Comparative transcriptome analysis reveals differential gene expression in resistant and susceptible tobacco cultivars in response to infection by cucumber mosaic virus
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摘要
Cucumber mosaic virus(CMV) is one of the most severe viral diseases transmitted by aphids infecting Solanum crops in China, causing great losses of crop yields and income in rural communities.The tobacco cultivars NC82 and Taiyan 8 are closely related but differ in resistance to CMV.NC82 is susceptible to infection and Taiyan 8 is resistant, but the mechanisms underlying this difference in resistance are not clear.In this study, we conducted RNA sequencing to analyze changes in gene expression induced in the leaves of Taiyan 8 and NC82 upon systemic infection with CMV, compared with gene expression in the leaves of mock-inoculated plants.Leaves were sampled at one, three, eight, and 15 days after infection.In total, 3443 and 747 differentially expressed genes were identified in Taiyan 8 and NC82, respectively.Gene ontology and pathway enrichment analyses revealed that the different responses to CMV infection between cultivars were based on microtubulebased processes, pentose and glucuronate interconversions, plant–pathogen interaction,and hormone signal transduction pathways.Genes encoding pathogenesis-related proteins, disease-resistance proteins, lipoxygenase, cellulose synthase, an auxin response factor, and an ethylene receptor showed different expression patterns.The differences in gene expression following CMV infection likely contributed to the different resistance levels of these two tobacco cultivars.The comprehensive transcriptome dataset described here,which includes candidate response genes, will serve as a resource for further studies of the molecular mechanisms associated with tobacco defense responses against CMV.
Cucumber mosaic virus(CMV) is one of the most severe viral diseases transmitted by aphids infecting Solanum crops in China, causing great losses of crop yields and income in rural communities.The tobacco cultivars NC82 and Taiyan 8 are closely related but differ in resistance to CMV.NC82 is susceptible to infection and Taiyan 8 is resistant, but the mechanisms underlying this difference in resistance are not clear.In this study, we conducted RNA sequencing to analyze changes in gene expression induced in the leaves of Taiyan 8 and NC82 upon systemic infection with CMV, compared with gene expression in the leaves of mock-inoculated plants.Leaves were sampled at one, three, eight, and 15 days after infection.In total, 3443 and 747 differentially expressed genes were identified in Taiyan 8 and NC82, respectively.Gene ontology and pathway enrichment analyses revealed that the different responses to CMV infection between cultivars were based on microtubulebased processes, pentose and glucuronate interconversions, plant–pathogen interaction,and hormone signal transduction pathways.Genes encoding pathogenesis-related proteins, disease-resistance proteins, lipoxygenase, cellulose synthase, an auxin response factor, and an ethylene receptor showed different expression patterns.The differences in gene expression following CMV infection likely contributed to the different resistance levels of these two tobacco cultivars.The comprehensive transcriptome dataset described here,which includes candidate response genes, will serve as a resource for further studies of the molecular mechanisms associated with tobacco defense responses against CMV.
Cucumber mosaic virus(CMV) is one of the most severe viral diseases transmitted by aphids infecting Solanum crops in China, causing great losses of crop yields and income in rural communities.The tobacco cultivars NC82 and Taiyan 8 are closely related but differ in resistance to CMV.NC82 is susceptible to infection and Taiyan 8 is resistant, but the mechanisms underlying this difference in resistance are not clear.In this study, we conducted RNA sequencing to analyze changes in gene expression induced in the leaves of Taiyan 8 and NC82 upon systemic infection with CMV, compared with gene expression in the leaves of mock-inoculated plants.Leaves were sampled at one, three, eight, and 15 days after infection.In total, 3443 and 747 differentially expressed genes were identified in Taiyan 8 and NC82, respectively.Gene ontology and pathway enrichment analyses revealed that the different responses to CMV infection between cultivars were based on microtubulebased processes, pentose and glucuronate interconversions, plant–pathogen interaction,and hormone signal transduction pathways.Genes encoding pathogenesis-related proteins, disease-resistance proteins, lipoxygenase, cellulose synthase, an auxin response factor, and an ethylene receptor showed different expression patterns.The differences in gene expression following CMV infection likely contributed to the different resistance levels of these two tobacco cultivars.The comprehensive transcriptome dataset described here,which includes candidate response genes, will serve as a resource for further studies of the molecular mechanisms associated with tobacco defense responses against CMV.
引文
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[13]J.Lu,Z.X.Du,J.Kong,L.N.Chen,Y.H.Qiu,G.F.Li,X.H.Meng,S.F.Zhu,Transcriptome analysis of Nicotiana tabacum infected by Cucumber mosaic virus during systemic symptom development,PLoS One 7(2012),e43447..
