{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T15:43:47Z","timestamp":1781711027421,"version":"3.54.5"},"reference-count":55,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T00:00:00Z","timestamp":1712707200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000199","name":"University of Georgia","doi-asserted-by":"publisher","award":["#58-6080-9-006"],"award-info":[{"award-number":["#58-6080-9-006"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Plants can respond to insect infestation and virus infection by inducing plant defenses, generally mediated by phytohormones. Moreover, plant defenses alter host quality for insect vectors with consequences for the spread of viruses. In agricultural settings, other organisms commonly interact with plants, thereby inducing plant defenses that could affect plant\u2013virus\u2013vector interactions. For example, plant defenses induced by omnivorous insects can modulate insect behavior. This study focused on tomato yellow leaf curl virus (TYLCV), a plant virus of the family Geminiviridae and genus Begomovirus. It is transmitted in a persistent circulative manner by the whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae), posing a global threat to tomato production. Mirids (Hemiptera: Miridae) are effective biological control agents of B. tabaci, but there is a possibility that their omnivorous nature could also interfere with the process of virus transmission. To test this hypothesis, this study first addressed to what extent the mirid bug Dicyphus hesperus Knight induces plant defenses in tomato. Subsequently, the impact of this plant\u2013omnivore interaction on the transmission of TYLCV was evaluated. Controlled cage experiments were performed in a greenhouse setting to evaluate the impact of mirids on virus transmission and vector acquisition by B. tabaci. While we observed a reduced number of whiteflies settling on plants exposed to D. hesperus, the plant defenses induced by the mirid bug did not affect TYLCV transmission and accumulation. Additionally, whiteflies were able to acquire comparable amounts of TYLCV on mirid-exposed plants and control plants. Overall, the induction of plant defenses by D. hesperus did not influence TYLCV transmission by whiteflies on tomato.<\/jats:p>","DOI":"10.3390\/v16040587","type":"journal-article","created":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T10:55:28Z","timestamp":1712746528000},"page":"587","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Begomovirus Transmission to Tomato Plants Is Not Hampered by Plant Defenses Induced by Dicyphus hesperus Knight"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9127-2794","authenticated-orcid":false,"given":"Saioa","family":"Legarrea","sequence":"first","affiliation":[{"name":"Department of Entomology, University of Georgia, 1109 Experiment Street, Griffin, GA 30223, USA"},{"name":"Department of Food and Agriculture, University of La Rioja, C\/Madre de Dios, 53, 26006 Logro\u00f1o, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela Gabrielle","family":"LaTora","sequence":"additional","affiliation":[{"name":"Department of Entomology, University of Georgia, 1109 Experiment Street, Griffin, GA 30223, USA"},{"name":"University of Georgia Extension Fulton County, 7741 Roswell Road NE, Room 248, Sandy Springs, GA 30350, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alvin M.","family":"Simmons","sequence":"additional","affiliation":[{"name":"U.S.D.A.\u2014Agricultural Research Service, U.S. Vegetable Laboratory, 2700 Savannah Highway, Charleston, SC 29414, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rajagopalbabu","family":"Srinivasan","sequence":"additional","affiliation":[{"name":"Department of Entomology, University of Georgia, 1109 Experiment Street, Griffin, GA 30223, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,4,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1007\/s003440000026","article-title":"The myriad plant responses to herbivores","volume":"19","author":"Walling","year":"2000","journal-title":"J. Plant Growth Regul."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1146\/annurev-cellbio-092910-154055","article-title":"Hormonal modulation of plant immunity","volume":"28","author":"Pieterse","year":"2012","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1111\/nph.17261","article-title":"Virus-induced phytohormone dynamics and their effects on plant\u2013insect interactions","volume":"230","author":"Pan","year":"2021","journal-title":"New Phytol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1146\/annurev.arplant.59.032607.092825","article-title":"Plant immunity to insect herbivores","volume":"59","author":"Howe","year":"2008","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1104\/pp.107.112177","article-title":"Arthropod-inducible proteins: Broad spectrum defenses against multiple herbivores","volume":"146","author":"Luthe","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"19237","DOI":"10.1073\/pnas.0509026102","article-title":"Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut","volume":"102","author":"Chen","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1126\/science.1147113","article-title":"Methyl salicylate is a critical mobile signal for plant systemic acquired resistance","volume":"318","author":"Park","year":"2007","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.cpb.2019.03.002","article-title":"Chemical elicitors of systemic acquired resistance\u2014Salicylic acid and its functional analogs","volume":"17","author":"Tripathi","year":"2019","journal-title":"Curr. Plant Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1111\/j.1365-313X.2010.04132.x","article-title":"Methyl salicylate production in tomato affects biotic interactions","volume":"62","author":"Ament","year":"2010","journal-title":"Plant J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.jare.2023.04.016","article-title":"Join the green team: Inducers of plant immunity in the plant disease sustainable control toolbox","volume":"57","author":"Zhu","year":"2023","journal-title":"J. Adv. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1093\/jxb\/ert026","article-title":"Controlling crop diseases using induced resistance: Challenges for the future","volume":"64","author":"Walters","year":"2013","journal-title":"J. Exp. Bot."