{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T11:03:34Z","timestamp":1789643014999,"version":"4.0.0"},"reference-count":58,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:00:00Z","timestamp":1788998400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Beet curly top viruses (BCTVs) are highly devastating viral pathogens affecting a wide range of plant species worldwide and are transmitted only by leafhoppers in the genus Circulifer. During viral infection, host plant cells undergo morphological changes known as cytopathic effects (CPEs). This study investigated CPEs induced by BCTVs infecting four plant hosts: tomato, pepper, sugar beet, and hemp. BCTV infection resulted in severe stunting, leaf curling, and yellowing, leading to reduced photosynthetic capacity and yield losses. Transmission electron microscopy of ultrathin leaf sections revealed that chloroplasts were the universal primary target of BCTV damage across all four hosts, consistently exhibiting severe structural disruption, while starch grains and vacuoles were also affected. Notably, host-specific ultrastructural alterations were observed: enlarged chloroplasts with disrupted grana stacks and small stromal vesicles in BCTV-Wor-infected tomato and hemp, swollen chloroplasts with disappeared grana and disorganized thylakoids in BCTV-Svr-infected sugar beet, and unidentifiable grana structures in BCTV-PeYDV-infected pepper. These alterations did not correlate with virus strain, suggesting that host-specific inducible defense mechanisms play a greater role than strain identity. This is the first study to highlight the diverse ultrastructural impacts of BCTVs across plant species, improving understanding of host\u2013virus interactions and aiding development of control strategies to safeguard global food security.<\/jats:p>","DOI":"10.3390\/pathogens15090965","type":"journal-article","created":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T09:13:03Z","timestamp":1789031583000},"page":"965","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Host-Dependent Cytopathological Responses to Beet Curly Top Virus Infection in Four Plant Species"],"prefix":"10.3390","volume":"15","author":[{"given":"Batool M.","family":"Alkhatib","sequence":"first","affiliation":[{"name":"College of Applied Medical Sciences, Amman Arab University, Amman 11953, Jordan"},{"name":"Molecular Biology and Interdisciplinary Life Sciences Program, New Mexico State University, Las Cruces, NM 88003, USA"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"software","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5058-2980","authenticated-orcid":false,"given":"Rebecca","family":"Creamer","sequence":"additional","affiliation":[{"name":"Molecular Biology and Interdisciplinary Life Sciences Program, New Mexico State University, Las Cruces, NM 88003, USA"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Ershova, N., Sheshukova, E., Kamarova, K., Arifulin, E., Tashlitsky, V., Serebryakova, M., and Komarova, T. (2022). Nicotiana benthamiana Kunitz Peptidase Inhibitor-like Protein Involved in Chloroplast-to-Nucleus Regulatory Pathway in Plant-Virus Interaction. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1041867"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Wang, P., Liu, J., Lyu, Y., Huang, Z., Zhang, X., Sun, B., Li, P., Jing, X., Li, H., and Zhang, C. (2022). A Review of Vector-Borne Rice Viruses. Viruses, 14.","DOI":"10.3390\/v14102258"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1007\/s007050170067","article-title":"Complementation of Bipartite Begomovirus Movement Functions by Topocuviruses and Curtoviruses","volume":"146","author":"Briddon","year":"2001","journal-title":"Arch. Virol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1146\/annurev-phyto-072910-095235","article-title":"Emerging Virus Diseases Transmitted by Whiteflies","volume":"49","year":"2011","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_5","unstructured":"Hull, R. (2014). Plant Virology, Academic Press. [5th ed.]."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.virusres.2008.07.028","article-title":"Plant Virus Emergence and Evolution: Origins, New Encounter Scenarios, Factors Driving Emergence, Effects of Changing World Conditions, and Prospects for Control","volume":"141","author":"Jones","year":"2009","journal-title":"Virus Res."