[14]L.Chen,C.Fei,L.Zhu,Z.Xu,W.Zou,T.Yang,H.Lin,D.Xi,RNA-seq approach to analysis of gene expression profiles in dark green islands and light green tissues of Cucumber mosaic virus-infected Nicotiana tabacum,PLoS One 12(2017),e0175391..
[15]S.Duan,X.Ma,W.Chen,W.Wan,Y.He,X.Ma,Y.Ma,N.Long,Y.Tan,Y.Wang,Y.Hou,Y.Dong,Transcriptomic profile of tobacco in response to Alternaria longipes and Alternaria alternata infections,Sci.Rep.6(2016)25635.
[16]J.K.Yang,Z.J.Tong,D.H.Fang,X.J.Chen,K.Q.Zhang,B.G.Xiao,Transcriptomic profile of tobacco in response to Phytophthora nicotianae infection,Sci.Rep.7(2017)401.
[17]X.Chen,S.Dai,X.Zhang,C.Jiang,M.Ren,L.Cheng,X.Fu,Y.Wang,Z.Zhang,A.Yang,Mixed major-gene plus polygenes inheritance analysis for CMV disease resistance in flue-cured tobacco,J.Plant Genet.Resour.15(2014)1278-1286.
[18]K.Wen,Z.Zhang,M.Ren,C.Jiang,L.Shen,L.Cheng,R.Geng,X.Chen,L.Feng,A.Yang,QTL analysis of the resistance gene to CMV in flue-cured tobacco,Chin.Tobacco Sci.34(2013)55-59(in Chinese with English abstract).
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[21]A.Conesa,S.G?tz,J.M.García-Gómez,J.Terol,M.Talón,M.Robles,Blast2GO:a universal tool for annotation,visualization and analysis in functional genomics research,Bioinformatics 21(2005)3674-3676.
[22]B.Li,C.N.Dewey,RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome,BMC Bioinforma.12(2011)323.
[23]S.Anders,W.Huber,Differential expression analysis for sequence count data,Genome Biol.11(2010)R106.
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[25]M.Kanehisa,M.Araki,S.Goto,M.Hattori,M.Hirakawa,M.Itoh,T.Katayama,S.Kawashima,S.Okuda,T.Tokimatsu,KEGG for linking genomes to life and the environment,Nucleic Acids Res.36(2008)D480-D484.
[26]J.Wu,X.Mao,T.Cai,J.Luo,L.Wei,KOBAS server:a webbased platform for automated annotation and pathway identification,Nucleic Acids Res.34(2006)720-724.
[27]T.D.Schmittgen,K.J.Livak,Analyzing real-time PCR data by the comparative CT method,Nat.Protoc.3(2008)1101-1108.
[28]N.Sierro,J.N.Battey,S.Ouadi,N.Bakaher,L.Bovet,A.Willig,S.Goepfert,M.C.Peitsch,N.V.Ivanov,The tobacco genome sequence and its comparison with those of tomato and potato,Nat.Commun.5(2014)3833.
[29]D.Takemoto,D.A.Jones,A.R.Hardham,GFP-tagging of cell components reveals the dynamics of subcellular reorganization in response to infection of Arabidopsis by oomycete pathogens,Plant J.33(2003)775-792.
[30]D.Takemoto,A.R.Hardham,The cytoskeleton as a regulator and target of biotic interactions in plants,Plant Physiol.136(2004)3864-3876.
[31]C.Geng,Q.Q.Cong,X.D.Li,A.L.Mou,R.Gao,J.L.Liu,Y.P.Tian,Developmentally regulated plasma membrane protein of Nicotiana benthamiana contributes to potyvirus movement and transports to plasmodesmata via the early secretory pathway and the actomyosin system,Plant Physiol.167(2015)394-410.
[32]M.Heinlein,The spread of Tobacco mosaic virus infection:insights into the cellular mechanism of RNA transport,Cell.Mol.Life Sci.59(2002)58-82.
[33]V.Boyko,J.Ferralli,J.Ashby,P.Schellenbaum,M.Heinlein,Function of microtubules in intercellular transport of plant virus RNA,Nat.Cell Biol.2(2000)826-832.
[34]Z.Zhang,Y.Xu,Z.Xie,X.Li,Z.H.He,X.X.Peng,Association-dissociation of glycolate oxidase with catalase in rice:a potential switch to modulate intracellular H2O2levels,Mol.Plant 9(2016)737-748.
