{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T06:57:17Z","timestamp":1790578637681,"version":"4.1.0"},"reference-count":86,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T00:00:00Z","timestamp":1790121600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T00:00:00Z","timestamp":1790553600000},"content-version":"vor","delay-in-days":5,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"name":"Excellence Strategy of the German Federal and State Governments"},{"DOI":"10.13039\/501100008257","name":"Tarbiat Modares University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100008257","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Virol J"],"DOI":"10.1186\/s12985-026-03309-9","type":"journal-article","created":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T11:13:46Z","timestamp":1790162026000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Characterization of the C4 protein encoded by parsley yellow leaf curl virus"],"prefix":"10.1186","volume":"23","author":[{"given":"Hasan","family":"Zeitooni","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosa","family":"Lozano-Dur\u00e1n","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masoud","family":"Shams-Bakhsh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,9,23]]},"reference":[{"key":"3309_CR1","doi-asserted-by":"publisher","first-page":"8029","DOI":"10.1073\/pnas.88.18.8029","volume":"88","author":"DC Stenger","year":"1991","unstructured":"Stenger DC, Revington GN, Stevenson MC, Bisaro DM. Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc Natl Acad Sci U S A. 1991;88:8029\u201333. https:\/\/doi.org\/10.1073\/pnas.88.18.8029.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3309_CR2","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1038\/nrmicro3117","volume":"11","author":"L Hanley-Bowdoin","year":"2013","unstructured":"Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol. 2013;11:777\u201388. https:\/\/doi.org\/10.1038\/nrmicro3117.","journal-title":"Nat Rev Microbiol"},{"key":"3309_CR3","doi-asserted-by":"publisher","unstructured":"Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J et al. ICTV virus taxonomy profile: Geminiviridae. J Gen Virol. 2017;98:131\u20133. Available from: https:\/\/www.microbiologyresearch.org\/content\/journal\/jgv\/https:\/\/doi.org\/10.1099\/jgv.0.000738","DOI":"10.1099\/jgv.0.000738"},{"key":"3309_CR4","doi-asserted-by":"publisher","unstructured":"Rojas MR, Macedo MA, Maliano MR, Soto-Aguilar M, Souza JO, Briddon RW et al. World Management of Geminiviruses. Annu Rev Phytopathol. 2018;56:637\u201377. Available from: https:\/\/www.annualreviews.org\/doi\/https:\/\/doi.org\/10.1146\/annurev-phyto-080615-100327","DOI":"10.1146\/annurev-phyto-080615-100327"},{"key":"3309_CR5","doi-asserted-by":"publisher","unstructured":"Fiallo-Oliv\u00e9 E, Lett JM, Martin DP, Roumagnac P, Varsani A, Zerbini FM et al. ICTV Virus Taxonomy Profile: Geminiviridae 2021. J Gen Virol. 2021;102:1\u20132. Available from: https:\/\/www.microbiologyresearch.org\/content\/journal\/jgv\/https:\/\/doi.org\/10.1099\/jgv.0.001696","DOI":"10.1099\/jgv.0.001696"},{"key":"3309_CR6","doi-asserted-by":"publisher","unstructured":"Roumagnac P, Lett JM, Fiallo-Oliv\u00e9 E, Navas-Castillo J, Zerbini FM, Martin DP et al. Establishment of five new genera in the family Geminiviridae: Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus. Arch Virol. 2022;167:695\u2013710. Available from: https:\/\/doi.org\/10.1007\/s00705-021-05309-2","DOI":"10.1007\/s00705-021-05309-2"},{"key":"3309_CR7","doi-asserted-by":"crossref","unstructured":"Gong P, Tan H, Zhao S, Li H, Liu H, Ma Y et al. Geminiviruses encode additional small proteins with specific subcellular localizations and virulence function. Nat Commun. 2021;12:4278. Available from: https:\/\/www.nature.com\/articles\/s41467-021-24617-4","DOI":"10.1038\/s41467-021-24617-4"},{"key":"3309_CR8","doi-asserted-by":"publisher","first-page":"1804","DOI":"10.1093\/plcell\/koac019","volume":"34","author":"CW Chiu","year":"2022","unstructured":"Chiu CW, Li YR, Lin CY, Yeh HH, Liu MJ. Translation initiation landscape profiling reveals hidden open-reading frames required for the pathogenesis of tomato yellow leaf curl Thailand virus. Plant Cell. 2022;34:1804\u201321. https:\/\/doi.org\/10.1093\/plcell\/koac019.","journal-title":"Plant Cell"},{"key":"3309_CR9","doi-asserted-by":"publisher","unstructured":"Zhao S, Gong P, Ren Y, Liu H, Li H, Li F et al. The novel C5 protein from tomato yellow leaf curl virus is a virulence factor and suppressor of gene silencing. Stress Biol. 2022;2:19. Available from: