{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:09:18Z","timestamp":1790831358956,"version":"4.1.0"},"reference-count":46,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,5,21]],"date-time":"2021-05-21T00:00:00Z","timestamp":1621555200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Russian Government","award":["14.W03.31.0003"],"award-info":[{"award-number":["14.W03.31.0003"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Plant-virus interactions are frequently influenced by elevated temperature, which often increases susceptibility to a virus, a scenario described for potato cultivar Chicago infected with potato virus Y (PVY). In contrast, other potato cultivars such as Gala may have similar resistances to PVY at both normal (22 \u00b0C) and high (28 \u00b0C) temperatures. To elucidate the mechanisms of temperature-independent antivirus resistance in potato, we analysed responses of Gala plants to PVY at different temperatures using proteomic, transcriptional and metabolic approaches. Here we show that in Gala, PVY infection generally upregulates the accumulation of major enzymes associated with the methionine cycle (MTC) independently of temperature, but that temperature (22 \u00b0C or 28 \u00b0C) may finely regulate what classes accumulate. The different sets of MTC-related enzymes that are up-regulated at 22 \u00b0C or 28 \u00b0C likely account for the significantly increased accumulation of S-adenosyl methionine (SAM), a key component of MTC which acts as a universal methyl donor in methylation reactions. In contrast to this, we found that in cultivar Chicago, SAM levels were significantly reduced which correlated with the enhanced susceptibility to PVY at high temperature. Collectively, these data suggest that MTC and its major transmethylation function determines resistance or susceptibility to PVY.<\/jats:p>","DOI":"10.3390\/v13060955","type":"journal-article","created":{"date-parts":[[2021,5,24]],"date-time":"2021-05-24T02:32:43Z","timestamp":1621823563000},"page":"955","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["The Resistance Responses of Potato Plants to Potato Virus Y Are Associated with an Increased Cellular Methionine Content and an Altered SAM:SAH Methylation Index"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8405-1862","authenticated-orcid":false,"given":"Nadezhda","family":"Spechenkova","sequence":"first","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, 117997 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5757-8271","authenticated-orcid":false,"given":"Igor A.","family":"Fesenko","sequence":"additional","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, 117997 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Mamaeva","sequence":"additional","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, 117997 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tatyana P.","family":"Suprunova","sequence":"additional","affiliation":[{"name":"Doka-Gene Technologies Ltd., Rogachevo, 141880 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia O.","family":"Kalinina","sequence":"additional","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, 117997 Moscow, Russia"},{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew J.","family":"Love","sequence":"additional","affiliation":[{"name":"The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Taliansky","sequence":"additional","affiliation":[{"name":"Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, 117997 Moscow, Russia"},{"name":"Doka-Gene Technologies Ltd., Rogachevo, 141880 Moscow, Russia"},{"name":"The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/B978-0-12-800098-4.00003-9","article-title":"Chapter Three\u2014Evolution and Emergence of Plant Viruses","volume":"Volume 88","author":"Maramorosch","year":"2014","journal-title":"Advances in Virus Research"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1111\/mpp.12322","article-title":"Antagonistic within-host interactions between plant viruses: Molecular basis and impact on viral and host fitness","volume":"17","author":"Syller","year":"2016","journal-title":"Mol. Plant Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.coviro.2016.06.013","article-title":"Dynamic cross-talk between host primary metabolism and viruses during infections in plants","volume":"19","author":"Llave","year":"2016","journal-title":"Curr. Opin. Virol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.pbi.2019.03.002","article-title":"The significance of methionine cycle enzymes in plant virus infections","volume":"50","author":"De","year":"2019","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1111\/mpp.13009","article-title":"Role of the methionine cycle in the temperature-sensitive responses of potato plants to potato virus Y","volume":"22","author":"Fesenko","year":"2021","journal-title":"Mol. Plant Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.tibs.2005.04.012","article-title":"RNA silencing","volume":"30","author":"Baulcombe","year":"2005","journal-title":"Trends Biochem. