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Phosphoproteomic analysis of the resistant and susceptible genotypes of maize infected with sugarcane mosaic virus

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Abstract

Protein phosphorylation plays a pivotal role in the regulation of many cellular events. No information is yet available, however, on protein phosphorylation in plants in response to virus infection. In this study, we characterized phosphoproteomes of resistant and susceptible genotypes of maize (Zea mays L.) in response to Sugarcane mosaic virus (SCMV) infection. Based on isotope tags for relative and absolute quantification technology, TiO2 enrichment method and LC–MS/MS analysis, we identified 65 and 59 phosphoproteins respectively, whose phosphorylation level regulated significantly in susceptible and resistant plants. Some identified phosphoproteins were shared by both genotypes, suggesting a partial overlapping of the responsive pathways to virus infection. While several phosphoproteins are well-known pathogen response phosphoproteins, virus infection differentially regulates most other phosphoproteins, which has not been reported in literature. Changes in protein phosphorylation status indicated that response to SCMV infection encompass a reformatting of major cellular processes. Our data provide new valuable insights into plant-virus interactions.

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References

  • Arosio P, Levi S (2002) Ferritin, iron homeostasis, and oxidative damage. Free Radic Biol Med 33:457–463

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Baxter CJ, Foyer CH, Turner J, Rolfe SA, Quick WP (2003) Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. J Exp Bot 54(389):1813–1820

    Article  CAS  PubMed  Google Scholar 

  • Benschop JJ, Mohammed S, O’Flaherty M, Heck AJR, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214

    Article  CAS  PubMed  Google Scholar 

  • Bent AF (1996) Plant disease resistance genes: function meets structure. Plant Cell 8:1757–1771

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carroll AJ, Heazlewood JL, Ito J, Millar AH (2008) Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol Cell Proteomics 7:347–369

    Article  CAS  PubMed  Google Scholar 

  • Cerny M, Dycka F, Bobál’ová J, Brzobohaty B (2011) Early cytokinin response proteins and phosphoproteins of Arabidopsis thaliana identified by proteome and phosphoproteome profiling. J Exp Bot 62:921–937

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  CAS  PubMed  Google Scholar 

  • Daniel JA, Yeager M (2005) Phosphorylation of aquaporin PvTIP3;1 defined by mass spectrometry and molecular modeling. Biochemistry 44:14443–14454

    Article  Google Scholar 

  • Di Carli M, Benvenuto E, Donini M (2012) Recent insight into plant-virus interactions through proteomic analysis. J Proteome Res 11:4765–4780

    Article  PubMed  Google Scholar 

  • Escalante-Pérez M, Krol E, Stange A, Geiger D, Al-Rasheid KA, Hause B, Neher E, Hedrich R (2011) A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proc Natl Acad Sci USA 108:15492–15497

    Article  PubMed Central  PubMed  Google Scholar 

  • Gan D, Zhang J, Jiang H, Jiang T, Zhu S, Cheng B (2010) Bacterially expressed dsRNA protects maize against SCMV infection. Plant Cell Rep 29:1261–1268

    Article  CAS  PubMed  Google Scholar 

  • Gao B, Cui XW, Li XD, Zhang CQ, Miao HQ (2011) Complete genomic sequence analysis of a highly virulent isolate revealed a novel strain of Sugarcane mosaic virus. Virus Genes 43:390–397

    Article  CAS  PubMed  Google Scholar 

  • Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, Sussman MR, Ané JM, Coon JJ (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol 152:19–28

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gudesblat GE, Torres PS, Vojnov AA (2009) Stomata and pathogens: warfare at the gates. Plant Signal Behav 4(12):1114–1116

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198

    Article  CAS  PubMed  Google Scholar 

  • Hanke GT, Kimata-Ariga Y, Taniguchi I, Hase T (2004) A post genomic characterization of Arabidopsis ferredoxins. Plant Physiol 134:255–2564

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang HE, Ger MJ, Yip MK, Chen CY, Pandey AK, Feng TY (2004) A hypersensitive response was induced by virulent bacteria in transgenic tobacco plants overexpressing a plant ferredoxin-like protein (PFLP). Physiol Mol Plant Pathol 64:103–110