https:\/\/doi.org\/10.1007\/s44154-022-00044-3","DOI":"10.1007\/s44154-022-00044-3"},{"key":"3309_CR10","doi-asserted-by":"publisher","unstructured":"Wang Z, Wang Y, Lozano-Duran R, Hu T, Zhou X. Identification of a novel C6 protein encoded by tomato leaf curl China virus. Phytopathol Res. 2022;4:46. Available from: https:\/\/phytopatholres.biomedcentral.com\/articles\/https:\/\/doi.org\/10.1186\/s42483-022-00151-z","DOI":"10.1186\/s42483-022-00151-z"},{"key":"3309_CR11","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1093\/plphys\/kiad338","volume":"193","author":"S Zhao","year":"2023","unstructured":"Zhao S, Gong P, Liu J, Liu H, Lozano-Dur\u00e1n R, Zhou X, et al. Geminivirus C5 proteins mediate formation of virus complexes at plasmodesmata for viral intercellular movement. Plant Physiol. 2023;193:322\u201338. https:\/\/doi.org\/10.1093\/plphys\/kiad338.","journal-title":"Plant Physiol"},{"key":"3309_CR12","doi-asserted-by":"crossref","unstructured":"Liu H, Chang Z, Zhao S, Gong P, Zhang M, Lozano-Dur\u00e1n R et al. Functional identification of a novel C7 protein of tomato yellow leaf curl virus. Virology. 2023;585:117\u201326. Available from: https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0042682223001162","DOI":"10.1016\/j.virol.2023.05.011"},{"key":"3309_CR13","doi-asserted-by":"publisher","unstructured":"Li F, Jia M, Wang A. Hidden viral proteins: How powerful are they? Evans MJ, editor. PLoS Pathog. 2024;20:e1011905. Available from: https:\/\/doi.org\/10.1371\/journal.ppat.1011905","DOI":"10.1371\/journal.ppat.1011905"},{"key":"3309_CR14","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1111\/mpp.12032","volume":"14","author":"VN Fondong","year":"2013","unstructured":"Fondong VN. Geminivirus protein structure and function. Mol Plant Pathol. 2013;14:635\u201349. https:\/\/doi.org\/10.1111\/mpp.12032.","journal-title":"Mol Plant Pathol"},{"key":"3309_CR15","doi-asserted-by":"publisher","first-page":"1707","DOI":"10.1111\/pce.14008","volume":"44","author":"X Liu","year":"2021","unstructured":"Liu X, Huang W, Zhai Z, Ye T, Yang C, Lai J. Protein modification: a critical modulator in the interaction between geminiviruses and host plants. Plant Cell Environ. 2021;44:1707\u201315. https:\/\/doi.org\/10.1111\/pce.14008.","journal-title":"Plant Cell Environ"},{"key":"3309_CR16","doi-asserted-by":"crossref","unstructured":"Hasanvand V, Heydanejad J, Massumi H, Kleinow T, Jeske H, Varsani A. Isolation and characterization of a novel geminivirus from parsley. Virus Res. 2020;286:198056. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S0168170220302598","DOI":"10.1016\/j.virusres.2020.198056"},{"key":"3309_CR17","doi-asserted-by":"publisher","DOI":"10.1186\/s12870-026-09617-0","volume":"26","author":"H Zeitooni","year":"2026","unstructured":"Zeitooni H, Medina-Puche L, Lozano-Dur\u00e1n R, Shams-Bakhsh M. The divergent V2 protein encoded by parsley yellow leaf curl virus is a suppressor of transcriptional and post-transcriptional gene silencing and a potential symptom determinant. BMC Plant Biol. 2026;26:1302. https:\/\/doi.org\/10.1186\/s12870-026-09617-0.","journal-title":"BMC Plant Biol"},{"key":"3309_CR18","doi-asserted-by":"publisher","DOI":"10.1007\/s00705-024-05984-x","volume":"169","author":"K Nichkerdar","year":"2024","unstructured":"Nichkerdar K, Heydarnejad J, Massumi H. Vector transmission of parsley yellow leaf curl virus by the leafhopper Austroagallia sinuata. Arch Virol. 2024;169:93. https:\/\/doi.org\/10.1007\/s00705-024-05984-x.","journal-title":"Arch Virol"},{"key":"3309_CR19","doi-asserted-by":"publisher","unstructured":"Mei Y, Zhang F, Wang M, Li F, Wang Y, Zhou X. Divergent Symptoms Caused by Geminivirus-Encoded C4 Proteins Correlate with Their Ability To Bind NbSK\u03b7. Sandri-Goldin RM, editor. J Virol. 2020;94:1\u20136. Available from: https:\/\/www.frontiersin.org\/journals\/microbiology\/articles\/https:\/\/doi.org\/10.3389\/fmicb.2020.00878","DOI":"10.3389\/fmicb.2020.00878"},{"key":"3309_CR20","doi-asserted-by":"publisher","unstructured":"Medina-Puche L, Or\u00edlio AF, Zerbini FM, Lozano-Dur\u00e1n R. Small but mighty: Functional landscape of the versatile geminivirus-encoded C4 protein. Wang X, editor. PLOS Pathog. 2021;17:1\u201315. Available from: https:\/\/doi.org\/10.1371\/journal.ppat.1009915","DOI":"10.1371\/journal.ppat.1009915"},{"key":"3309_CR21","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1013798","volume":"22","author":"S Pan","year":"2026","unstructured":"Pan S, Wei H, Dr\u00f6st F, Fenn A, Kamal N, Lozano-Dur\u00e1n R. Viral proteins as discovery tools for cell biology: the case of the geminivirus-encoded C4. PLoS Pathog. 