{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T12:34:08Z","timestamp":1791203648684,"version":"4.2.0"},"reference-count":66,"publisher":"American Society for Microbiology","issue":"1","license":[{"start":{"date-parts":[[2014,1,21]],"date-time":"2014-01-21T00:00:00Z","timestamp":1390262400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-sa\/3.0\/"},{"start":{"date-parts":[[2014,2,28]],"date-time":"2014-02-28T00:00:00Z","timestamp":1393545600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["mBio"],"published-print":{"date-parts":[[2014,2,28]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Emerging and reemerging diseases that result from pathogen host shifts are a threat to the health of humans and their domesticates. RNA viruses have extremely high mutation rates and thus represent a significant source of these infectious diseases. In the present study, we showed that a plant-pathogenic RNA virus, tobacco ringspot virus (TRSV), could replicate and produce virions in honeybees,<jats:named-content content-type=\"genus-species\">Apis mellifera<\/jats:named-content>, resulting in infections that were found throughout the entire body. Additionally, we showed that TRSV-infected individuals were continually present in some monitored colonies. While intracellular life cycle, species-level genetic variation, and pathogenesis of the virus in honeybee hosts remain to be determined, the increasing prevalence of TRSV in conjunction with other bee viruses from spring toward winter in infected colonies was associated with gradual decline of host populations and winter colony collapse, suggesting the negative impact of the virus on colony survival. Furthermore, we showed that TRSV was also found in ectoparasitic<jats:italic>Varroa<\/jats:italic>mites that feed on bee hemolymph, but in those instances the virus was restricted to the gastric cecum of<jats:italic>Varroa<\/jats:italic>mites, suggesting that<jats:italic>Varroa<\/jats:italic>mites may facilitate the spread of TRSV in bees but do not experience systemic invasion. Finally, our phylogenetic analysis revealed that TRSV isolates from bees, bee pollen, and<jats:italic>Varroa<\/jats:italic>mites clustered together, forming a monophyletic clade. The tree topology indicated that the TRSVs from arthropod hosts shared a common ancestor with those from plant hosts and subsequently evolved as a distinct lineage after transkingdom host alteration. This study represents a unique example of viruses with host ranges spanning both the plant and animal kingdoms.<\/jats:p><jats:p><jats:bold>IMPORTANCE<\/jats:bold>Pathogen host shifts represent a major source of new infectious diseases. Here we provide evidence that a pollen-borne plant virus, tobacco ringspot virus (TRSV), also replicates in honeybees and that the virus systemically invades and replicates in different body parts. In addition, the virus was detected inside the body of parasitic<jats:italic>Varroa<\/jats:italic>mites, which consume bee hemolymph, suggesting that<jats:italic>Varroa<\/jats:italic>mites may play a role in facilitating the spread of the virus in bee colonies. This study represents the first evidence that honeybees exposed to virus-contaminated pollen could also be infected and raises awareness of potential risks of new viral disease emergence due to host shift events. About 5% of known plant viruses are pollen transmitted, and these are potential sources of future host-jumping viruses. The findings from this study showcase the need for increased surveillance for potential host-jumping events as an integrated part of insect pollinator management programs.<\/jats:p>","DOI":"10.1128\/mbio.00898-13","type":"journal-article","created":{"date-parts":[[2014,1,22]],"date-time":"2014-01-22T05:34:53Z","timestamp":1390368893000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":78,"title":["Systemic Spread and Propagation of a Plant-Pathogenic Virus in European Honeybees, Apis mellifera"],"prefix":"10.1128","volume":"5","author":[{"given":"Ji Lian","family":"Li","sequence":"first","affiliation":[{"name":"Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R. Scott","family":"Cornman","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Bee Research Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jay D.","family":"Evans","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Bee Research Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffery S.","family":"Pettis","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Bee Research Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS Molecular Plant Pathology Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles","family":"Murphy","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Soybean Genomic &amp; Improvement Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen Jun","family":"Peng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Wu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Science, Beijing, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michele","family":"Hamilton","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Bee Research Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"Jr.","given":"Humberto F.","family":"Boncristiani","sequence":"additional","affiliation":[{"name":"Department of Biology, University North Carolina at Greensboro, Greensboro, North Carolina, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liang","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John","family":"Hammond","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Floral and Nursery Plants Research Unit, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan Ping","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Agriculture, ARS, Bee Research Laboratory, Beltsville, Maryland, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","first-page":"1","article-title":"The value of honey bee pollination in the United States","volume":"128","author":"Morse R","year":"2000","unstructured":"MorseR CalderoneN . 2000. The value of honey bee pollination in the United States. Bee Cult. 128:1\u201315.","journal-title":"Bee Cult."},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2010.01.007"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1146498"},{"key":"e_1_3_2_5_2","first-page":"599","article-title":"An estimate of managed colony losses in the winter of 2006\u20132007: a report commissioned by the apiary inspectors of America","volume":"147","author":"VanEngelsdorp D","year":"2007","unstructured":"VanEngelsdorpD UnderwoodR CaronD HayesJJr. 2007. An estimate of managed colony losses in the winter of 2006\u20132007: a report commissioned by the apiary inspectors of America. Am. Bee J. 147:599\u2013603.","journal-title":"Am. Bee J."},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.3896\/IBRA.1.49.1.01"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1758-2229.2011.00312.x"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1051\/apido\/2010014"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2005.10.002"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1603\/EC10355"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13592-011-0061-5"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0014357"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ento.54.110807.090454"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.87.1.434"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.081288198"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1100773108"},{"key":"e_1_3_2_17_2","volume-title":"Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses","author":"King AMQ","year":"2012","unstructured":"KingAMQ CarstensEB LefkowitzEJ . 