Skip to main content
Top
Published in: Virology Journal 1/2015

Open Access 01-12-2015 | Research

Quantitative proteomics identifies 38 proteins that are differentially expressed in cucumber in response to cucumber green mottle mosaic virus infection

Authors: Hua-Wei Liu, Chao-Qiong Liang, Peng-Fei Liu, Lai-Xin. Luo, Jian-Qiang Li

Published in: Virology Journal | Issue 1/2015

Login to get access

Abstract

Background

Since it was first reported in 1935, Cucumber green mottle mosaic virus (CGMMV) has become a serious pathogen in a range of cucurbit crops. The virus is generally transmitted by propagation materials, and to date no effective chemical or cultural methods of control have been developed to combat its spread. The current study presents a preliminary analysis of the pathogenic mechanisms from the perspective of protein expression levels in an infected cucumber host, with the objective of elucidating the infection process and potential strategies to reduce both the economic and yield losses associated with CGMMV.

Methods

Isobaric tags for relative and absolute quantitation (iTRAQ) technology coupled with liquid chromatography-tandem mass spectrometric (LC-MS/MS) were used to identify the differentially expressed proteins in cucumber plants infected with CGMMV compared with mock-inoculated plants. The functions of the proteins were deduced by functional annotation and their involvement in metabolic processes explored by KEGG pathway analysis to identify their interactions during CGMMV infection, while their in vivo expression was further verified by qPCR.

Results

Infection by CGMMV altered both the expression level and absolute quantity of 38 proteins (fold change >0.6) in cucumber hosts. Of these, 23 were found to be up-regulated, while 15 were down-regulated. Gene ontology (GO) analysis revealed that 22 of the proteins had a combined function and were associated with molecular function (MF), biological process (BP) and cellular component (CC). Several other proteins had a dual function with 1, 7, and 2 proteins being associated with BP/CC, BP/MF, CC/MF, respectively. The remaining 3 proteins were only involved in MF. In addition, Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis identified 18 proteins that were involved in 13 separate metabolic pathways. These pathways were subsequently merged to generate three network diagrams illustrating the interactions between the different pathways, while qPCR was used to track the changes in expression levels of the proteins identified at 3 time points during CGMMV infection. Taken together these results greatly expand our understanding of the relationships between CGMMV and cucumber hosts.