2026;22:e1013798. https:\/\/doi.org\/10.1371\/journal.ppat.1013798.","journal-title":"PLoS Pathog"},{"key":"3309_CR22","doi-asserted-by":"publisher","first-page":"9487","DOI":"10.1128\/jvi.78.17.9487-9498.2004","volume":"78","author":"R Vanitharani","year":"2004","unstructured":"Vanitharani R, Chellappan P, Pita JS, Fauquet CM. Differential Roles of AC2 and AC4 of Cassava Geminiviruses in Mediating Synergism and Suppression of Posttranscriptional Gene Silencing. J Virol. 2004;78:9487\u201398. https:\/\/doi.org\/10.1128\/jvi.78.17.9487-9498.2004.","journal-title":"J Virol."},{"key":"3309_CR23","doi-asserted-by":"publisher","first-page":"10381","DOI":"10.1073\/pnas.0504439102","volume":"102","author":"P Chellappan","year":"2005","unstructured":"Chellappan P, Vanitharani R, Fauquet CM. MicroRNA-binding viral protein interferes with Arabidopsis development. Proc Natl Acad Sci U S A. 2005;102:10381\u20136. https:\/\/doi.org\/10.1073\/pnas.0504439102.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3309_CR24","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1007\/s11103-009-9506-x","volume":"71","author":"SC Dogra","year":"2009","unstructured":"Dogra SC, Eini O, Rezaian MA, Randles JW. A novel shaggy-like kinase interacts with the tomato leaf curl virus pathogenicity determinant C4 protein. Plant Mol Biol. 2009;71:25\u201338. https:\/\/doi.org\/10.1007\/s11103-009-9506-x.","journal-title":"Plant Mol Biol"},{"key":"3309_CR25","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1094\/MPMI-01-11-0001","volume":"24","author":"I Amin","year":"2011","unstructured":"Amin I, Hussain K, Akbergenov R, Yadav JS, Qazi J, Mansoor S, et al. Suppressors of RNA silencing encoded by the components of the cotton leaf curl begomovirus-betasatellite complex. Mol Plant-Microbe Interact. 2011;24:973\u201383. https:\/\/doi.org\/10.1094\/MPMI-01-11-0001.","journal-title":"Mol Plant-Microbe Interact"},{"key":"3309_CR26","doi-asserted-by":"publisher","unstructured":"Luna AP, Morilla G, Voinnet O, Bejarano ER. Functional analysis of gene-silencing suppressors from tomato yellow leaf curl disease viruses. Mol Plant-Microbe Interact. 2012;25:1294\u2013306. Available from: https:\/\/apsjournals.apsnet.org\/doi\/https:\/\/doi.org\/10.1094\/MPMI-04-12-0094-R","DOI":"10.1094\/MPMI-04-12-0094-R"},{"key":"3309_CR27","doi-asserted-by":"publisher","unstructured":"Xie Y, Zhao L, Jiao X, Jiang T, Gong H, Wang B et al. A recombinant begomovirus resulting from exchange of the C4 gene. J Gen Virol. 2013;94:1896\u2013907. Available from: https:\/\/www.microbiologyresearch.org\/content\/journal\/jgv\/https:\/\/doi.org\/10.1099\/vir.0.053181-0","DOI":"10.1099\/vir.0.053181-0"},{"key":"3309_CR28","doi-asserted-by":"publisher","first-page":"e1007282","DOI":"10.1371\/journal.ppat.1007282","volume":"14","author":"A Ismayil","year":"2018","unstructured":"Ismayil A, Haxim Y, Wang Y, Li H, Qian L, Han T, et al. Cotton Leaf Curl Multan virus C4 protein suppresses both transcriptional and post-transcriptional gene silencing by interacting with SAM synthetase. PLoS Pathog. 2018;14:e1007282. https:\/\/doi.org\/10.1371\/journal.ppat.1007282.","journal-title":"PLoS Pathog."},{"key":"3309_CR29","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1007207","volume":"14","author":"AV Carluccio","year":"2018","unstructured":"Carluccio AV, Prigigallo MI, Rosas-Diaz T, Lozano-Duran R, Stavolone L. S-acylation mediates Mungbean yellow mosaic virus AC4 localization to the plasma membrane and in turns gene silencing suppression. PLoS Pathog. 2018;14:e1007207. https:\/\/doi.org\/10.1371\/journal.ppat.1007207.","journal-title":"PLoS Pathog"},{"key":"3309_CR30","doi-asserted-by":"publisher","unstructured":"Mei Y, Wang Y, Li F, Zhou X. The C4 protein encoded by tomato leaf curl Yunnan virus reverses transcriptional gene silencing by interacting with NbDRM2 and impairing its DNA-binding ability. Dinesh-Kumar SP, editor. PLoS Pathog. 2020;16:e1008829. Available from: https:\/\/doi.org\/10.1371\/journal.ppat.1008829","DOI":"10.1371\/journal.ppat.1008829"},{"key":"3309_CR31","doi-asserted-by":"crossref","unstructured":"Jupin I, De Kouchkovsky F, Jouanneau F, Gronenborn B. Movement of tomato yellow leaf curl geminivirus (TYLCV): Involvement of the protein encoded by ORF C4. Virology. 1994 [cited 2025 Aug 26];204:82\u201390. Available from: https:\/\/www.sciencedirect.com\/science\/article\/abs\/pii\/S0042682284715121","DOI":"10.1006\/viro.1994.1512"},{"key":"3309_CR32","doi-asserted-by":"crossref","unstructured":"Rojas MR, Jiang H, Salati R, Xoconostle-C\u00e1zares B, Sudarshana MR, Lucas WJ et al. Functional analysis of proteins involved in movement of the monopartite begomovirus, Tomato yellow leaf curl virus. Virology. 