    Article  CAS  Google Scholar 

  • Huang C, Verrillo F, Renzone G, Arena S, Rocco M, Scaloni A, Marra M (2011) Response to biotic and oxidative stress in Arabidopsis thaliana: analysis of variably phosphorylated proteins. J Proteomics 74:1934–1949

    Article  CAS  PubMed  Google Scholar 

  • Huber SC, Huber JLA (1996) Role and regulation of sucrosephosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:431–444

    Article  CAS  PubMed  Google Scholar 

  • Kline KG, Barrett-Wilt GA, Sussman MR (2011) Quantitative Plant Phosphoproteomics. Curr Opin Plant Biol 14(5):507–511

    Article  PubMed Central  Google Scholar 

  • Laporte MM, Galagon JA, Shapiro JA, Boersig MR, Shewmaker CR, Sharkey TD (2001) Promoter strength and tissue specificity effects on growth of tomato plants transformed with maize sucrose-phosphate synthase. Planta 212:817–822

    Article  CAS  PubMed  Google Scholar 

  • Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJ (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 4(7):873–886

    Article  CAS  PubMed  Google Scholar 

  • Lasonder E, Green JL, Camarda G, Talabani H, Holder AA, Langsley G, Alano P (2012) The Plasmodium falciparum schizont phosphoproteome reveals extensive phosphatidylinositol and cAMP-protein kinase A signaling. J Proteome Res 11(11):5323–5337

    Article  CAS  PubMed  Google Scholar 

  • Margaria P, Abbà S, Palmano S (2013) Novel aspects of grapevine response to phytoplasma infection investigated by a proteomic and phospho-proteomic approach with data integration into functional networks. BMC Genom 14:38

    Article  CAS  Google Scholar 

  • Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236

    Article  CAS  PubMed  Google Scholar 

  • Mehta A, Magalhães BS, Souza DS, Vasconcelos EA, Silva LP, Grossi-de-Sa MF, Franco OL, da Costa PH, Rocha TL (2008) Rooteomics: the challenge of discovering plant defense-related proteins in roots. Curr Protein Pept Sci 9:108–116

    Article  CAS  PubMed  Google Scholar 

  • Morel JB, Dangl JL (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:671–683

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153(3):1161–1174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen TH, Brechenmacher L, Aldrich JT, Clauss TR, Gritsenko MA et al (2012) Quantitative phosphoproteomic analysis of soybean root hairs inoculated with Bradyrhizobium japonicum. Mol Cell Proteomics 11(11):1140–1155

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Rourke JA, Charlson DV, Gonzalez DO, Vodkin LO, Graham MA, Cianzio SR, Grusak MA, Shoemaker RC (2007) Microarray analysis of iron deficiency chlorosis in near-isogenic soybean lines. BMC Genom 8:476

    Article  Google Scholar 

  • Padhi A, Ramu K (2011) Genomic evidence of intraspecific recombination in sugarcane mosaic virus. Virus Genes 42:282–285

    Article  CAS  PubMed  Google Scholar 

  • Pandey A, Mann M (2000) Proteomics to study genes and genomes. Nature 405:837–846

    Article  CAS  PubMed  Google Scholar 

  • Perera MF, Filippone MP, Ramallo CJ, Cuenya MI, García ML, Ploper LD, Castagnaro AP (2009) Genetic diversity among viruses associated with sugarcane mosaic disease in Tucumán, Argentina. Phytopathology 99:38–49

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA Bioenergetics 975:384–394

    Article  CAS  Google Scholar 

  • Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C, Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins. Mol Cell Proteomics 7:1019–1030

    Article  CAS  PubMed  Google Scholar 

  • Roman DG, Dancis A, Anderson GJ, Klausner RD (1993) The fission yeast ferric reductase gene frp1 + is required for ferric iron uptake and encodes a protein that is homologous to the gp91-phox subunit of the human NADPH phagocyte oxidoreductase. Mol Cell Biol 13:4342–4350

    PubMed Central  CAS  PubMed  Google Scholar 

  • Scharte J, Sch ÖH, Weis E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ 28:1421–1435