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Lalibert\u00e9, J.F., Moffett, P., Sanfa\u00e7on, H., Wang, A., Nelson, R.S., and Schoelz, J.E. (2013). e-Book on Plant Virus Infection\u2014A Cell Biology Perspective. Front. Plant Sci., 4.","DOI":"10.3389\/fpls.2013.00203"},{"key":"ref_8","unstructured":"Anikina, I.N., and Seitzhanova, L.L. (2015). Phytovirusology, Kereku."},{"key":"ref_9","unstructured":"Thomas, P.E., and Mink, G.I. (1979). Beet Curly Top Virus. Descriptions of Plant Viruses, Association of Applied Biologists. Available online: http:\/\/www.dpvweb.net\/dpv\/showdpv\/?dpvno=210."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1586","DOI":"10.1094\/PDIS-10-15-1189-RE","article-title":"Characterization of Beet Curly Top Virus Strains Circulating in Beet Leafhoppers (Hemiptera: Cicadellidae) in Northeastern Oregon","volume":"100","author":"Rondon","year":"2016","journal-title":"Plant Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1094\/PD-89-0480","article-title":"Curtovirus Infection of Chile Pepper in New Mexico","volume":"89","author":"Creamer","year":"2005","journal-title":"Plant Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1094\/PDIS-92-4-0650A","article-title":"First Report of Beet Mild Curly Top Virus Infection of Chile Pepper in North-Central Mexico","volume":"92","author":"Creamer","year":"2008","journal-title":"Plant Dis."},{"key":"ref_13","first-page":"727","article-title":"First Report of Beet Curly Top Virus Infecting Industrial Hemp (Cannabis sativa) in Arizona","volume":"105","author":"Hu","year":"2020","journal-title":"Plant Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1093\/ee\/nvad069","article-title":"Interactions of beet leafhopper (Hemiptera: Cicadellidae), vector of beet curly top virus, and hemp in New Mexico","volume":"53","author":"Creamer","year":"2024","journal-title":"Environ. Entomol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1094\/PHYTO-09-25-0297-R","article-title":"Beet curly top virus genetic diversity, impact on cannabinoid profiles, vector survival, and potential for seed transmission in hemp","volume":"116","author":"Han","year":"2026","journal-title":"Phytopathology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1094\/PDIS-94-1-0099","article-title":"Characterization of Curtoviruses Associated with Curly Top Disease of Tomato in California and Monitoring for These Viruses in Beet Leafhoppers","volume":"94","author":"Chen","year":"2010","journal-title":"Plant Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1094\/PHYTO-98-11-1212","article-title":"Curly Top Survey in the Western United States","volume":"98","author":"Strausbaugh","year":"2008","journal-title":"Phytopathology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1094\/PDIS-03-17-0381-RE","article-title":"Beet Curly Top Virus Strains Associated with Sugar Beet in Idaho, Oregon, and a Western U.S. Collection","volume":"101","author":"Strausbaugh","year":"2017","journal-title":"Plant Dis."},{"key":"ref_19","unstructured":"Bamford, D.H., and Zuckerman, M. (2020). Beet Curly Top Virus (Geminiviridae). Encyclopedia of Virology, Academic Press. [4th ed.]."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s10681-016-1693-3","article-title":"Evaluation of Sugar Beet Lines for Resistance to Beet Curly Top Viruses","volume":"210","author":"Montazeri","year":"2016","journal-title":"Euphytica"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/0042-6822(73)90049-4","article-title":"Particles and Associated Inclusions in Sugarbeet Infected with the Curly Top Virus","volume":"56","author":"Esau","year":"1973","journal-title":"Virology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/BF02712670","article-title":"A Plant DNA Minipreparation: Version II","volume":"1","author":"Dellaporta","year":"1983","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1007\/s00705-009-0320-1","article-title":"Characterization of a New Curtovirus, Pepper Yellow Dwarf Virus, from Chile Pepper and Distribution in Weed Hosts in New Mexico","volume":"154","author":"Lam","year":"2009","journal-title":"Arch. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1007\/s10535-016-0600-z","article-title":"Impact of Exogenous Caffeine on Morphological, Biochemical, and Ultrastructural Characteristics of Nicotiana tabacum","volume":"60","author":"Alkhatib","year":"2016","journal-title":"Biol. Plant."