Conclusions

The results of the study indicate that CGMMV infection significantly changes the physiology of cucumbers, affecting the expression levels of individual proteins as well as entire metabolic pathways. The bioinformatic analysis also identified several pathogenesis-related (PR) proteins that could be useful in the development of disease-resistant plants.
Literature
1.
go back to reference Mink GI. Pollen- and seed-transmitted viruses and viroids. Annu Rev Phytopathol. 1993;31:375–402.CrossRefPubMed Mink GI. Pollen- and seed-transmitted viruses and viroids. Annu Rev Phytopathol. 1993;31:375–402.CrossRefPubMed
2.
go back to reference Liu HW, Luo LX, Li JQ, Liu PF, Chen XY, Hao JJ. Pollen and seed transmission of cucumber green mottle mosaic virus in cucumber. Plant Pathol. 2014;63:72–7.CrossRef Liu HW, Luo LX, Li JQ, Liu PF, Chen XY, Hao JJ. Pollen and seed transmission of cucumber green mottle mosaic virus in cucumber. Plant Pathol. 2014;63:72–7.CrossRef
3.
go back to reference Shim CK, Han KS, Lee JH, Bae DW, Kim DK, Kim HK. Isolation and characterization of watermelon isolate of Cucumber green mottle mosaic virus (CGMMV-HY1) from watermelon plants with severe mottle mosaic symptoms. J Plant Pathol. 2005;21:167–71.CrossRef Shim CK, Han KS, Lee JH, Bae DW, Kim DK, Kim HK. Isolation and characterization of watermelon isolate of Cucumber green mottle mosaic virus (CGMMV-HY1) from watermelon plants with severe mottle mosaic symptoms. J Plant Pathol. 2005;21:167–71.CrossRef
4.
go back to reference Ainsworth GC. Mosaic diseases of the cucumber. Ann Appl Biol. 1935;22:55–67.CrossRef Ainsworth GC. Mosaic diseases of the cucumber. Ann Appl Biol. 1935;22:55–67.CrossRef
5.
go back to reference Antignus Y, Pearlsman M, Ben-Yoseph R, Cohen S. Occurrence of variant of cucumber green mottle mosaic virus in Israel. Phys Chem Chem Phys. 2002;18:50–6. Antignus Y, Pearlsman M, Ben-Yoseph R, Cohen S. Occurrence of variant of cucumber green mottle mosaic virus in Israel. Phys Chem Chem Phys. 2002;18:50–6.
6.
go back to reference Varveri C, Vassilakos N, Bem F. Characterization and detection of cucumber green mottle mosaic virus in Greece. Phys Chem Chem Phys. 2002;30:493–501. Varveri C, Vassilakos N, Bem F. Characterization and detection of cucumber green mottle mosaic virus in Greece. Phys Chem Chem Phys. 2002;30:493–501.
7.
go back to reference Zhang YJ, Li GF, Li MF. Occurrence of cucumber green mottle mosaic virus on cucurbitaceous plants in China. Plant Dis. 2009;93:200.CrossRef Zhang YJ, Li GF, Li MF. Occurrence of cucumber green mottle mosaic virus on cucurbitaceous plants in China. Plant Dis. 2009;93:200.CrossRef
9.
go back to reference Ling KS, Li R, Zhang W. First Report of Cucumber green mottle mosaic virus Infecting Greenhouse Cucumber in Canada. Plant Dis. 2014;98(5):701. Ling KS, Li R, Zhang W. First Report of Cucumber green mottle mosaic virus Infecting Greenhouse Cucumber in Canada. Plant Dis. 2014;98(5):701.
10.
go back to reference O’Donnell PJ, Schmelz EA, Moussatche P, Lund ST, Jones JB, Klee HJ. Susceptible to intolerance -a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J. 2003;33:245–57.CrossRefPubMed O’Donnell PJ, Schmelz EA, Moussatche P, Lund ST, Jones JB, Klee HJ. Susceptible to intolerance -a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J. 2003;33:245–57.CrossRefPubMed
12.
14.
go back to reference Ventelon-Debout M, Delalande F, Brizard JP, Diemer H, Van Dorsselaer A, Brugidou C. Proteome analysis of cultivar-specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing rice yellow mottle virus infection. Proteomics. 2004;4:216–25.CrossRefPubMed Ventelon-Debout M, Delalande F, Brizard JP, Diemer H, Van Dorsselaer A, Brugidou C. Proteome analysis of cultivar-specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing rice yellow mottle virus infection. Proteomics. 2004;4:216–25.CrossRefPubMed
15.
go back to reference Weeb KM, Broccardo CJ, Prenni JE, Wintermantel WM. Proteomic profiling of sugar beet (Beta vulgaris) leaves during rhizomania compatible interactions. Protromes. 2014;2:208–23.CrossRef Weeb KM, Broccardo CJ, Prenni JE, Wintermantel WM. Proteomic profiling of sugar beet (Beta vulgaris) leaves during rhizomania compatible interactions. Protromes. 2014;2:208–23.CrossRef
16.
go back to reference Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cells host microbe. 2009;6(5):457–69.CrossRef Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cells host microbe. 2009;6(5):457–69.CrossRef
17.