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1038\/nri2824","article-title":"RNA-based antiviral immunity","volume":"10","author":"Ding","year":"2010","journal-title":"Nat. Rev. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1038\/s41577-018-0071-x","article-title":"Small RNA-based antimicrobial immunity","volume":"19","author":"Guo","year":"2019","journal-title":"Nat. Rev. Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.tplants.2008.04.009","article-title":"Small RNAs in viral infection and host defense","volume":"13","author":"Mlotshwa","year":"2008","journal-title":"Trends Plant Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.coviro.2018.08.003","article-title":"Dissection of RNAi-based antiviral immunity in plants","volume":"32","author":"Yang","year":"2018","journal-title":"Curr. Opin. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1016\/j.cub.2005.07.029","article-title":"Methylation Protects miRNAs and siRNAs from a 3\u2032-End Uridylation Activity in Arabidopsis","volume":"15","author":"Li","year":"2005","journal-title":"Curr. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/tpj.13088","article-title":"Molecular insights into the function of the viral RNA silencing suppressor HCPro","volume":"85","author":"Ivanov","year":"2016","journal-title":"Plant J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1004","DOI":"10.1094\/MPMI-02-13-0037-R","article-title":"Effects of the Crinivirus Coat Protein\u2013Interacting Plant Protein SAHH on Post-Transcriptional RNA Silencing and Its Suppression","volume":"26","author":"Canto","year":"2013","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1104\/pp.15.00677","article-title":"Ethylene Response Factors: A Key Regulatory Hub in Hormone and Stress Signaling","volume":"169","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Torrance, L., and Talianksy, M.E. (2020). Potato Virus Y Emergence and Evolution from the Andes of South America to Become a Major Destructive Pathogen of Potato and Other Solanaceous Crops Worldwide. Viruses, 12.","DOI":"10.3390\/v12121430"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2582","DOI":"10.3389\/fmicb.2018.02582","article-title":"Interactive Responses of Potato (Solanum tuberosum L.) Plants to Heat Stress and Infection with Potato Virus Y","volume":"9","author":"Makarova","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1111\/j.1744-7348.1990.tb06594.x","article-title":"Resistance to potato virus Y and potato virus X in Solanurn brevidens","volume":"116","author":"Gibson","year":"1990","journal-title":"Ann. Appl. Biol."},{"key":"ref_18","unstructured":"Thiellement, H., Zivy, M., Damerval, C., and M\u00e9chin, V. (2007). Phenol Extraction of Proteins for Proteomic Studies of Recalcitrant Plant Tissues. Plant Proteomics: Methods and Protocols, Humana Press. Methods in Molecular Biology."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5347","DOI":"10.1021\/pr900634c","article-title":"iTRAQ Underestimation in Simple and Complex Mixtures: \u201cThe Good, the Bad and the Ugly\u201d","volume":"8","author":"Ow","year":"2009","journal-title":"J. Proteome Res."},{"key":"ref_20","unstructured":"(2021, April 12). STRING: Functional Protein Association Networks. Available online: https:\/\/string-db.org\/cgi\/input?sessionId=bqGWh48lnqym&input_page_show_search=on."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"D447","DOI":"10.1093\/nar\/gku1003","article-title":"STRING v10: Protein\u2013protein interaction networks, integrated over the tree of life","volume":"43","author":"Szklarczyk","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."},{"key":"ref_23","unstructured":"(2021, April 12). g:Profiler\u2014A Web Server for Functional Enrichment Analysis and Conversions of Gene Lists. Available online: https:\/\/biit.cs.ut.ee\/gprofiler\/gost."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"W191","DOI":"10.1093\/nar\/gkz369","article-title":"g:Profiler: A web server for functional enrichment analysis and conversions of gene lists (2019 update)","volume":"47","author":"Raudvere","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_25","unstructured":"(2021, April 12). Phytozome v12.1: Home, Available online: https:\/\/phytozome.jgi.doe.gov\/pz\/portal.html."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2907","DOI":"10.1093\/jxb\/eri285","article-title":"Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress","volume":"56","author":"Nicot","year":"2005","journal-title":"J. Exp. Bot."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Baebler, \u0160., Stare, K., Kova\u010d, M., Blejec, A., Prezelj, N., Stare, T., Kogov\u0161ek, P., Pompe-Novak, M., Rosahl, S., and Ravnikar, M. (2011). Dynamics of Responses in Compatible Potato\u2014Potato virus Y Interaction Are Modulated by Salicylic Acid. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0029009"},{"key":"ref_28","unstructured":"Van Rossum, G. (1995). Python Tutorial, Technical Report CS-R9526, Centrum voor Wiskunde en Informatica."