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kenney, J.R., Grandmont, M.E., and Mauck, K.E. (2020). Priming melon defenses with acibenzolar-s-methyl attenuates infections by phylogenetically distinct viruses and diminishes vector preferences for infected hosts. Viruses, 12.","DOI":"10.3390\/v12030257"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"105796","DOI":"10.1016\/j.cropro.2021.105796","article-title":"Acibenzolar-s-methyl induces resistance against cassava mosaic geminiviruses in Nicotiana benthamiana and their vector Bemisia tabaci in cassava (Manihot esculenta)","volume":"150","author":"Doungous","year":"2021","journal-title":"Crop Prot."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/S0261-2194(00)00028-4","article-title":"Effect of acibenzolar-s-methyl and imidacloprid on suppression of tomato spotted wilt tospovirus in flue-cured tobacco","volume":"19","author":"Pappu","year":"2000","journal-title":"Crop Prot."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2797","DOI":"10.1111\/pce.13885","article-title":"Defence priming in tomato by the green leaf volatile (Z)-3-hexenol reduces whitefly transmission of a plant virus","volume":"43","author":"Su","year":"2020","journal-title":"Plant Cell Environ."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.cois.2021.06.001","article-title":"Global change calls for novel plant protection: Reviewing the potential of omnivorous plant-inhabiting arthropods as predators and plant defence inducers","volume":"47","author":"Zhang","year":"2021","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Roda, A., Castillo, J., Allen, C., Urbaneja, A., P\u00e9rez-Hedo, M., Weihman, S., and Stansly, P.A. (2020). Biological control potential and drawbacks of three zoophytophagous mirid predators against Bemisia tabaci in the United States. Insects, 11.","DOI":"10.3390\/insects11100670"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Smith, H.A., and Krey, K.L. (2019). Three release rates of Dicyphus hesperus (Hemiptera: Miridae) for management of Bemisia tabaci (Hemiptera: Aleyrodidae) on greenhouse tomato. Insects, 10.","DOI":"10.3390\/insects10070213"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Pappas, M.L., Steppuhn, A., Geuss, D., Topalidou, N., Zografou, A., Sabelis, M.W., and Broufas, G.D. (2015). Beyond predation: The zoophytophagous predator Macrolophus pygmaeus induces tomato resistance against spider mites. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0127251"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/s00442-017-4000-7","article-title":"Phytophagy of omnivorous predator Macrolophus pygmaeus affects performance of herbivores through induced plant defences","volume":"186","author":"Zhang","year":"2018","journal-title":"Oecologia"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1002\/ps.5547","article-title":"Zoophytophagous predator-induced defences restrict accumulation of the tomato spotted wilt virus","volume":"76","author":"Bouagga","year":"2020","journal-title":"Pest Manag. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.biocontrol.2015.04.006","article-title":"Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae)","volume":"86","author":"Bouagga","year":"2015","journal-title":"Biol. Control"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1007\/s10340-022-01506-3","article-title":"Induction of plant defenses: The added value of zoophytophagous predators","volume":"95","author":"Bouagga","year":"2022","journal-title":"J. Pest Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1007\/s10340-018-1036-3","article-title":"Herbivores avoid host plants previously exposed to their omnivorous predator Macrolophus pygmaeus","volume":"92","author":"Zhang","year":"2019","journal-title":"J. Pest Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1127\/entomologia\/2021\/1196","article-title":"Eliciting tomato plant defenses by exposure to herbivore induced plant volatiles","volume":"41","author":"Vacas","year":"2021","journal-title":"Entomol. Gen."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Yan, Z., Wolters, A.M.A., Navas-castillo, J., and Bai, Y. (2021). The global dimension of tomato yellow leaf curl disease: Current status and breeding perspectives. Microorganisms, 9.","DOI":"10.3390\/microorganisms9040740"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1603\/EC11402","article-title":"Whitefly population dynamics and evaluation of whitefly-transmitted tomato yellow leaf curl virus (TYLCV)-resistant tomato genotypes as whitefly and TYLCV reservoirs","volume":"105","author":"Srinivasan","year":"2012","journal-title":"J. Econ. Entomol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1111\/pce.12650","article-title":"Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non-vector herbivore","volume":"39","author":"Su","year":"2016","journal-title":"Plant Cell Environ."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1111\/nph.13075","article-title":"Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk","volume":"205","author":"Alba","year":"2015","journal-title":"New Phytol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1007\/BF00040610","article-title":"Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum","volume":"20","author":"Joosten","year":"1992","journal-title":"Plant Mol. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/j.1365-313X.2010.04128.x","article-title":"Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate","volume":"62","author":"Tieman","year":"2010","journal-title":"Plant J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1094\/MPMI-9-0409","article-title":"Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants","volume":"9","author":"Gadea","year":"1996","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"6561","DOI":"10.1016\/S0021-9258(18)88818-4","article-title":"Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II","volume":"260","author":"Graham","year":"1985","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1104\/pp.111.188698","article-title":"Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato","volume":"158","author":"Nambeesan","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Naselli, M., Urbaneja, A., Siscaro, G., Jaques, J.A., Zappal\u00e0, L., Flors, V., and P\u00e9rez-Hedo, M. (2016). Stage-related defense response induction in tomato plants by Nesidiocoris tenuis. