Zucchini yellow mosaic virus (ZYMV) is an emerging viral pathogen in cucurbit-growing areas wordwide. Infection causes significant yield losses in several species of the family Cucurbitaceae. To identify proteins potentially involved with resistance toward infection by the severe ZYMV-H isolate, two Cucurbita pepo cultivars (Zelena susceptible and Jaguar partially resistant) were analyzed using a two-dimensional gel electrophoresis-based proteomic approach. Initial symptoms on leaves (clearing veins) developed 6-7 days post-inoculation (dpi) in the susceptible C. pepo cv. Zelena. In contrast, similar symptoms appeared on the leaves of partially resistant C. pepo cv. Jaguar only after 15 dpi. This finding was confirmed by immune-blot analysis which showed higher levels of viral proteins at 6 dpi in the susceptible cultivar. Leaf proteome analyses revealed 28 and 31 spots differentially abundant between cultivars at 6 and 15 dpi, respectively. The variance early in infection can be attributed to a rapid activation of proteins involved with redox homeostasis in the partially resistant cultivar. Changes in the proteome of the susceptible cultivar are related to the cytoskeleton and photosynthesis.

Institute of Botany Slovak Academy of Sciences Bratislava Slovakia

Institute of Virology Slovak Academy of Sciences Bratislava Slovakia

Institute of Virology Slovak Academy of Sciences Bratislava Slovakia ; Institute of Microbiology Academy of Sciences of Czech Republic Prague Czech Republic

See more in PubMed

Alvarez M. E., Pennell R. I., Meijer P. J., Ishikawa A., Dixon R. A., Lamb C. (1998). Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784. 10.1016/S0092-8674(00)81405-1 PubMed DOI

Apel K., Hirt H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. 10.1146/annurev.arplant.55.031903.141701 PubMed DOI

Babu M., Gagarinova A. G., Brandle J. E., Wang A. (2008). Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. J. Gen. Virol. 89, 1069–1080. 10.1099/vir.0.83531-0 PubMed DOI

Bevan M., Bancroft I., Bent E., Love K., Goodman H., Dean C., et al. . (1998). Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391, 485–488. 10.1038/35140 PubMed DOI

Blua M. J., Perring T. M. (1989). Effect of Zuccini yellow mosaic virus on development and yield of cantaloupe (Cucumis melo). Plant Dis. 73, 317–320 10.1094/PD-73-0317 DOI

Bollenbach T. J., Sharwood R. E., Gutierrez R., Lerbs-Mache S., Stern D. B. (2009). The RNA-binding proteins CSP41a and CSP41b may regulate transcription and translation of chloroplast-encoded RNAs in Arabidopsis. Plant Mol. Biol. 69, 541–552. 10.1007/s11103-008-9436-z PubMed DOI

Bonardi V., Cherkis K., Nishimura M. T., Dangl J. L. (2012). A new eye on NLR proteins: focused on clarity or diffused by complexity? Curr. Opin. Immunol. 24, 41–50. 10.1016/j.coi.2011.12.006 PubMed DOI PMC

Bradford M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254. 10.1016/0003-2697(76)90527-3 PubMed DOI

Brown R. N., Bolanos-Herrera A., Myers J. R., Jahn M. M. (2003). Inheritance of resistance to four cucurbit viruses in Cucurbita moschata. Euphytica 129, 253–258 10.1023/A:1022224327064 DOI

Canto T., Aranda M. A., Fereres A. (2009). Climate change effects on physiology and population processes of hosts and vectors that influence the spread of hemipteran-borne plant viruses. Glob. Change Biol. 15, 1884–1894 10.1111/j.1365-2486.2008.01820.x DOI

De Gara L., Locato V., Dipierro S., De Pinto M. C. (2010). Redox homeostasis in plants. The challenge of living with endogenous oxygen production. Respir. Physiol. Neurobiol. 173, S13–S19. 10.1016/j.resp.2010.02.007 PubMed DOI

Desbiez C., Lecoq H. (1997). Zucchini yellow mosaic virus. Plant Pathol. 46, 809–829 10.1046/j.1365-3059.1997.d01-87.x DOI

Di Carli M., Benvenuto E., Donini M. (2012). Recent insights into plant-virus interactions through proteomic analysis. J. Proteome Res. 11, 4765–4780. 10.1021/pr300494e PubMed DOI