2001;291:110\u201325. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S0042682201911948","DOI":"10.1006\/viro.2001.1194"},{"key":"3309_CR33","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0011280","volume":"5","author":"K Teng","year":"2010","unstructured":"Teng K, Chen H, Lai J, Zhang Z, Fang Y, Xia R, et al. Involvement of C4 protein of beet severe curly top virus (Family Geminiviridae) in virus movement. PLoS One. 2010;5:e11280. https:\/\/doi.org\/10.1371\/journal.pone.0011280.","journal-title":"PLoS One"},{"key":"3309_CR34","doi-asserted-by":"crossref","unstructured":"Rigden JE, Krake LR, Rezaian MA, Dry IB. ORF C4 of tomato leaf curl geminivirus is a determinant of symptom severity. Virology. 1994 [cited 2025 Aug 26];204:847\u201350. Available from: https:\/\/www.sciencedirect.com\/science\/article\/abs\/pii\/S0042682284716060?via%3Dihub","DOI":"10.1006\/viro.1994.1606"},{"key":"3309_CR35","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1007\/s00709-009-0086-z","volume":"239","author":"K Mills-Lujan","year":"2010","unstructured":"Mills-Lujan K, Deom CM. Geminivirus C4 protein alters Arabidopsis development. Protoplasma. 2010;239:95\u2013110. https:\/\/doi.org\/10.1007\/s00709-009-0086-z.","journal-title":"Protoplasma"},{"key":"3309_CR36","doi-asserted-by":"crossref","unstructured":"Zhan B, Zhao W, Li S, Yang X, Zhou X. Functional scanning of apple geminivirus proteins as symptom determinants and suppressors of posttranscriptional gene silencing. Viruses. 2018;10:488. Available from: https:\/\/www.mdpi.com\/1999-4915\/10\/9\/488","DOI":"10.3390\/v10090488"},{"key":"3309_CR37","doi-asserted-by":"publisher","first-page":"4459","DOI":"10.1093\/jxb\/ery228","volume":"69","author":"H Li","year":"2018","unstructured":"Li H, Zeng R, Chen Z, Liu X, Cao Z, Xie Q, et al. S-acylation of a geminivirus C4 protein is essential for regulating the CLAVATA pathway in symptom determination. J Exp Bot. 2018;69:4459\u201368. https:\/\/doi.org\/10.1093\/jxb\/ery228.","journal-title":"J Exp Bot"},{"key":"3309_CR38","doi-asserted-by":"publisher","first-page":"2817","DOI":"10.1093\/jxb\/eraa053","volume":"71","author":"R Zeng","year":"2020","unstructured":"Zeng R, Liu X, Li H, Wu S, Huang W, Zhai Z, et al. Danger peptide signaling enhances internalization of a geminivirus symptom determinant in plant cells during infection. J Exp Bot. 2020;71:2817\u201327. https:\/\/doi.org\/10.1093\/jxb\/eraa053.","journal-title":"J Exp Bot."},{"key":"3309_CR39","doi-asserted-by":"crossref","unstructured":"Gao M, Aguilar E, G\u00f3mez BG, Medina-Puche L, Fan P, Ontiveros I et al. A plant virus causes symptoms through the deployment of a host-mimicking protein domain to attract the insect vector. Mol Plant. 2025;18:1029\u201346. Available from: https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1674205225001704","DOI":"10.1016\/j.molp.2025.05.011"},{"key":"3309_CR40","doi-asserted-by":"publisher","unstructured":"Mei Y, Ma Z, Wang Y, Zhou X. Geminivirus C4 antagonizes the HIR1-mediated hypersensitive response by inhibiting the HIR1 self-interaction and promoting degradation of the protein. New Phytol. 2020;225:1311\u201326. Available from: https:\/\/nph.onlinelibrary.wiley.com\/doi\/https:\/\/doi.org\/10.1111\/nph.16208","DOI":"10.1111\/nph.16208"},{"key":"3309_CR41","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1111\/j.1365-313X.2008.03737.x","volume":"57","author":"J Lai","year":"2009","unstructured":"Lai J, Chen H, Teng K, Zhao Q, Zhang Z, Li Y, et al. RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle. Plant J. 2009;57:905\u201317. https:\/\/doi.org\/10.1111\/j.1365-313X.2008.03737.x.","journal-title":"Plant J"},{"key":"3309_CR42","doi-asserted-by":"publisher","first-page":"1377","DOI":"10.1007\/s00299-010-0923-8","volume":"29","author":"J Park","year":"2010","unstructured":"Park J, Hwang HS, Buckley KJ, Park JB, Auh CK, Kim DG, et al. C4 protein of Beet severe curly top virus is a pathomorphogenetic factor in Arabidopsis. Plant Cell Rep. 2010;29:1377\u201389. https:\/\/doi.org\/10.1007\/s00299-010-0923-8.","journal-title":"Plant Cell Rep."