go back to reference Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: shaping the evolution of the plant immune. Cell. 2006;124(4):803–14.CrossRefPubMed Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: shaping the evolution of the plant immune. Cell. 2006;124(4):803–14.CrossRefPubMed
18.
go back to reference Bhat S, Folimonova SY, Cole A, Ballard KD, Lei ZT, Watson B, et al. Influence of host chloroplast proteins on tobacco mosaic virus accumulation and intercellar movement. Plant Physiol. 2013;161:134–47.PubMedCentralCrossRefPubMed Bhat S, Folimonova SY, Cole A, Ballard KD, Lei ZT, Watson B, et al. Influence of host chloroplast proteins on tobacco mosaic virus accumulation and intercellar movement. Plant Physiol. 2013;161:134–47.PubMedCentralCrossRefPubMed
19.
go back to reference Czosnek H, Eybishtz A, Sade D, Gorovits R, Sobol I, Bejarano E, et al. Discovering host genes involved in the infection by the tomato yellow leaf curl virus complex and in the establishment of resistance to the virus using tobacco rattle virus-based post transcriptional gene silencing. Viruses. 2013;5:998–1022.PubMedCentralCrossRefPubMed Czosnek H, Eybishtz A, Sade D, Gorovits R, Sobol I, Bejarano E, et al. Discovering host genes involved in the infection by the tomato yellow leaf curl virus complex and in the establishment of resistance to the virus using tobacco rattle virus-based post transcriptional gene silencing. Viruses. 2013;5:998–1022.PubMedCentralCrossRefPubMed
20.
go back to reference Jenner RG, Young RA. Insights to host responses against pathogens from transcriptional profiling. Nat Rev Microbiol. 2005;3:281–94.CrossRefPubMed Jenner RG, Young RA. Insights to host responses against pathogens from transcriptional profiling. Nat Rev Microbiol. 2005;3:281–94.CrossRefPubMed
22.
go back to reference Wu WW, Wang GH, Baek SJ, Shen RF. Comparative study of three proteomic quantitative methods, DIGE, clCAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res. 2006;5(3):651–8.CrossRefPubMed Wu WW, Wang GH, Baek SJ, Shen RF. Comparative study of three proteomic quantitative methods, DIGE, clCAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF. J Proteome Res. 2006;5(3):651–8.CrossRefPubMed
24.
go back to reference Wu LJ, Wang SX, Wu JY, Han ZP, Wang R, Wu, LC, et al. Phosphoproteomic analysis of the resistant and susceptible genotypes of maize infected with sugarcane mosaic virus. Amino acids. 2014;doi:10.1007/s00726-014-1880-2. Wu LJ, Wang SX, Wu JY, Han ZP, Wang R, Wu, LC, et al. Phosphoproteomic analysis of the resistant and susceptible genotypes of maize infected with sugarcane mosaic virus. Amino acids. 2014;doi:10.​1007/​s00726-014-1880-2.
26.
28.
go back to reference Lobo I. Pleiotropy: One gene can affect multiple traits. Nature Education. 2008;1:10. Lobo I. Pleiotropy: One gene can affect multiple traits. Nature Education. 2008;1:10.
29.
go back to reference Kuromori T, Takahashi S, Kondou Y, Shinozaki K, Matsui M. Phenome analysis in plant species using loss-of-function and gain-of-function mutants. Plant Cell Physiol. 2009;50:1215–31.PubMedCentralCrossRefPubMed Kuromori T, Takahashi S, Kondou Y, Shinozaki K, Matsui M. Phenome analysis in plant species using loss-of-function and gain-of-function mutants. Plant Cell Physiol. 2009;50:1215–31.PubMedCentralCrossRefPubMed
31.
go back to reference Plader W, Yukawa Y, Sugiura M, Malepszy S. The complete structure of the cucumber (Cucumis sativus L.) chloroplast genome: its composition and comparative analysis. Cell Mol Biol Lett. 2007;12:584–94.CrossRefPubMed Plader W, Yukawa Y, Sugiura M, Malepszy S. The complete structure of the cucumber (Cucumis sativus L.) chloroplast genome: its composition and comparative analysis. Cell Mol Biol Lett. 2007;12:584–94.CrossRefPubMed
32.
go back to reference Spetea C. Role of chloroplast thylakoid lumen in photosynthetic regulation and plant cell signaling. Progress in botany. 2012;73:207–30.CrossRef Spetea C. Role of chloroplast thylakoid lumen in photosynthetic regulation and plant cell signaling. Progress in botany. 2012;73:207–30.CrossRef
33.
go back to reference Ahuja I, de Vos RC, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci. 2010;15:664–74.CrossRefPubMed Ahuja I, de Vos RC, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci. 2010;15:664–74.CrossRefPubMed
34.
go back to reference Shirley BW. Flavonoid biosynthesis: ‘new’ functions for an ‘old’ pathway. Trends Plant Sci. 1996;1:377–82. Shirley BW. Flavonoid biosynthesis: ‘new’ functions for an ‘old’ pathway. Trends Plant Sci. 1996;1:377–82.