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1111\/mpp.12533","article-title":"Chloroplast: The Trojan horse in plant\u2013virus interaction","volume":"19","author":"Bhattacharyya","year":"2018","journal-title":"Mol. Plant Pathol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3389\/fpls.2014.00143","article-title":"\u00ce\u00b2-catenin in plants and animals: Common players but different pathways","volume":"5","author":"Sharma","year":"2014","journal-title":"Front. Plant Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1836","DOI":"10.3389\/fpls.2018.01836","article-title":"Glutathione S-transferase enzymes in plant-pathogen interactions","volume":"9","author":"Gullner","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"512","DOI":"10.3389\/fpls.2013.00512","article-title":"Profilin as a regulator of the membrane-actin cytoskeleton interface in plant cells","volume":"4","author":"Sun","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1093\/jxb\/erx334","article-title":"The roles of membranes and associated cytoskeleton in plant virus replication and cell-to-cell movement","volume":"69","author":"Pitzalis","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"14463","DOI":"10.1073\/pnas.0506948102","article-title":"Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis","volume":"102","author":"Bozhkov","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_35","first-page":"88","article-title":"Therapeutic potentials of superoxide dismutase","volume":"12","author":"Younus","year":"2018","journal-title":"Int. J. Health Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1006\/abbi.1995.1078","article-title":"Methionine Biosynthesis in Higher Plants.II. Purification and Characterization of Cystathionine \u03b2-Lyase from Spinach Chloroplasts","volume":"316","author":"Droux","year":"1995","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"355","DOI":"10.3389\/fpls.2018.00355","article-title":"Modify the Histone to Win the Battle: Chromatin Dynamics in Plant\u2013Pathogen Interactions","volume":"9","author":"Piquerez","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1104\/pp.124.3.1121","article-title":"A Leaf Lipoxygenase of Potato Induced Specifically by Pathogen Infection","volume":"124","author":"Kolomiets","year":"2000","journal-title":"Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1034\/j.1399-3054.2001.1130401.x","article-title":"SustainingS-adenosyl-l-methionine-dependent methyltransferase activity in plant cells","volume":"113","author":"Moffatt","year":"2001","journal-title":"Physiol. Plant."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/ismej.2017.155","article-title":"Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale","volume":"12","author":"Bernardo","year":"2018","journal-title":"ISME J."},{"key":"ref_41","unstructured":"Vreugdenhil, D., Bradshaw, J., Gebhardt, C., Govers, F., Mackerron, D.K.L., Taylor, M.A., and Ross, H.A. (2007). Chapter 28\u2014Viruses: Economical Losses and Biotechnological Potential. Potato Biology and Biotechnology, Elsevier Science B.V."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1094\/PD-90-0073","article-title":"Effect of Potato virus Y on Yield of Three Potato Cultivars Grown under Different Nitrogen Levels","volume":"90","author":"Whitworth","year":"2006","journal-title":"Plant Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s11540-007-9031-8","article-title":"Resistance to Potato virus Y in a Multitrait Potato Breeding Scheme without Direct Selection in Each Generation","volume":"50","author":"Bradshaw","year":"2007","journal-title":"Potato Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"6142","DOI":"10.1093\/jxb\/eraa320","article-title":"Capsicum annum Hsp26.5 promotes defense responses against RNA viruses via ATAF2 but is hijacked as a chaperone for tobamovirus movement protein","volume":"71","author":"Foong","year":"2020","journal-title":"J. Exp. Bot."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1866","DOI":"10.1093\/molbev\/msaa091","article-title":"Viral Fitness Determines the Magnitude of Transcriptomic and Epigenomic Reprograming of Defense Responses in Plants","volume":"37","author":"Kogej","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"ref_46","first-page":"10","article-title":"BABA-Induced DNA Methylome Adjustment to Intergenerational Defense Priming in Potato to Phytophthora infestans","volume":"10","author":"Meller","year":"2019","journal-title":"Front. Plant Sci."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/955\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:05:35Z","timestamp":1760162735000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/955"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,21]]},"references-count":46,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["v13060955"],"URL":"https:\/\/doi.org\/10.3390\/v13060955","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,21]]}}}