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Alkhatib, R., Alkhatib, B., Abdo, N., Al-Eitan, L., and Creamer, R. (2019). Physio-Biochemical and Ultrastructural Impact of (Fe3O4) Nanoparticles on Tobacco. BMC Plant Biol., 19.","DOI":"10.1186\/s12870-019-1864-1"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1083\/jcb.17.1.208","article-title":"The Use of Lead Citrate at High pH as an Electron-Opaque Stain in Electron Microscopy","volume":"17","author":"Reynolds","year":"1963","journal-title":"J. Cell Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An Open-Source Platform for Biological-Image Analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Bennett, C.W. (1971). The Curly Top Disease of Sugarbeet and Other Plants, The American Phytopathological Society. Monograph No. 7.","DOI":"10.1094\/9780890546260"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1094\/PDIS-08-19-1656-PDN","article-title":"First Report of Beet Curly Top Virus Infecting Cannabis sativa in Western Colorado","volume":"104","author":"Giladi","year":"2020","journal-title":"Plant Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2211","DOI":"10.1099\/0022-1317-71-10-2211","article-title":"Genomic Characterization of Phenotypic Variants of Beet Curly Top Virus","volume":"71","author":"Stenger","year":"1990","journal-title":"J. Gen. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/0042-6822(91)90127-W","article-title":"Point Mutations in the Turnip Crinkle Virus Capsid Protein Affect the Symptoms Expressed by Nicotiana benthamiana","volume":"183","author":"Heaton","year":"1991","journal-title":"Virology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1016\/0042-6822(91)90902-N","article-title":"Role of Alfalfa Mosaic Virus Coat Protein Gene in Symptom Formation","volume":"181","author":"Neeleman","year":"1991","journal-title":"Virology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1094\/Phyto-60-419","article-title":"Discrepancies in the Intracellular Behavior of Three Strains of Tobacco Mosaic Virus, Two of Which Are Serologically Indistinguishable","volume":"60","author":"Granett","year":"1970","journal-title":"Phytopathology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1111\/j.1439-0434.1972.tb02616.x","article-title":"An Electron Microscopic and Autoradiographic Study of Tobacco Leaves Infected with the U5 Strain of Tobacco Mosaic Virus","volume":"75","author":"Betto","year":"1972","journal-title":"J. Phytopathol."},{"key":"ref_35","unstructured":"Brinton, M., and Rueckert, R. (1987). Responses of Plant Cells to Virus Infection with Special Reference to the Sites of RNA Replication. Positive Strand RNA Viruses, Alan R. Liss, Inc."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"12252","DOI":"10.1128\/JVI.01329-08","article-title":"Biogenesis of Cytoplasmic Membranous Vesicles for Plant Potyvirus Replication Occurs at the Endoplasmic Reticulum Exit Sites in a COPI- and COPII-Dependent Manner","volume":"82","author":"Wei","year":"2008","journal-title":"J. Virol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/BF00027494","article-title":"The Double-Stranded RNA Associated with the \u2018447\u2019 Cytoplasmic Male Sterility in Vicia faba Is Packaged Together with Its Replicase in Cytoplasmic Membranous Vesicles","volume":"14","author":"Lefebvre","year":"1990","journal-title":"Plant Mol. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"10460","DOI":"10.1128\/JVI.00819-09","article-title":"Turnip Mosaic Virus RNA Replication Complex Vesicles Are Mobile, Align with Microfilaments, and Are Each Derived from a Single Viral Genome","volume":"83","author":"Cotton","year":"2009","journal-title":"J. Virol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2594","DOI":"10.1105\/tpc.18.00281","article-title":"Turnip Mosaic Virus Uses the SNARE Protein VTI11 in an Unconventional Route for Replication Vesicle Trafficking","volume":"30","author":"Cabanillas","year":"2018","journal-title":"Plant Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1099\/0022-1317-21-1-9","article-title":"Mitochondrial Vesiculation Associated with Cucumber Green Mottle Mosaic Virus-Infected Plants","volume":"21","author":"Hatta","year":"1973","journal-title":"J. Gen. Virol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1099\/0022-1317-53-2-343","article-title":"Cytopathic Structures Associated with Tonoplasts of Plant Cells Infected with Cucumber Mosaic and Tomato Aspermy Viruses","volume":"53","author":"Hatta","year":"1980","journal-title":"J. Gen. Virol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/S0022-5320(84)90125-4","article-title":"The Origin of Multivesicular Bodies in Tomato Bushy Stunt Virus-Infected Gomphrena globosa Plants","volume":"88","author":"Martelli","year":"1984","journal-title":"J. Ultrastruct. