oxidative stress-associated metabolomic profiles.Journal of Allergy and Clinical Immunology,2014,133(1):258-261.e8.
[37]Lu JP,Cao HJ,Zhang LL,Huang PY,Lin FC.Systematic analysis of Zn2Cys6 transcription factors required for development and pathogenicity by High-throughput gene knockout in the rice blast fungus.PLo S Pathogens,2014,10(10):e1004432.
[38]Cummins I,Cole DJ,Edwards R.A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass.The Plant Journal,1999,18(3):285-292.
[39]Kobayashi M,Kakizono T,Naga S.Enhanced carotenoid biosynthesis by oxidative stress in acetate-induced cyst cells of a green unicellular alga,Haematococcus pluvialis.Applied Environmental Microbiology,1993,59(3):867-873.
[40]Hartmann A,Hurek T.Effect of carotenoid overproduction on oxygen tolerance of nitrogen fixation in Azospirillum brasilense Sp7.Microbiology,1988,134(9):2449-2455.
[41]Singh S,Brocker C,Koppaka V,Chen Y,Jackson BC,Matsumoto A,Thompson DC,Vasiliou V.Aldehyde dehydrogenases in cellular responses to oxidative/electrophilicstress.Free Radical Biology and Medicine,2013,56:89-101.
[42]Ohsawa I,Nishimaki K,Yasuda C,Kamino K,Ohta S.Deficiency in a mitochondrial aldehyde dehydrogenase increases vulnerability to oxidative stress in PC12 cells.Journal of Neurochemistry,2003,84(5):1110-1117.
[43]White WH,Skatrud PL,Xue ZX,Toyn JH.Specialization of function among aldehyde dehydrogenases:the ALD2 and ALD3 genes are required forβ-alanine biosynthesis in Saccharomyces cerevisiae.Genetics,2003,163(1):69-77.
[44]El Golli-Bennour E,Bach H.Hsp70 expression as biomarkers of oxidative stress:mycotoxins'exploration.Toxicology,2011,287(1/3):1-7.
[45]Ilbert M,Horst J,Ahrens S,Winter J,Graf PCF,Lilie H,Jakob U.The redox-switch domain of Hsp33 functions as dual stress sensor.Nature Structural&Molecular Biology,2007,14(6):556-563.