Dielen A. S., Badaoui S., Candresse T., German-Retana S. (2010). The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game. Mol. Plant Pathol. 11, 293–308. 10.1111/j.1364-3703.2009.00596.x PubMed DOI PMC

Doubnerova V., Muller K., Cerovska N., Synkova H., Spoustova P., Ryslava H. (2009). Effect of potato virus Y on the NADP-malic enzyme from nicotiana tabacum L.: mRNA, expressed protein and activity. Int. J. Mol. Sci. 10, 3583–3598. 10.3390/ijms10083583 PubMed DOI PMC

Drincovich M. F., Casati P., Andreo C. S. (2001). NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett. 490, 1–6. 10.1016/S0014-5793(00)02331-0 PubMed DOI

Figueiredo A., Monteiro F., Fortes A. M., Bonow-Rex M., Zyprian E., Sousa L., et al. . (2012). Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine. Funct. Integr. Genomics 12, 379–386. 10.1007/s10142-012-0261-8 PubMed DOI

Flores-Ramirez G., Jankovicova B., Bilkova Z., Miernyk J. A., Skultety L. (2014). Identification of Coxiella burnetii surface-exposed and cell envelope associated proteins using a combined bioinformatics plus proteomics strategy. Proteomics 16, 1868–1881. 10.1002/pmic.201300338 PubMed DOI

Gadjev I., Vanderauwera S., Gechev T. S., Laloi C., Minkov I. N., Shulaev V., et al. . (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436–445. 10.1104/pp.106.078717 PubMed DOI PMC

Gal-On A. (2007). Zucchini yellow mosaic virus: insect transmission and pathogenicity—the tails of two proteins. Mol. Plant Pathol. 8, 139–150. 10.1111/j.1364-3703.2007.00381.x PubMed DOI

Glasa M., Svoboda J., Novakova S. (2007). Analysis of the molecular and biological variability of Zucchini yellow mosaic virus isolates from Slovakia and Czech Republic. Virus Genes 35, 415–421. 10.1007/s11262-007-0101-4 PubMed DOI

Gotor C., Romero L. C. (2013). S-sulfocysteine synthase function in sensing chloroplast redox status. Plant Signal. Behav. 8:e23313. 10.4161/psb.23313 PubMed DOI PMC

Hanna J., Finley D. (2007). A proteasome for all occasions. FEBS Lett. 581, 2854–2861. 10.1016/j.febslet.2007.03.053 PubMed DOI PMC

Heyno E., Alkan N., Fluhr R. (2013). A dual role for plant quinone reductases in host-fungus interaction. Physiol. Plant. 149, 340–353. 10.1111/ppl.12042 PubMed DOI

Jankovicova B., Skultety L., Dubrovcakova M., Stern M., Bilkova Z., Lakota J. (2013). Overlap of epitopes recognized by anti-carbonic anhydrase I IgG in patients with malignancy-related aplastic anemia-like syndrome and in patients with aplastic anemia. Immunol. Lett. 153, 47–49. 10.1016/j.imlet.2013.07.006 PubMed DOI

Jansson S. (1994). The light harvesting chlorophyll A/B binding proteins. Biochim. Biophys. Acta 1184, 1–19. 10.1016/0005-2728(94)90148-1 PubMed DOI

Jones J. D. G., Dangl J. L. (2006). The plant immune system. Nature 444, 323–329. 10.1038/nature05286 PubMed DOI

Journet E. P., Neuburger M., Douce R. (1981). Role of glutamate-oxaloacetate transaminase and malate dehydrogenase in the regeneration of NAD for glycine oxidation by spinach leaf mitochondria. Plant Physiol. 67, 467–469. 10.1104/pp.67.3.467 PubMed DOI PMC

Katis N. I., Tsitsipis J. A., Lykouressis D. P., Papapanayotou A., Margaritopoulos J. T., Kokinis G. M., et al. (2006). Transmission of Zucchini yellow mosaic virus by colonizing and non-colonizing aphids in Greece and new aphid species vectors of the virus. J. Phytopathol. 154, 293–302 10.1111/j.1439-0434.2006.01096.x DOI

Klubicova K., Bercak M., Danchenko M., Skultety L., Rashydov N. M., Berezhna V. V., et al. . (2011). Agricultural recovery of a formerly radioactive area: I. Establishment of high-resolution quantitative protein map of mature flax seeds harvested from the remediated Chernobyl area. Phytochemistry 72, 1308–1315. 10.1016/j.phytochem.2010.11.010 PubMed DOI