35.
go back to reference Schijlen EGWM, Chr-De V, Aj-Van T, Bovy AG. Modification of flavonoid biosynthesis in crop plants. Phytochemistry. 2004;65:2631–48.CrossRefPubMed Schijlen EGWM, Chr-De V, Aj-Van T, Bovy AG. Modification of flavonoid biosynthesis in crop plants. Phytochemistry. 2004;65:2631–48.CrossRefPubMed
36.
go back to reference Besseau S, Hoffmanna L, Geoffroya P, Lapierreb C, Polletb B, Legranda M. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. The Plant Cell January. 2007;19:148–62.CrossRef Besseau S, Hoffmanna L, Geoffroya P, Lapierreb C, Polletb B, Legranda M. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. The Plant Cell January. 2007;19:148–62.CrossRef
37.
go back to reference Xu L, Zhu LF, Tu LL, Liu LL, Yuan DJ, Jin L, et al. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot. 2011;62:5607–21.PubMedCentralCrossRefPubMed Xu L, Zhu LF, Tu LL, Liu LL, Yuan DJ, Jin L, et al. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot. 2011;62:5607–21.PubMedCentralCrossRefPubMed
38.
go back to reference Kao YY, Harding SA, Tsai CJ. Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol. 2002;130:796–807.PubMedCentralCrossRefPubMed Kao YY, Harding SA, Tsai CJ. Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol. 2002;130:796–807.PubMedCentralCrossRefPubMed
39.
go back to reference Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA. Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry. 2003;64:153–61.CrossRefPubMed Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C, Dixon RA. Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry. 2003;64:153–61.CrossRefPubMed
40.
go back to reference Gayoso C, Pomar F, Novo-Uzal E, Merino F, Martinez de Ilarduya O. The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol. 2010;10:232–51.PubMedCentralCrossRefPubMed Gayoso C, Pomar F, Novo-Uzal E, Merino F, Martinez de Ilarduya O. The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol. 2010;10:232–51.PubMedCentralCrossRefPubMed
41.
go back to reference Mao WH, Gong YM, Song XS, Xia XJ, Shi K, Zhou YH, et al. Construction of a cucumber cDNA microarray and its application in the study of response of cucumber plants to magnesium deficiency stress. Acta horticulturae sinica (in Chinese). 2006;33:767–72. Mao WH, Gong YM, Song XS, Xia XJ, Shi K, Zhou YH, et al. Construction of a cucumber cDNA microarray and its application in the study of response of cucumber plants to magnesium deficiency stress. Acta horticulturae sinica (in Chinese). 2006;33:767–72.
42.
go back to reference Li JW. Identification of cucumber genes associated with resistance to downy mildew and mechanism for the hypersensitive response. Huazhong agricultural university. Academic thesis. 2010. Li JW. Identification of cucumber genes associated with resistance to downy mildew and mechanism for the hypersensitive response. Huazhong agricultural university. Academic thesis. 2010.
43.
go back to reference Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, Ellerstrom M, et al. Arabidopsis phospholipase d is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol. 2013;163:896–906.PubMedCentralCrossRefPubMed Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, Ellerstrom M, et al. Arabidopsis phospholipase d is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol. 2013;163:896–906.PubMedCentralCrossRefPubMed
45.
go back to reference Walker SK, Garrill A. Actin microfilaments in fungi. Mycologist. 2006;20:26–31.CrossRef Walker SK, Garrill A. Actin microfilaments in fungi. Mycologist. 2006;20:26–31.CrossRef
46.
go back to reference Day B, Graham T. The host-pathogen interface cell wall and membrane dynamics of pathogen-induced responses. Ann N Y Acad Sci. 2007;1113:123–34.CrossRefPubMed Day B, Graham T. The host-pathogen interface cell wall and membrane dynamics of pathogen-induced responses. Ann N Y Acad Sci. 2007;1113:123–34.CrossRefPubMed
48.
go back to reference Day B, Henty JL, Porter KJ, Staiger CJ. The pathogen-actin connection: a platform for defense signaling in plants. Annu Rev Phytopathol. 2011;49:483–506.CrossRefPubMed Day B, Henty JL, Porter KJ, Staiger CJ. The pathogen-actin connection: a platform for defense signaling in plants. Annu Rev Phytopathol. 2011;49:483–506.CrossRefPubMed
49.
go back to reference van den Ent F, Amos LA, LÖwe J. Prokaryotic origin of the actin cytoskeleton. Nature. 2001;413:39–44.CrossRefPubMed van den Ent F, Amos LA, LÖwe J. Prokaryotic origin of the actin cytoskeleton. Nature. 2001;413:39–44.CrossRefPubMed