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17081210"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"The Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635\u2013641.","DOI":"10.1038\/nature11119"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Legarrea, S., Barman, A., Marchant, W., Diffie, S., and Srinivasan, R. (2015). Temporal effects of a begomovirus infection and host plant resistance on the preference and development of an insect vector, Bemisia tabaci, and implications for epidemics. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0142114"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Pappas, M.L., Steppuhn, A., and Broufas, G.D. (2016). The role of phytophagy by predators in shaping plant interactions with their pests. Commun. Integr. Biol., 9.","DOI":"10.1080\/19420889.2016.1145320"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1286","DOI":"10.1002\/ps.4838","article-title":"Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants","volume":"74","author":"Bouagga","year":"2018","journal-title":"Pest Manag. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3314","DOI":"10.1002\/ps.6958","article-title":"Two in one: The neotropical mirid predator Macrolophus basicornis increases pest control by feeding on plants","volume":"78","author":"Silva","year":"2022","journal-title":"Pest Manag. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3458","DOI":"10.1016\/j.febslet.2010.06.046","article-title":"SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-s-methyl in plants","volume":"584","author":"Tripathi","year":"2010","journal-title":"FEBS Lett."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1094\/PHYTO-08-12-0188-R","article-title":"Induction of antiviral responses by acibenzolar-s-methyl against cucurbit chlorotic yellows virus in melon","volume":"103","author":"Takeshita","year":"2013","journal-title":"Phytopathology"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Johnston, N., and Martini, X. (2020). The influence of visual and olfactory cues in host selection for Bemisia tabaci biotype b in the presence or absence of tomato yellow leaf curl virus. Insects, 11.","DOI":"10.3390\/insects11020115"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1007\/s10340-021-01463-3","article-title":"The omnivorous predator Macrolophus pygmaeus induces production of plant volatiles that attract a specialist predator","volume":"95","author":"Zhang","year":"2022","journal-title":"J. Pest Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s10340-017-0886-4","article-title":"Orius laevigatus strengthens its role as a biological control agent by inducing plant defenses","volume":"91","author":"Bouagga","year":"2018","journal-title":"J. Pest Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1002\/ps.5309","article-title":"Zoophytophagous mites can trigger plant-genotype specific defensive responses affecting potential prey beyond predation: The case of Euseius stipulatus and Tetranychus urticae in citrus","volume":"75","author":"Flors","year":"2019","journal-title":"Pest Manag. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.coviro.2015.06.008","article-title":"Persistent, circulative transmission of begomoviruses by whitefly vectors","volume":"15","author":"Rosen","year":"2015","journal-title":"Curr. Opin. Virol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1111\/j.1744-7348.2002.tb00175.x","article-title":"The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci\u2014Insights from studies with tomato yellow leaf curl virus","volume":"140","author":"Czosnek","year":"2002","journal-title":"Ann. Appl. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"661141","DOI":"10.3389\/fpls.2021.661141","article-title":"Spotlight on the roles of whitefly effectors in insect\u2013plant interactions","volume":"12","author":"Naalden","year":"2021","journal-title":"Front. Plant Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"5230","DOI":"10.1038\/srep05230","article-title":"Bemisia tabaci Q carrying tomato yellow leaf curl virus strongly suppresses host plant defenses","volume":"4","author":"Shi","year":"2014","journal-title":"Sci. Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1007\/s00442-003-1289-1","article-title":"Herbivore host plant selection: Whitefly learns to avoid host plants that harbour predators of her offspring","volume":"136","author":"Nomikou","year":"2003","journal-title":"Oecologia"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1094\/PDIS.2004.88.8.882","article-title":"Integrated management of tomato spotted wilt on field-grown tomatoes","volume":"88","author":"Momol","year":"2004","journal-title":"Plant Dis."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1007\/s10658-015-0657-0","article-title":"Evaluation of acibenzolar-s-methyl-induced resistance against iris yellow spot tospovirus","volume":"142","author":"Tripathi","year":"2015","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/S0261-2194(00)00031-4","article-title":"Benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester induces systemic resistance in tomato (Lycopersicon esculentum. Mill cv. Vollendung) to cucumber mosaic virus","volume":"19","author":"Anfoka","year":"2000","journal-title":"Crop Prot."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Latora, A.G., Codod, C.B., Legarrea, S., Dutta, B., Kemerait, R.C., Adkins, S., Turechek, W., Coolong, T., da Silva, A.L.B.R., and Srinivasan, R. (2022). Combining cultural tactics and insecticides for the management of the sweetpotato whitefly, Bemisia tabaci MEAM1, and viruses in yellow squash. Horticulturae, 8.","DOI":"10.3390\/horticulturae8040341"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/4\/587\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:25:50Z","timestamp":1760106350000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/4\/587"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,10]]},"references-count":55,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["v16040587"],"URL":"https:\/\/doi.org\/10.3390\/v16040587","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,10]]}}}