},{"key":"3309_CR43","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0122356","volume":"10","author":"K Mills-Lujan","year":"2015","unstructured":"Mills-Lujan K, Andrews DL, Chou CW, Deom CM. The roles of phosphorylation and SHAGGY-like protein kinases in geminivirus C4 protein induced hyperplasia. PLoS One. 2015;10:e0122356. https:\/\/doi.org\/10.1371\/journal.pone.0122356.","journal-title":"PLoS One"},{"key":"3309_CR44","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1006789","volume":"14","author":"Y Mei","year":"2018","unstructured":"Mei Y, Yang X, Huang C, Zhang X, Zhou X. Tomato leaf curl Yunnan virus-encoded C4 induces cell division through enhancing stability of Cyclin D 1.1 via impairing NbSK\u03b7 -mediated phosphorylation in Nicotiana benthamiana. PLoS Pathog. 2018;14:e1006789. https:\/\/doi.org\/10.1371\/journal.ppat.1006789.","journal-title":"PLoS Pathog"},{"key":"3309_CR45","doi-asserted-by":"publisher","first-page":"1388","DOI":"10.1073\/pnas.1715556115","volume":"115","author":"T Rosas-Diaz","year":"2018","unstructured":"Rosas-Diaz T, Zhang D, Fan P, Wang L, Ding X, Jiang Y, et al. A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi. Proc Natl Acad Sci U S A. 2018;115:1388\u201393. https:\/\/doi.org\/10.1073\/pnas.1715556115.","journal-title":"Proc Natl Acad Sci U S A."},{"key":"3309_CR46","doi-asserted-by":"crossref","unstructured":"Garnelo G\u00f3mez B, Zhang D, Rosas-D\u00edaz T, Wei Y, Macho AP, Lozano-Dur\u00e1n R. The C4 Protein from Tomato Yellow Leaf Curl Virus Can Broadly Interact with Plant Receptor-Like Kinases. Viruses. 2019;11:1009. Available from: https:\/\/www.mdpi.com\/1999-4915\/11\/11\/1009","DOI":"10.3390\/v11111009"},{"key":"3309_CR47","doi-asserted-by":"publisher","unstructured":"Mei Y, Wang Y, Hu T, He Z, Zhou X. The C4 protein encoded by Tomato leaf curl Yunnan virus interferes with mitogen-activated protein kinase cascade-related defense responses through inhibiting the dissociation of the ERECTA\/BKI1 complex. New Phytol. 2021;231:747\u201362. Available from: https:\/\/nph.onlinelibrary.wiley.com\/doi\/https:\/\/doi.org\/10.1111\/nph.17387","DOI":"10.1111\/nph.17387"},{"key":"3309_CR48","doi-asserted-by":"crossref","unstructured":"Piroux N, Saunders K, Page A, Stanley J. Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggy-related protein kinase AtSK\u03b7, a component of the brassinosteroid signalling pathway. Virology. 2007;362:428\u201340. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S0042682206009305","DOI":"10.1016\/j.virol.2006.12.034"},{"key":"3309_CR49","doi-asserted-by":"publisher","unstructured":"Bi H, Fan W, Zhang P. C4 Protein of Sweet Potato Leaf Curl Virus Regulates Brassinosteroid Signaling Pathway through Interaction with AtBIN2 and Affects Male Fertility in Arabidopsis. Front Plant Sci. 2017;8:1\u201315. Available from: https:\/\/www.frontiersin.org\/journals\/plant-science\/articles\/https:\/\/doi.org\/10.3389\/fpls.2017.01689","DOI":"10.3389\/fpls.2017.01689"},{"key":"3309_CR50","doi-asserted-by":"publisher","first-page":"1109","DOI":"10.1016\/j.cell.2020.07.020","volume":"182","author":"L Medina-Puche","year":"2020","unstructured":"Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, et al. A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell. 2020;182:1109-1124.e25. https:\/\/doi.org\/10.1016\/j.cell.2020.07.020.","journal-title":"Cell"},{"key":"3309_CR51","doi-asserted-by":"publisher","DOI":"10.1007\/s00425-020-03452-9","volume":"252","author":"T Vinutha","year":"2020","unstructured":"Vinutha T, Vanchinathan S, Bansal N, Kumar G, Permar V, Watts A, et al. Tomato auxin biosynthesis\/signaling is reprogrammed by the geminivirus to enhance its pathogenicity. Planta. 2020;252:51. https:\/\/doi.org\/10.1007\/s00425-020-03452-9.","journal-title":"Planta"},{"key":"3309_CR52","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1010217","volume":"18","author":"P Li","year":"2022","unstructured":"Li P, Guo L, Lang X, Li M, Wu G, Wu R, et al. Geminivirus C4 proteins inhibit GA signaling via prevention of NbGAI degradation, to promote viral infection and symptom development in N. benthamiana. PLoS Pathog. 2022;18:e1010217. https:\/\/doi.org\/10.1371\/journal.ppat.1010217.","journal-title":"PLoS Pathog"},{"key":"3309_CR53","doi-asserted-by":"publisher","first-page":"1121","DOI":"10.1111\/pbi.13280","volume":"18","author":"M Corrales-Guti\u00e9rrez","year":"2020","unstructured":"Corrales-Guti\u00e9rrez M, Medina-Puche L, Yu Y, Wang L, Ding X, Luna AP, et al. The C4 protein from the geminivirus Tomato yellow leaf curl virus confers drought tolerance in Arabidopsis through an ABA-independent mechanism. Plant Biotechnol J. 2020;18:1121\u20133. https:\/\/doi.org\/10.1111\/pbi.13280.","journal-title":"Plant Biotechnol J."