51.
go back to reference Millar AJ, McGrath RB, Chua NH. Phytochrome phototransduction pathways. Annu Rev Genet. 1994;28:325–49.CrossRefPubMed Millar AJ, McGrath RB, Chua NH. Phytochrome phototransduction pathways. Annu Rev Genet. 1994;28:325–49.CrossRefPubMed
52.
go back to reference Esposti MD, Vries SD, Crimi M, Ghelli A, Patarnello T, Meyer A. Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta. 1993;1143:243–71.CrossRefPubMed Esposti MD, Vries SD, Crimi M, Ghelli A, Patarnello T, Meyer A. Mitochondrial cytochrome b: evolution and structure of the protein. Biochim Biophys Acta. 1993;1143:243–71.CrossRefPubMed
53.
go back to reference Brandt U, Trumpower BL. The proton-motive Q cycle in mitochondria and bacteria. Crit Rev Biochem Mol Biol. 1994;29:165–97.CrossRefPubMed Brandt U, Trumpower BL. The proton-motive Q cycle in mitochondria and bacteria. Crit Rev Biochem Mol Biol. 1994;29:165–97.CrossRefPubMed
54.
go back to reference Zannoni D. Cytochrome b type oxidases in the respiratory chains of the phytopathogenic fluorescent bacteria Pseudomonas cichorii and Pseudomonas aptata. Arch microbial. 1982;133:267–73.CrossRef Zannoni D. Cytochrome b type oxidases in the respiratory chains of the phytopathogenic fluorescent bacteria Pseudomonas cichorii and Pseudomonas aptata. Arch microbial. 1982;133:267–73.CrossRef
55.
go back to reference Zannoni D. The respiratory chains of pathogenic pseudomonads. Biochim Biophys Acta. 1989;975:299–316.CrossRefPubMed Zannoni D. The respiratory chains of pathogenic pseudomonads. Biochim Biophys Acta. 1989;975:299–316.CrossRefPubMed
56.
go back to reference Semar M, Strobel D, Koch A, Klappach K, Stammler G. Field efficacy of pyraclostrobin against populations of Pyrenophora teres containing the F129L mutation in the cytochrome b gene. Journal of plant diseases and protection. 2007;114:117–9. Semar M, Strobel D, Koch A, Klappach K, Stammler G. Field efficacy of pyraclostrobin against populations of Pyrenophora teres containing the F129L mutation in the cytochrome b gene. Journal of plant diseases and protection. 2007;114:117–9.
57.
go back to reference Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B. The strobilurin fungicides. Pest Manag Sci. 2002;58:649–62.CrossRefPubMed Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B. The strobilurin fungicides. Pest Manag Sci. 2002;58:649–62.CrossRefPubMed
58.
go back to reference Xoconostle-Cázares B, Ruiz-Medrano R, Lucas WJ. Proteolytic processing of CmPP36, a protein from the cytochrome b5 reductase family, is required for entry into the phloem translocation pathway. Plant J. 2000;24(6):735–47.CrossRefPubMed Xoconostle-Cázares B, Ruiz-Medrano R, Lucas WJ. Proteolytic processing of CmPP36, a protein from the cytochrome b5 reductase family, is required for entry into the phloem translocation pathway. Plant J. 2000;24(6):735–47.CrossRefPubMed
59.
go back to reference Simn-Buela L, Garca-Arenal F. Virus particles of cucumber green mottle mosaic tobamovirus move systemically in the phloem of infected cucumber plants. Mol Plant Microbe Interact. 1999;12(2):112–8.CrossRef Simn-Buela L, Garca-Arenal F. Virus particles of cucumber green mottle mosaic tobamovirus move systemically in the phloem of infected cucumber plants. Mol Plant Microbe Interact. 1999;12(2):112–8.CrossRef
60.
go back to reference Miles D. The role of high chlorophyll fluorescence photosynthesis mutants in the analysis of chloroplast thylakoid membrane assembly and function. Maydica. 1994;39:35–45. Miles D. The role of high chlorophyll fluorescence photosynthesis mutants in the analysis of chloroplast thylakoid membrane assembly and function. Maydica. 1994;39:35–45.
61.
go back to reference Hutcheson SW, Buchanan BB. Enzyme regulation in Crassulacean acid metabolism photosynthesis. Plant Physiol. 1979;72:870–6.CrossRef Hutcheson SW, Buchanan BB. Enzyme regulation in Crassulacean acid metabolism photosynthesis. Plant Physiol. 1979;72:870–6.CrossRef
62.
go back to reference Balachandran S, Hurry VM, Kelley SE, Osmond CB, Robinson SA, Rohozinski J, et al. Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiol Plant. 1997;100:203–13.CrossRef Balachandran S, Hurry VM, Kelley SE, Osmond CB, Robinson SA, Rohozinski J, et al. Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiol Plant. 1997;100:203–13.CrossRef
63.