[35]K.H.Caffall,D.Mohnen,The structure,function,and biosynthesis of plant cell wall pectic polysaccharides,Carbohydr.Res.344(2009)1879-1900.
[36]A.Giovane,C.Balestrieri,L.Quagliuolo,D.Castaldo,L.Servillo,A glycoprotein inhibitor of pectin methylesterase in kiwi fruit.Purification by affinity chromatography and evidence of a ripening-related precursor,Eur.J.Biochem.233(1995)926-929.
[37]D.Douchkov,S.Lueck,G.Hensel,J.Kumlehn,J.Rajaraman,A.Johrde,M.S.Doblin,C.T.Beahan,M.Kopischke,R.Fuchs,The barley(Hordeum vulgare)cellulose synthase-like D2 gene(HvCslD2)mediates penetration resistance to host-adapted and nonhost isolates of the powdery mildew fungus,New Phytol.212(2016)421-433.
[38]J.D.Jones,J.L.Dangl,The plant immune system,Nature444(2006)323-329.
[39]J.E.Parker,M.J.Coleman,V.Szabo,L.N.Frost,R.Schmidt,E.van der Biezen,T.Moores,C.Dean,M.Daniels,J.D.Jones,The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1receptors with N and L6,Plant Cell 9(1997)879-894.
[40]E.van der Biezen,J.Sun,M.J.Coleman,M.J.Bibb,J.D.Jones,Arabidopsis RelA/SpoT homologs implicate(p)ppGpp in plant signaling,Proc.Natl.Acad.Sci.U.S.A.97(2000)3747-3752.
[41]I.S.Hwang,B.K.Hwang,The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens,Plant Physiol.152(2010)948-967.
[42]M.Alazem,N.S.Lin,Roles of plant hormones in the regulation of host-virus interactions,Mol.Plant Pathol.16(2015)529-540.
[43]C.M.J.Pieterse,A.Leon-Reyes,S.van der Ent,S.C.M.van Wees,Networking by small-molecule hormones in plant immunity,Nat.Chem.Biol.5(2009)308-316.
[44]M.S.Padmanabhan,S.R.Kramer,X.Wang,J.N.Culver,Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions:reprogramming the auxin response pathway to enhance virus infection,J.Virol.82(2008)2477-2485.
[45]S.Marco,D.Levy,Involvement of ethylene in the development of Cucumber mosaic virus-induced chlorotic lesions in cucumber cotyledons,Physiol.Plant Pathol.14(1979)235-244.
[46]L.Chen,L.Zhang,D.Li,F.Wang,D.Yu,WRKY8transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.110(2013)E1963-E1971.
[47]Y.Zhang,Y.T.Cheng,N.Qu,Q.Zhao,D.Bi,X.Li,Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs,Plant J.48(2006)647-656.
[2]Y.Wei,F.Wang,Y.Qian,Interaction between host plants and cucumber mosaic virus,Plant Prot.31(2005)15-18(in Chinese with English abstract).
[3]B.J.Deyoung,R.W.Innes,Plant NBS-LRR proteins in pathogen sensing and host defense,Nat.Immunol.7(2006)1243-1249.
[4]S.T.Chisholm,G.Coaker,B.Day,B.J.Staskawicz,Hostmicrobe interactions:shaping the evolution of the plant immune response,Cell 124(2006)803-814.
[5]H.Takahashi,N.Goto,Y.Ehara,Hypersensitive response in cucumber mosaic virus-inoculated Arabidopsis thaliana,Plant J.6(1994)369-377.
[6]H.Takahashi,J.Miller,Y.Nozaki,Sukamto,M.Takeda,J.Shah,H.Shu,M.Ikegami,Y.Ehara,S.P.Dinesh-Kumar,RCY1,an Arabidopsis thaliana RPP8/HRT family resistance gene,conferring resistance to cucumber mosaic virus requires salicylic acid,ethylene and a novel signal transduction mechanism,Plant J.32(2002)655-667.
[7]Y.S.Seo,M.R.Rojas,J.Y.Lee,S.W.Lee,J.S.Jeon,P.Ronald,W.J.Lucas,R.L.Gilbertson,A viral resistance gene from common bean functions across plant families and is upregulated in a non-virus-specific manner,Proc.Natl.Acad.Sci.U.S.A.103(2006)11856-11861.
[8]J.L.M.Soosaar,T.M.Burchsmith,S.P.Dineshkumar,Mechanisms of plant resistance to viruses,Nat.Rev.Microbiol.3(2005)789-798.
[9]P.Ahlquist,RNA-dependent RNA polymerases,viruses and RNA silencing,Science 296(2002)1270-1273.