},{"key":"3309_CR54","doi-asserted-by":"publisher","unstructured":"Pagliarani C, Moine A, Chitarra W, Nerva L, Catoni M, Tavazza R et al. The C4 protein of tomato yellow leaf curl Sardinia virus primes drought tolerance in tomato through morphological adjustments. Hortic Res. 2022;9:uhac164. Available from: https:\/\/doi.org\/10.1093\/hr\/uhac164","DOI":"10.1093\/hr\/uhac164"},{"key":"3309_CR55","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1094\/MPMI-20-4-0380","volume":"20","author":"VN Fondong","year":"2007","unstructured":"Fondong VN, Reddy RVC, Lu C, Hankoua B, Felton C, Czymmek K, et al. The consensus N-myristoylation motif of a geminivirus AC4 protein is required for membrane binding and pathogenicity. Mol Plant-Microbe Interact. 2007;20:380\u201391. https:\/\/doi.org\/10.1094\/MPMI-20-4-0380.","journal-title":"Mol Plant-Microbe Interact."},{"key":"3309_CR56","doi-asserted-by":"publisher","unstructured":"Mei Y, Wang Y, Hu T, Yang X, Lozano-Duran R, Sunter G et al. Nucleocytoplasmic Shuttling of Geminivirus C4 Protein Mediated by Phosphorylation and Myristoylation Is Critical for Viral Pathogenicity. Mol Plant. 2018;11:1466\u201381. Available from: https:\/\/doi.org\/10.1016\/j.molp.2018.10.004","DOI":"10.1016\/j.molp.2018.10.004"},{"key":"3309_CR57","doi-asserted-by":"publisher","unstructured":"Li Z, Du Z, Tang Y, She X, Wang X, Zhu Y et al. C4, the Pathogenic Determinant of Tomato Leaf Curl Guangdong Virus, May Suppress Post-transcriptional Gene Silencing by Interacting With BAM1 Protein. Front Microbiol. 2020;11:1\u201314. Available from: https:\/\/www.frontiersin.org\/journals\/microbiology\/articles\/https:\/\/doi.org\/10.3389\/fmicb.2020.00851","DOI":"10.3389\/fmicb.2020.00851"},{"key":"3309_CR58","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1007\/s44154-024-00166-w","volume":"4","author":"Y Zhao","year":"2024","unstructured":"Zhao Y, Li Z, Wang Z, Huang L, Li G, Liu X, et al. Improvement of plant resistance to geminiviruses via protein de-S-acylation. Stress Biol. 2024;4:23. https:\/\/doi.org\/10.1007\/s44154-024-00166-w.","journal-title":"Stress Biol."},{"key":"3309_CR59","doi-asserted-by":"crossref","unstructured":"Voinnet O, Baulcombe DC. Systemic signalling in gene silencing. Nature. 1997;389:553. Available from: https:\/\/www.nature.com\/articles\/39215","DOI":"10.1038\/39215"},{"key":"3309_CR60","doi-asserted-by":"crossref","unstructured":"Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng. 2007;104:34\u201341. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S1389172307701160","DOI":"10.1263\/jbb.104.34"},{"key":"3309_CR61","doi-asserted-by":"publisher","first-page":"3718","DOI":"10.1073\/pnas.97.7.3718","volume":"97","author":"SR Cutler","year":"2000","unstructured":"Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci U S A. 2000;97:3718\u201323. https:\/\/doi.org\/10.1073\/pnas.97.7.3718.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3309_CR62","doi-asserted-by":"publisher","unstructured":"Postma J, Liebrand TWH, Bi G, Evrard A, Bye RR, Mbengue M et al. Avr4 promotes Cf-4 receptor-like protein association with the BAK1\/SERK3 receptor-like kinase to initiate receptor endocytosis and plant immunity. New Phytol. 2016;210:627\u201342. Available from: https:\/\/nph.onlinelibrary.wiley.com\/doi\/https:\/\/doi.org\/10.1111\/nph.13802","DOI":"10.1111\/nph.13802"},{"key":"3309_CR63","doi-asserted-by":"publisher","first-page":"e48938","DOI":"10.1371\/journal.pone.0048938","volume":"7","author":"H Nausch","year":"2012","unstructured":"Nausch H, Mikschofsky H, Koslowski R, Meyer U, Broer I, Huckauf J. High-Level Transient Expression of ER-Targeted Human Interleukin 6 in Nicotiana benthamiana. PLoS One. 2012;7:e48938. https:\/\/doi.org\/10.1371\/journal.pone.0048938.","journal-title":"PLoS One."},{"key":"3309_CR64","doi-asserted-by":"crossref","unstructured":"Wang L, Ding X, Xiao J, Jim\u00e9nez-G\u03ccngora T, Liu R, Lozano-Dur\u00e1n R. Inference of a geminivirus\u2013host protein\u2013protein interaction network through affinity purification and mass spectrometry analysis. Viruses. 2017;9:275. https:\/\/www.mdpi.com\/1999-4915\/9\/10\/275","DOI":"10.3390\/v9100275"},{"key":"3309_CR65","doi-asserted-by":"publisher","unstructured":"Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C, Roy S et al. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science. 2014;343:1509\u201312. Available from: https:\/\/www.science.org\/doi\/https:\/\/doi.org\/10.1126\/science.1248849","DOI":"10.1126\/science.1248849"},{"key":"3309_CR66","doi-asserted-by":"crossref","unstructured":"O\u00f1ate-S\u00e1nchez L, Verdonk JC. Citrate-Citric Acid RNA Isolation (CiAR) for Fast, Low-Cost, and Reliable RNA Extraction from Multiple Plant Species and Tissues. Curr Protoc. 