    Article  CAS  Google Scholar 

  • Shin R, Alvarez S, Burch AY, Jez JM, Schachtman DP (2007) Phosphoproteomic identification of targets of the Arabidopsis sucrose nonfermenting-like kinase SnRK2.8 reveals a connection to metabolic processes. Proc Natl Acad Sci USA 104:6460–6465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sinapidou E, Williams K, Nott L, Bahkt S, Tör M, Crute I, Bittner-Eddy P, Beynon J (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J 38:898–909

    Article  CAS  PubMed  Google Scholar 

  • Stulemeijer IJ, Joosten MH, Jensen ON (2009) Quantitative phosphoproteomics of tomato mounting a hypersensitive response reveals a swift suppression of photosynthetic activity and a differential role for hsp90 isoforms. J Proteome Res 8(3):1168–1182

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4:193. doi:10.1038/msb.2008.32

    Article  PubMed Central  PubMed  Google Scholar 

  • Taus T, Kocher T, Pichler P, Paschke C, Schmidt A, Henrich C, Mechtler K (2011) Universal and confident phosphorylation site localization using phosphors. J Proteome Res 10(12):5354–5362

    Article  CAS  PubMed  Google Scholar 

  • van Loon L (1987) Disease induction by plant virus. Adv Virus Res 33:205–255

    Article  PubMed  Google Scholar 

  • Viswanathan R, Karuppaiah R, Balamuralikrishnan M (2009) Identification of new variants of SCMV causing sugarcane mosaic in India and assessing their genetic diversity in relation to SCMV type strains. Virus Genes 39:375–386

    Article  CAS  PubMed  Google Scholar 

  • Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362

    Article  PubMed  Google Scholar 

  • Wu LJ, Zu XF, Wang SX, Chen YH (2012) Sugarcane mosaic virus—long history but still a threat to industry. Crop Prot 42:74–78

    Article  Google Scholar 

  • Wu LJ, Han ZP, Wang SX, Wang XT, Sun AG, Zu XF, Chen YH (2013) Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible genotypes of maize infected with sugarcane mosaic virus. J Proteomics 89:124–140

    Article  PubMed  Google Scholar 

  • Xing T, Laroche A (2011) Revealing plant defense signaling: getting more sophisticated with phosphoproteomics. Plant Signal Behav 6(10):1469–1474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu DL, Park JW, Mirkov TE, Zhou GH (2008) Viruses causing mosaic disease in sugarcane and their genetic diversity in southern China. Arch Virol 153:1031–1039

    Article  PubMed  Google Scholar 

  • Zwerger K, Hirt H (2001) Recent advances in plant MAP kinase signalling. Biol Chem 382:1123–1131

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Yingying Zhang for help with pathogen collection. This work was supported by the National Natural Science Foundation of China (31471503), the Ph.D Programs Foundation of the Ministry of Education of China (30600272) and the China Postdoctoral Science Foundation (201104369).

Conflict of interest

We declare that we have no conflict of interest.

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Authors and Affiliations

  1. Henan Agricultural University and Synergetic Innovation Center of Henan Grain Crops, Zhengzhou, China

    Liuji Wu, Shunxi Wang, Jianyu Wu, Liancheng Wu, Huimin Zhang, Yanhui Chen & Xiuli Hu

  2. Key Laboratory of Physiological Ecology and Genetic Improvement of Food Crops in Henan Province, Zhengzhou, China

    Liuji Wu, Shunxi Wang, Jianyu Wu, Liancheng Wu, Huimin Zhang & Yanhui Chen

  3. College of Agronomy, Henan University of Science and Technology, Luoyang, 471003, China

    Zanping Han

  4. Shanghai Applied Protein Technology Co. Ltd, Shanghai, 200233, China

    Rui Wang

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  1. Liuji Wu
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Correspondence to Yanhui Chen or Xiuli Hu.

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726_2014_1880_MOESM1_ESM.doc

Supplementary material 1 (DOC 2440 kb) Figure S1. Mass spectra for the phosphopeptides exhibit significant difference in quantity

Supplementary material 2 (XLSX 136 kb) Table S1. Original data for all the identified and quantified phosphopeptides

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Wu, L., Wang, S., Wu, J. et al. Phosphoproteomic analysis of the resistant and susceptible genotypes of maize infected with sugarcane mosaic virus . Amino Acids 47, 483–496 (2015). https://doi.org/10.1007/s00726-014-1880-2

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