[10]P.Mourrain,C.Béclin,T.Elmayan,F.Feuerbach,C.Godon,J.B.Morel,D.Jouette,A.M.Lacombe,S.Nikic,N.Picault,Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance,Cell 101(2000)533-542.
[11]R.Marathe,Z.Guan,R.Anandalakshmi,H.Zhao,S.Dinesh-Kumar,Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray,Plant Mol.Biol.55(2004)501-520.
[12]H.Choi,Y.Jo,S.Lian,K.M.Jo,H.Chu,J.Y.Yoon,S.K.Choi,K.H.Kim,W.K.Cho,Comparative analysis of chrysanthemum transcriptome in response to three RNA viruses:cucumber mosaic virus,Tomato spotted wilt virus and Potato virus X,Plant Mol.Biol.88(2015)233-248.
[13]J.Lu,Z.X.Du,J.Kong,L.N.Chen,Y.H.Qiu,G.F.Li,X.H.Meng,S.F.Zhu,Transcriptome analysis of Nicotiana tabacum infected by Cucumber mosaic virus during systemic symptom development,PLoS One 7(2012),e43447..
[14]L.Chen,C.Fei,L.Zhu,Z.Xu,W.Zou,T.Yang,H.Lin,D.Xi,RNA-seq approach to analysis of gene expression profiles in dark green islands and light green tissues of Cucumber mosaic virus-infected Nicotiana tabacum,PLoS One 12(2017),e0175391..
[15]S.Duan,X.Ma,W.Chen,W.Wan,Y.He,X.Ma,Y.Ma,N.Long,Y.Tan,Y.Wang,Y.Hou,Y.Dong,Transcriptomic profile of tobacco in response to Alternaria longipes and Alternaria alternata infections,Sci.Rep.6(2016)25635.
[16]J.K.Yang,Z.J.Tong,D.H.Fang,X.J.Chen,K.Q.Zhang,B.G.Xiao,Transcriptomic profile of tobacco in response to Phytophthora nicotianae infection,Sci.Rep.7(2017)401.
[17]X.Chen,S.Dai,X.Zhang,C.Jiang,M.Ren,L.Cheng,X.Fu,Y.Wang,Z.Zhang,A.Yang,Mixed major-gene plus polygenes inheritance analysis for CMV disease resistance in flue-cured tobacco,J.Plant Genet.Resour.15(2014)1278-1286.
[18]K.Wen,Z.Zhang,M.Ren,C.Jiang,L.Shen,L.Cheng,R.Geng,X.Chen,L.Feng,A.Yang,QTL analysis of the resistance gene to CMV in flue-cured tobacco,Chin.Tobacco Sci.34(2013)55-59(in Chinese with English abstract).
[19]M.G.Grabherr,B.J.Haas,M.Yassour,J.Z.Levin,D.A.Thompson,I.Amit,X.Adiconis,L.Fan,R.Raychowdhury,Q.Zeng,Full-length transcriptome assembly from RNA-Seq data without a reference genome,Nat.Biotechnol.29(2011)644-652.
[20]N.M.Davidson,A.Oshlack,Corset:enabling differential gene expression analysis for de novo assembled transcriptomes,Genome Biol.15(2014)410.
[21]A.Conesa,S.G?tz,J.M.García-Gómez,J.Terol,M.Talón,M.Robles,Blast2GO:a universal tool for annotation,visualization and analysis in functional genomics research,Bioinformatics 21(2005)3674-3676.
[22]B.Li,C.N.Dewey,RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome,BMC Bioinforma.12(2011)323.
[23]S.Anders,W.Huber,Differential expression analysis for sequence count data,Genome Biol.11(2010)R106.
[24]J.Ye,L.Fang,H.Zheng,Y.Zhang,J.Chen,Z.Zhang,J.Wang,S.Li,R.Li,L.Bolund,WEGO:a web tool for plotting GO annotations,Nucleic Acids Res.34(2006)W293-W297.
[25]M.Kanehisa,M.Araki,S.Goto,M.Hattori,M.Hirakawa,M.Itoh,T.Katayama,S.Kawashima,S.Okuda,T.Tokimatsu,KEGG for linking genomes to life and the environment,Nucleic Acids Res.36(2008)D480-D484.
[26]J.Wu,X.Mao,T.Cai,J.Luo,L.Wei,KOBAS server:a webbased platform for automated annotation and pathway identification,Nucleic Acids Res.34(2006)720-724.
[27]T.D.Schmittgen,K.J.Livak,Analyzing real-time PCR data by the comparative CT method,Nat.Protoc.3(2008)1101-1108.