2021;1:e298. Available from: http:\/\/europepmc.org\/abstract\/MED\/34874606","DOI":"10.1002\/cpz1.298"},{"key":"3309_CR67","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0046451","volume":"7","author":"D Liu","year":"2012","unstructured":"Liu D, Shi L, Han C, Yu J, Li D, Zhang Y. Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS One. 2012;7:e46451. https:\/\/doi.org\/10.1371\/journal.pone.0046451.","journal-title":"PLoS One"},{"key":"3309_CR68","doi-asserted-by":"publisher","unstructured":"Emanuelsson O, Nielsen H, Heijne G, Von. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 1999;8:978\u201384. Available from: https:\/\/onlinelibrary.wiley.com\/doi\/https:\/\/doi.org\/10.1110\/ps.8.5.978","DOI":"10.1110\/ps.8.5.978"},{"key":"3309_CR69","doi-asserted-by":"crossref","unstructured":"Maurer-Stroh S, Eisenhaber B, Eisenhaber F. N-terminal N-myristoylation of proteins: Prediction of substrate proteins from amino acid sequence. J Mol Biol. 2002;317:541\u201357. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S0022283602954264","DOI":"10.1006\/jmbi.2002.5426"},{"key":"3309_CR70","doi-asserted-by":"publisher","first-page":"1836","DOI":"10.1093\/bib\/bbaa038","volume":"22","author":"W Ning","year":"2021","unstructured":"Ning W, Jiang P, Guo Y, Wang C, Tan X, Zhang W, et al. GPS-Palm: a deep learning-based graphic presentation system for the prediction of S-palmitoylation sites in proteins. Brief Bioinform. 2021;22:1836\u201347. https:\/\/doi.org\/10.1093\/bib\/bbaa038.","journal-title":"Brief Bioinform"},{"key":"3309_CR71","doi-asserted-by":"publisher","first-page":"10171","DOI":"10.1073\/pnas.0900604106","volume":"106","author":"S Kosugi","year":"2009","unstructured":"Kosugi S, Hasebe M, Tomita M, Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009;106:10171\u20136. https:\/\/doi.org\/10.1073\/pnas.0900604106.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3309_CR72","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1038\/cr.2009.6","volume":"19","author":"J Ren","year":"2009","unstructured":"Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. DOG 1.0: illustrator of protein domain structures. Cell Res. 2009;19:271\u20133. https:\/\/doi.org\/10.1038\/cr.2009.6.","journal-title":"Cell Res"},{"key":"3309_CR73","doi-asserted-by":"publisher","first-page":"1357","DOI":"10.1093\/bioinformatics\/btu826","volume":"31","author":"D Xu","year":"2015","unstructured":"Xu D, Marquis K, Pei J, Fu SC, Ca\u0287atay T, Grishin NV, et al. LocNES: A computational tool for locating classical NESs in CRM1 cargo proteins. Bioinformatics. 2015;31:1357\u201365. https:\/\/doi.org\/10.1093\/bioinformatics\/btu826.","journal-title":"Bioinformatics."},{"key":"3309_CR74","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0108277","volume":"9","author":"BM Muhire","year":"2014","unstructured":"Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One. 2014;9:e108277. https:\/\/doi.org\/10.1371\/journal.pone.0108277.","journal-title":"PLoS One"},{"key":"3309_CR75","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msae263","volume":"41","author":"S Kumar","year":"2024","unstructured":"Kumar S, Stecher G, Suleski M, Sanderford M, Sharma S, Tamura K. MEGA12: molecular evolutionary genetic analysis version 12 for adaptive and green computing. Mol Biol Evol. 2024;41:msae263. https:\/\/doi.org\/10.1093\/molbev\/msae263.","journal-title":"Mol Biol Evol"},{"key":"3309_CR76","doi-asserted-by":"publisher","first-page":"1669","DOI":"10.1093\/bioinformatics\/btq243","volume":"26","author":"T Junier","year":"2010","unstructured":"Junier T, Zdobnov EM. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics. 2010;26:1669\u201370. https:\/\/doi.org\/10.1093\/bioinformatics\/btq243.","journal-title":"Bioinformatics."},{"key":"3309_CR77","doi-asserted-by":"publisher","first-page":"W78","DOI":"10.1093\/nar\/gkae268","volume":"52","author":"I Letunic","year":"2024","unstructured":"Letunic I, Bork P. Interactive Tree of Life (iTOL) v6: Recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 2024;52:W78-82. https:\/\/doi.org\/10.1093\/nar\/gkae268.","journal-title":"Nucleic Acids Res."},{"key":"3309_CR78","doi-asserted-by":"publisher","unstructured":"Chodon A, Medina-Puche L, Wei H, Pandi G, Lozano-Dur\u00e1n R. Characterization of the C4 proteins encoded by okra-infecting geminiviruses in India. BMC Plant Biol. 2026; Available from: https:\/\/link.springer.com\/https:\/\/doi.org\/10.1186\/s12870-026-09348-2","DOI":"10.1186\/s12870-026-09348-2"},{"key":"3309_CR79","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1007\/s00705-021-05338-x","volume":"167","author":"R Devendran","year":"2022","unstructured":"Devendran R, Namgial T, Reddy KK, Kumar M, Zarreen F, Chakraborty S. Insights into the multifunctional roles of geminivirus-encoded proteins in pathogenesis. Arch Virol. 