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1146\/annurev-virology-031413-085532","article-title":"Viral Manipulation of Plant Host Membranes","volume":"1","author":"Zheng","year":"2014","journal-title":"Annu. Rev. Virol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.molp.2016.01.011","article-title":"Biogenesis of Plant Prevacuolar Multivesicular Bodies","volume":"9","author":"Cui","year":"2016","journal-title":"Mol. Plant"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1139\/x93-174","article-title":"Effect of Ozone and Aluminum on Pitch Pine (Pinus rigida) Seedlings: Needle Ultrastructure","volume":"23","author":"McQuattie","year":"1993","journal-title":"Can. J. For. Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/j.pbi.2011.07.009","article-title":"Plant Endosomal Trafficking Pathways","volume":"14","author":"Reyes","year":"2011","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1146\/annurev-arplant-043015-112242","article-title":"Endocytosis and Endosomal Trafficking in Plants","volume":"67","author":"Goodman","year":"2016","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1146\/annurev-cellbio-092910-154152","article-title":"Multivesicular Body Morphogenesis","volume":"28","author":"Hanson","year":"2012","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e23897","DOI":"10.7554\/eLife.23897","article-title":"Autophagy Functions as an Antiviral Mechanism Against Geminiviruses in Plants","volume":"6","author":"Haxim","year":"2017","journal-title":"eLife"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1093\/jxb\/erx234","article-title":"Vacuolar Degradation of Chloroplast Components: Autophagy and Beyond","volume":"69","author":"Otegui","year":"2018","journal-title":"J. Exp. Bot."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Zhuang, X., and Jiang, L. (2019). Chloroplast Degradation: Multiple Routes into the Vacuole. Front. Plant Sci., 10.","DOI":"10.3389\/fpls.2019.00359"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1111\/nph.14134","article-title":"Chloroplast Quality Control\u2014Balancing Energy Production and Stress","volume":"212","author":"Woodson","year":"2016","journal-title":"New Phytol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.pbi.2019.06.005","article-title":"Chloroplast Stress Signals: Regulation of Cellular Degradation and Chloroplast Turnover","volume":"52","author":"Woodson","year":"2019","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2152","DOI":"10.1002\/1873-3468.14349","article-title":"Autophagy in Plant Viral Infection","volume":"596","author":"Yang","year":"2022","journal-title":"FEBS Lett."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"254","DOI":"10.5897\/AJMR2017.8786","article-title":"Evidence of curtovirus competition and synergy in co-infected plant hosts","volume":"12","author":"Peinado","year":"2018","journal-title":"Afr. J. Microbiol. Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1094\/PDIS-04-22-0856-SC","article-title":"Curly top disease of hemp (Cannabis sativa) in California is caused by mild-type strains of Beet curly top virus often in mixed infection","volume":"106","author":"Melgarejo","year":"2022","journal-title":"Plant Dis."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Withycombe, J., Han, J., MacWilliams, J., Dorn, K.M., Nalam, V.J., and Nachappa, P. (2024). Transcriptomic profiling reveals distinct responses to beet curly top virus (BCTV) infection in resistant and susceptible sugar beet genotypes. BMC Genom., 25.","DOI":"10.1186\/s12864-024-11143-y"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1094\/PBIOMES-06-24-0068-R","article-title":"Exploring the hemp virome and assessing hemp germplasm for resistance to an emerging pathogen","volume":"9","author":"Hackenberg","year":"2025","journal-title":"Phytobiomes J."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/9\/965\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T10:30:53Z","timestamp":1789641053000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/15\/9\/965"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,10]]},"references-count":58,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["pathogens15090965"],"URL":"https:\/\/doi.org\/10.3390\/pathogens15090965","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,10]]}}}