2012. Secoviridae. In Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier Scientific, San Diego, CA."},{"key":"e_1_3_2_18_2","first-page":"57","volume-title":"Compendium of soybean diseases","author":"Demski JW","year":"1989","unstructured":"DemskiJW KuhnCW . 1989. Tobacco ringspot virus, p 57\u201359. In Compendium of soybean diseases, 3rd ed. American Phytopathological Society, St. Paul, MN.","edition":"3"},{"key":"e_1_3_2_19_2","volume-title":"CMI\/AAB descriptions of plant viruses no. 309 (no. 17 revised)","author":"R-S-S","year":"1985","unstructured":"R-S-S . 1985. Tobacco ringspot virus. In CMI\/AAB descriptions of plant viruses no. 309 (no. 17 revised). Association of Applied Biologists, Wellesbourne, United Kingdom."},{"key":"e_1_3_2_20_2","first-page":"723","article-title":"Transmission, movement, and vector relationships of tobacco ringspot virus in soybean","volume":"54","author":"Bergeson GB","year":"1964","unstructured":"BergesonGB AthowKL LavioletteFA ThomasineM . 1964. Transmission, movement, and vector relationships of tobacco ringspot virus in soybean. Phytopathology 54:723\u2013728.","journal-title":"Phytopathology"},{"key":"e_1_3_2_21_2","first-page":"164","article-title":"Transmission of tobacco ringspot virus by Xiphinema americanum to a wide range of hosts","volume":"62","author":"Douthit LB","year":"1978","unstructured":"DouthitLB McGuireJM . 1978. Transmission of tobacco ringspot virus by Xiphinema americanum to a wide range of hosts. Plant Dis. Rep. 62:164\u2013166.","journal-title":"Plant Dis. Rep."},{"key":"e_1_3_2_22_2","first-page":"681","article-title":"The grasshopper as a vector of tobacco ringspot virus in soybean","volume":"47","author":"Dunleavy JM","year":"1957","unstructured":"DunleavyJM . 1957. The grasshopper as a vector of tobacco ringspot virus in soybean. Phytopathology 47:681\u2013682.","journal-title":"Phytopathology"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1094\/Phyto-67-292"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1094\/PHYTO.1999.89.2.124"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1071\/AP07050"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1094\/Phyto-77-167"},{"key":"e_1_3_2_27_2","first-page":"85","volume-title":"Plant virus epidemiology.","author":"Mink G","year":"1982","unstructured":"MinkG . 1982. The possible role of honey bees in long-distance spread of prunus necrotic ringspot virus from California into Washington sweet cherry orchards, p 85\u201392. In PlumbRT ThreshJM (ed), Plant virus epidemiology. Blackwell Publishing, Oxford, United Kingdom."},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1007\/s13592-011-0009-9"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1186\/1743-422X-6-221"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.24.13910"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1001005"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1087139"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.287.5453.607"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2001.0997"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.279.5349.393"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0966-842X(02)02428-9"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.phyto.31.1.375"},{"key":"e_1_3_2_38_2","doi-asserted-by":"crossref","DOI":"10.1079\/9780851987941.0000","volume-title":"iruses of plants: descriptions and lists from the VIDE database.","author":"Brunt A","year":"1996","unstructured":"BruntA CrabtreeK DallwitzM GibbsA WatsonL . 1996. iruses of plants: descriptions and lists from the VIDE database. CABI International, Wallingford, United Kingdom."},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1094\/PHI-I-2006-0414-01"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-3527(07)70002-7"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1080\/00218839.1982.11100535"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1080\/00218839.1992.11101278"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1080\/00218839.1988.11100808"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1051\/apido:19850407"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0501860102"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1220941"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1006\/jipa.1998.4807"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1051\/apido:2004031"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.virol.2005.07.012"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1099\/vir.0.023853-0"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2011.09.010"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-3527(03)62002-6"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0906970106"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0006481"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2009.06.011"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.1603\/EC09429"},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2006.11.001"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-2920.2008.01687.x"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2005.08.005"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jip.2004.07.005"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.3390\/v3122425"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1099\/vir.0.81401-0"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.1.436-441.2005"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msm092"},{"key":"e_1_3_2_65_2","first-page":"406","article-title":"The neighbor-joining method: a new method for reconstructing phylogenetic trees","volume":"4","author":"Saitou N","year":"1987","unstructured":"SaitouN NeiM . 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406\u2013425.","journal-title":"Mol. Biol. Evol."},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0404206101"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.2307\/2408678"}],"container-title":["mBio"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00898-13","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/mBio.00898-13","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,9]],"date-time":"2023-07-09T23:31:47Z","timestamp":1688945507000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/mBio.00898-13"}},"subtitle":[],"editor":[{"given":"Anne K.","family":"Vidaver","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2014,2,28]]},"references-count":66,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2014,2,28]]}},"alternative-id":["10.1128\/mBio.00898-13"],"URL":"https:\/\/doi.org\/10.1128\/mbio.00898-13","relation":{},"ISSN":["2161-2129","2150-7511"],"issn-type":[{"value":"2161-2129","type":"print"},{"value":"2150-7511","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,2,28]]},"assertion":[{"value":"2013-10-20","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2013-12-13","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2014-01-21","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00898-13"}}