2022;167:307\u201326. https:\/\/doi.org\/10.1007\/s00705-021-05338-x.","journal-title":"Arch Virol."},{"key":"3309_CR80","doi-asserted-by":"publisher","DOI":"10.1002\/biot.202300736","volume":"19","author":"H Kamal","year":"2024","unstructured":"Kamal H, Zafar MM, Razzaq A, Parvaiz A, Ercisli S, Qiao F, et al. Functional role of geminivirus encoded proteins in the host: past and present. Biotechnol J. 2024;19:2300736. https:\/\/doi.org\/10.1002\/biot.202300736.","journal-title":"Biotechnol J"},{"key":"3309_CR81","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.molp.2018.12.006","volume":"12","author":"VN Fondong","year":"2019","unstructured":"Fondong VN. The Ever-Expanding Role of C4\/AC4 in Geminivirus Infection: Punching above Its Weight? Mol Plant. 2019;12:145\u20137. https:\/\/doi.org\/10.1016\/j.molp.2018.12.006.","journal-title":"Mol Plant."},{"key":"3309_CR82","doi-asserted-by":"publisher","first-page":"1826","DOI":"10.1093\/plphys\/kiae436","volume":"196","author":"W Zhao","year":"2024","unstructured":"Zhao W, Ji Y, Zhou Y, Wang X. Geminivirus C4\/AC4 proteins hijack cellular Coat protein complex I for chloroplast targeting and viral infections. Plant Physiol. 2024;196:1826\u201339. https:\/\/doi.org\/10.1093\/plphys\/kiae436.","journal-title":"Plant Physiol."},{"key":"3309_CR83","doi-asserted-by":"crossref","unstructured":"Kulshreshtha A, Kumar Y, Roshan P, Bhattacharjee B, Mukherjee SK, Hallan V. AC4 protein of tomato leaf curl Palampur virus is an RNA silencing suppressor and a pathogenicity determinant. Microb Pathog. 2019;135:103636. Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S0882401019306540","DOI":"10.1016\/j.micpath.2019.103636"},{"key":"3309_CR84","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.01307-20","author":"Y Mei","year":"2020","unstructured":"Mei Y, Zhang F, Wang M, Li F, Wang Y, Zhou X. Divergent symptoms caused by geminivirus-encoded C4 proteins correlate with their ability to bind NbSK\u03b7. J Virol. 2020. https:\/\/doi.org\/10.1128\/jvi.01307-20.","journal-title":"J Virol"},{"key":"3309_CR85","doi-asserted-by":"publisher","first-page":"2235","DOI":"10.1007\/s11033-021-06235-x","volume":"48","author":"KV Kiselev","year":"2021","unstructured":"Kiselev KV, Aleynova OA, Ogneva ZV, Suprun AR, Dubrovina AS. 35S promoter-driven transgenes are variably expressed in different organs of Arabidopsis thaliana and in response to abiotic stress. Mol Biol Rep. 2021;48:2235\u201341. https:\/\/doi.org\/10.1007\/s11033-021-06235-x.","journal-title":"Mol Biol Rep"},{"key":"3309_CR86","doi-asserted-by":"publisher","first-page":"286","DOI":"10.3390\/v12030286","volume":"12","author":"MG Rodr\u00edguez-Gandarilla","year":"2020","unstructured":"Rodr\u00edguez-Gandarilla MG, Rodr\u00edguez-Negrete EA, Rivera-Bustamante RF. Superinfection by PHYVV alters the recovery process in PepGMV-Infected pepper plants. Viruses. 2020;12:286.\u00a0https:\/\/www.mdpi.com\/1999-4915\/12\/3\/286","journal-title":"Viruses"}],"container-title":["Virology Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12985-026-03309-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12985-026-03309-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12985-026-03309-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T06:34:28Z","timestamp":1790577268000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1186\/s12985-026-03309-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,23]]},"references-count":86,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["3309"],"URL":"https:\/\/doi.org\/10.1186\/s12985-026-03309-9","relation":{},"ISSN":["1743-422X"],"issn-type":[{"value":"1743-422X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,23]]},"assertion":[{"value":"12 August 2026","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 September 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Not applicable. This manuscript does not involve any studies with human participants or animals conducted by the authors.","order":1,"name":"Ethics","label":"Ethics approval and consent to participate","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All authors consent to publication.","order":2,"name":"Ethics","label":"Consent for publication","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","label":"Competing interests","group":{"name":"EthicsHeading","label":"Declarations"}}],"article-number":"224"}}