[28]N.Sierro,J.N.Battey,S.Ouadi,N.Bakaher,L.Bovet,A.Willig,S.Goepfert,M.C.Peitsch,N.V.Ivanov,The tobacco genome sequence and its comparison with those of tomato and potato,Nat.Commun.5(2014)3833.
[29]D.Takemoto,D.A.Jones,A.R.Hardham,GFP-tagging of cell components reveals the dynamics of subcellular reorganization in response to infection of Arabidopsis by oomycete pathogens,Plant J.33(2003)775-792.
[30]D.Takemoto,A.R.Hardham,The cytoskeleton as a regulator and target of biotic interactions in plants,Plant Physiol.136(2004)3864-3876.
[31]C.Geng,Q.Q.Cong,X.D.Li,A.L.Mou,R.Gao,J.L.Liu,Y.P.Tian,Developmentally regulated plasma membrane protein of Nicotiana benthamiana contributes to potyvirus movement and transports to plasmodesmata via the early secretory pathway and the actomyosin system,Plant Physiol.167(2015)394-410.
[32]M.Heinlein,The spread of Tobacco mosaic virus infection:insights into the cellular mechanism of RNA transport,Cell.Mol.Life Sci.59(2002)58-82.
[33]V.Boyko,J.Ferralli,J.Ashby,P.Schellenbaum,M.Heinlein,Function of microtubules in intercellular transport of plant virus RNA,Nat.Cell Biol.2(2000)826-832.
[34]Z.Zhang,Y.Xu,Z.Xie,X.Li,Z.H.He,X.X.Peng,Association-dissociation of glycolate oxidase with catalase in rice:a potential switch to modulate intracellular H2O2levels,Mol.Plant 9(2016)737-748.
[35]K.H.Caffall,D.Mohnen,The structure,function,and biosynthesis of plant cell wall pectic polysaccharides,Carbohydr.Res.344(2009)1879-1900.
[36]A.Giovane,C.Balestrieri,L.Quagliuolo,D.Castaldo,L.Servillo,A glycoprotein inhibitor of pectin methylesterase in kiwi fruit.Purification by affinity chromatography and evidence of a ripening-related precursor,Eur.J.Biochem.233(1995)926-929.
[37]D.Douchkov,S.Lueck,G.Hensel,J.Kumlehn,J.Rajaraman,A.Johrde,M.S.Doblin,C.T.Beahan,M.Kopischke,R.Fuchs,The barley(Hordeum vulgare)cellulose synthase-like D2 gene(HvCslD2)mediates penetration resistance to host-adapted and nonhost isolates of the powdery mildew fungus,New Phytol.212(2016)421-433.
[38]J.D.Jones,J.L.Dangl,The plant immune system,Nature444(2006)323-329.
[39]J.E.Parker,M.J.Coleman,V.Szabo,L.N.Frost,R.Schmidt,E.van der Biezen,T.Moores,C.Dean,M.Daniels,J.D.Jones,The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1receptors with N and L6,Plant Cell 9(1997)879-894.
[40]E.van der Biezen,J.Sun,M.J.Coleman,M.J.Bibb,J.D.Jones,Arabidopsis RelA/SpoT homologs implicate(p)ppGpp in plant signaling,Proc.Natl.Acad.Sci.U.S.A.97(2000)3747-3752.
[41]I.S.Hwang,B.K.Hwang,The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens,Plant Physiol.152(2010)948-967.
[42]M.Alazem,N.S.Lin,Roles of plant hormones in the regulation of host-virus interactions,Mol.Plant Pathol.16(2015)529-540.
[43]C.M.J.Pieterse,A.Leon-Reyes,S.van der Ent,S.C.M.van Wees,Networking by small-molecule hormones in plant immunity,Nat.Chem.Biol.5(2009)308-316.
[44]M.S.Padmanabhan,S.R.Kramer,X.Wang,J.N.Culver,Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions:reprogramming the auxin response pathway to enhance virus infection,J.Virol.82(2008)2477-2485.
[45]S.Marco,D.Levy,Involvement of ethylene in the development of Cucumber mosaic virus-induced chlorotic lesions in cucumber cotyledons,Physiol.Plant Pathol.14(1979)235-244.
[46]L.Chen,L.Zhang,D.Li,F.Wang,D.Yu,WRKY8transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis,Proc.Natl.Acad.Sci.U.S.A.110(2013)E1963-E1971.
[47]Y.Zhang,Y.T.Cheng,N.Qu,Q.Zhao,D.Bi,X.Li,Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs,Plant J.48(2006)647-656.