Kobayashi K., Mochizuki N., Yoshimura N., Motohashi K., Hisabori T., Masuda T. (2008). Functional analysis of Arabidopsis thaliana isoforms of the Mg-chelatase CHLI subunit. Photochem. Photobiol. Sci. 7, 1188–1195. 10.1039/b802604c PubMed DOI

Lecoq H., Desbiez C. (2008). Watermelon mosaic virus and Zucchini yellow mosaic virus, in Encyclopedia of Virology, Vol. 5, 3rd Edn, eds Mahy B. W. J., Van Regenmortel M. H. V., Lecoq H. (Oxford: Elsevier; ), 433–440.

Lecoq H., Desbiez C. (2012). Viruses of cucurbit crops in the mediterranean region: an ever-changing picture, in Viruses and Virus Diseases of Vegetables in the Mediterranean Basin, eds Loebenstein G., Lecoq H. (San Diego, CA: Elsevier Academic Press Inc.), 67–126. PubMed

Maurino V. G., Saigo M., Andreo C. S., Drincovich M. F. (2001). Non-photosynthetic 'malic enzyme' from maize: a constituvely expressed enzyme that responds to plant defence inducers. Plant Mol. Biol. 45, 409–420. 10.1023/A:1010665910095 PubMed DOI

Mawassi M., Gera A. (2012). Controlling plant response to enviroment:viral diseases, in Plant Biotechnology and Agriculture: Prospects for the 21st Century, eds Altman A., Hasegawa P. M. (Oxford: Elsevier; ), 343–349.

Nurnberger T., Lipka V. (2005). Non-host resistance in plants: new insights into an old phenomenon. Mol. Plant Pathol. 6, 335–345. 10.1111/j.1364-3703.2005.00279.x PubMed DOI

Pachner M., Paris H. S., Lelley T. (2011). Genes for resistance to zucchini yellow mosaic in tropical pumpkin. J. Hered. 102, 330–335. 10.1093/jhered/esr006 PubMed DOI

Paris H. S. (1989). Historical records, origins, and development of the edible cultivar groups of Cucurbita pepo (Cucurbitaceae). Econ. Bot. 43, 423–443 10.1007/BF02935916 DOI

Paris H. S., Brown R. N. (2005). The genes of pumpkin and squash. Hortscience 40, 1620–1630.

Paris H. S., Cohen S. (2000). Oligogenic inheritance for resistance to Zucchini yellow mosaic virus in Cucurbita pepo. Ann. Appl. Biol. 136, 209–214 10.1111/j.1744-7348.2000.tb00027.x DOI

Peng L. W., Ma J. F., Chi W., Guo J. K., Zhu S. Y., Lu Q. T., et al. . (2006). Low PSII accumulation1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18, 955–969. 10.1105/tpc.105.037689 PubMed DOI PMC

Peterhansel C., Horst I., Niessen M., Blume C., Kebeish R., Kurkcuoglu S., et al. . (2010). Photorespiration. Arabidopsis Book 8:e0130. 10.1199/tab.0130 PubMed DOI PMC

Petriccione M., Di Cecco I., Arena S., Scaloni A., Scortichini M. (2013). Proteomic changes in Actinidia chinensis shoot during systemic infection with a pandemic Pseudomonas syringae pv. actinidiae strain. J. Proteomics 78, 461–476 10.1016/j.jprot.2012.10.014 PubMed DOI

Plucken H., Muller B., Grohmann D., Westhoff P., Eichacker L. A. (2002). The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Lett. 532, 85–90. 10.1016/S0014-5793(02)03634-7 PubMed DOI

Pontier D., Albrieux C., Joyard J., Lagrange T., Block M. A. (2007). Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis—effects on chloroplast development and on chloroplast-to-nucleus signaling. J. Biol. Chem. 282, 2297–2304. 10.1074/jbc.M610286200 PubMed DOI PMC

Pospisil P. (2009). Production of reactive oxygen species by photosystem II. Biochim. Biophys. Acta 1787, 1151–1160. 10.1016/j.bbabio.2009.05.005 PubMed DOI

Qi Y. F., Armbruster U., Schmitz-Linneweber C., Delannoy E., De Longevialle A. F., Ruhle T., et al. . (2012). Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts. J. Exp. Bot. 63, 1251–1270. 10.1093/jxb/err347 PubMed DOI PMC