go back to reference Jaber R, Isabel GL, Matilde B. Inhibition of photosynthesis by viral infection: Effect on PSII structure and function. Physiol Plant. 2000;110:286–92.CrossRef Jaber R, Isabel GL, Matilde B. Inhibition of photosynthesis by viral infection: Effect on PSII structure and function. Physiol Plant. 2000;110:286–92.CrossRef
65.
67.
go back to reference Deng W, Liu C, Deng X, Niu L, Cao X. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol. 2007;143:1660–8.PubMedCentralCrossRefPubMed Deng W, Liu C, Deng X, Niu L, Cao X. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol. 2007;143:1660–8.PubMedCentralCrossRefPubMed
68.
go back to reference Solomon PS, Lee RC, Greer TJW, Oliver RP. Pathogenicity of Stagonospora nodorum requires malate synthase. Mol Microbiol. 2004;53:1065–73.CrossRefPubMed Solomon PS, Lee RC, Greer TJW, Oliver RP. Pathogenicity of Stagonospora nodorum requires malate synthase. Mol Microbiol. 2004;53:1065–73.CrossRefPubMed
69.
go back to reference Wang ZY, Thornton CR, Kershaw MJ, Li DB, Talbot NJ. The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol. 2003;47:1601–12.CrossRefPubMed Wang ZY, Thornton CR, Kershaw MJ, Li DB, Talbot NJ. The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol. 2003;47:1601–12.CrossRefPubMed
70.
go back to reference Idnurm A, Howlett BJ. Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola Brassica napus. Eukaryot Cell. 2002;1:719–24.PubMedCentralCrossRefPubMed Idnurm A, Howlett BJ. Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola Brassica napus. Eukaryot Cell. 2002;1:719–24.PubMedCentralCrossRefPubMed
71.
go back to reference Kim MS, Cho SM, Kang EY, Im YJ, Hwangbo H, Kim YC, et al. Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol Plant Microbe Interact. 2008;21:1643–53.CrossRefPubMed Kim MS, Cho SM, Kang EY, Im YJ, Hwangbo H, Kim YC, et al. Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol Plant Microbe Interact. 2008;21:1643–53.CrossRefPubMed
72.
go back to reference Van VL. A new evolutionary law. Evolutionary Theory. 1973;1:1–30. Van VL. A new evolutionary law. Evolutionary Theory. 1973;1:1–30.
73.
go back to reference De Meaux J, Mitchell-Olds T. Evolution of plant resistance at the molecular level: Ecological context of species interactions. Heredity. 2003;91(4):345–52.CrossRefPubMed De Meaux J, Mitchell-Olds T. Evolution of plant resistance at the molecular level: Ecological context of species interactions. Heredity. 2003;91(4):345–52.CrossRefPubMed
74.
go back to reference Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 1998;17:170–80.PubMedCentralCrossRefPubMed Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 1998;17:170–80.PubMedCentralCrossRefPubMed
75.
go back to reference Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA. Structure-function of the cytochrome b6f complex. Photochem Photobiol. 2008;84(6):1349–58.CrossRefPubMed Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA. Structure-function of the cytochrome b6f complex. Photochem Photobiol. 2008;84(6):1349–58.CrossRefPubMed
76.
go back to reference Berg JM, Tymoczko JL, Biochemistry SL. Biochemistry. New York: W.H. Freeman; 2007. ISBN 978-0-7167-8724-2. Berg JM, Tymoczko JL, Biochemistry SL. Biochemistry. New York: W.H. Freeman; 2007. ISBN 978-0-7167-8724-2.
77.
go back to reference Reinero A, Beachy RN. Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Mol Biol. 1986;6:291–301.CrossRefPubMed Reinero A, Beachy RN. Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Mol Biol. 1986;6:291–301.CrossRefPubMed
78.
go back to reference Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63:3523–43.CrossRefPubMed Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63:3523–43.CrossRefPubMed
79.
go back to reference Fan YH, Chen J, Zhang CY, Guo H, Lin Y. A two-dimensional electrophoresis protocol suitable for proteomic analysis of cucumber leaves. Journal of Shenyang agricultural university. 2007;39:365–7. Fan YH, Chen J, Zhang CY, Guo H, Lin Y. A two-dimensional electrophoresis protocol suitable for proteomic analysis of cucumber leaves. Journal of Shenyang agricultural university. 2007;39:365–7.
Metadata
Title
Quantitative proteomics identifies 38 proteins that are differentially expressed in cucumber in response to cucumber green mottle mosaic virus infection
Authors
Hua-Wei Liu
Chao-Qiong Liang
Peng-Fei Liu
Lai-Xin. Luo
Jian-Qiang Li
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2015
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-015-0442-x

Other articles of this Issue 1/2015

Virology Journal 1/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.