Ravanel S., Gakiere B., Job D., Douce R. (1998). The specific features of methionine biosynthesis and metabolism in plants. Proc. Natl. Acad. Sci. U.S.A. 95, 7805–7812. 10.1073/pnas.95.13.7805 PubMed DOI PMC

Robinson C., Klosgen R. B. (1994). Targeting of proteins into and across the thylakoid membrane—a multitude of mechanisms. Plant Mol. Biol. 26, 15–24. 10.1007/BF00039516 PubMed DOI

Rodrigues S. P., Ventura J. A., Aguilar C., Nakayasu E. S., Almeida I. C., Fernandes P. M. B., et al. . (2011). Proteomic analysis of papaya (Carica papaya L.) displaying typical sticky disease symptoms. Proteomics 11, 2592–2602. 10.1002/pmic.201000757 PubMed DOI

Shand K., Theodoropoulos C., Stenzel D., Dale J. L., Harrison M. D. (2009). Expression of Potato virus Y cytoplasmic inclusion protein in tobacco results in disorganization of parenchyma cells, distortion of epidermal cells, and induces mitochondrial and chloroplast abnormalities, formation of membrane whorls and atypical lipid accumulation. Micron 40, 730–736. 10.1016/j.micron.2009.04.011 PubMed DOI

Simmons H. E., Dunham J. P., Zinn K. E., Munkvold G. P., Holmes E. C., Stephenson A. G. (2013). Zucchini yellow mosaic virus (ZYMV, Potyvirus): vertical transmission, seed infection and cryptic infections. Virus Res. 176, 259–264. 10.1016/j.virusres.2013.06.016 PubMed DOI PMC

Skultety L., Hajduch M., Flores-Ramirez G., Miernyk J. A., Ciampor F., Toman R., et al. . (2011). Proteomic comparison of virulent phase I and avirulent phase II of Coxiella burnetii, the causative agent of Q fever. J. Proteomics 74, 1974–1984. 10.1016/j.jprot.2011.05.017 PubMed DOI

Staneloni R. J., Jose Rodriguez-Batiller M., Casal J. J. (2008). Abscisic acid, high-light, and oxidative stress down-regulate a photosynthetic gene via a promoter motif not involved in phytochrome-mediated transcriptional regulation. Mol. Plant 1, 75–83 10.1093/mp/ssm007 PubMed DOI

Su S. Z., Liu Z. H., Chen C., Zhang Y., Wang X., Zhu L., et al. . (2010). Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22, 1373–1387. 10.1105/tpc.108.064212 PubMed DOI PMC

Suorsa M., Aro E.-M. (2007). Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosyn. Res. 93, 89–100. 10.1007/s11120-007-9154-4 PubMed DOI

Uvackova L., Skultety L., Bekesova S., McClain S., Hajduch M. (2013). MSE based multiplex protein analysis quantified important allergenic proteins and detected relevant peptides carrying known epitopes in wheat grain extracts. J. Proteome Res. 12, 4862–4869 10.1021/pr400336f PubMed DOI

Uvackova L., Skultety L., Bekesova S., McClain S., Hajduch M. (2014). The MSE-proteomic analysis of gliadins and glutenins in wheat grain identifies and quantifies proteins associated with celiac disease and baker's asthma. J. Proteomics 93, 65–73. 10.1016/j.jprot.2012.12.011 PubMed DOI

Vranova E., Inze D., Van Breusegem F. (2002). Signal transduction during oxidative stress. J. Exp. Bot. 53, 1227–1236. 10.1093/jexbot/53.372.1227 PubMed DOI

Wu L. J., Han Z. P., Wang S. X., Wang X. T., Sun A. G., Zu X. F., et al. . (2013a). Comparative proteomic analysis of the plant-virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J. Proteomics 89, 124–140. 10.1016/j.jprot.2013.06.005 PubMed DOI

Wu L. J., Wang S. X., Chen X., Wang X. T., Wu L. C., Zu X. F., et al. . (2013b). Proteomic and Phytohormone Analysis of the Response of Maize (Zea mays L.) Seedlings to Sugarcane Mosaic Virus. PLoS ONE 8:e70295. 10.1371/journal.pone.0070295 PubMed DOI PMC

Yang H., Huang Y., Zhi H., Yu D. (2011). Proteomics-based analysis of novel genes involved in response toward soybean mosaic virus infection. Mol. Biol. Rep. 38, 511–521 10.1007/s11033-010-0135-x PubMed DOI