{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T14:07:51Z","timestamp":1789567671573,"version":"build-2803163510"},"reference-count":50,"publisher":"American Chemical Society (ACS)","issue":"36","license":[{"start":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T00:00:00Z","timestamp":1788307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T00:00:00Z","timestamp":1788307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T00:00:00Z","timestamp":1788307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2022YFD1401201"],"award-info":[{"award-number":["2022YFD1401201"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002365","name":"China Agricultural University","doi-asserted-by":"publisher","award":["PC2024B01010"],"award-info":[{"award-number":["PC2024B01010"]}],"id":[{"id":"10.13039\/501100002365","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005236","name":"Chinese Universities Scientific Fund","doi-asserted-by":"publisher","award":["2022RC015"],"award-info":[{"award-number":["2022RC015"]}],"id":[{"id":"10.13039\/501100005236","id-type":"DOI","asserted-by":"publisher"}]},{"name":"State Key Laboratory of Agricultural and Forestry Biosecurity","award":["SKLJRP2505"],"award-info":[{"award-number":["SKLJRP2505"]}]},{"name":"National Top Young Talents Program of China"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,16]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Bemisia tabaci is a destructive agricultural pest with a remarkable capacity to exploit diverse host plants. Horizontally transferred genes (HTGs) have recently been implicated in this adaptive success, yet the functions of most HTGs in the whitefly remain unclear. Feeding behavior is crucial for nutrient acquisition and reproduction in piercing-sucking insects, but whether HTGs contribute to host adaptation by regulating feeding remains largely unknown. Here, we identified BtHCYP, a plant-derived HGT gene in B. tabaci encoding a cysteine protease. Biochemical and in vivo assays confirmed that BtHCYP retained cysteine protease activity. RNA interference-mediated silencing of BtHCYP significantly reduced whitefly fecundity. Electrical penetration graph on cotton plants analyses further revealed that BtHCYP knockdown impaired phloem feeding. Collectively, these findings demonstrate that a plant-derived HTG can enhance whitefly fecundity and efficient phloem feeding, as BtHCYP silencing reduced oviposition by 27.6%, highlighting a potential molecular target for whitefly management.<\/jats:p>","DOI":"10.1021\/acs.jafc.6c05658","type":"journal-article","created":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T16:19:39Z","timestamp":1788452379000},"page":"28230-28240","source":"Crossref","is-referenced-by-count":0,"title":["Plant-Derived\n                    <i>BtHCYP<\/i>\n                    Promotes Phloem\nFeeding and Fecundity in\n                    <i>Bemisia tabaci<\/i>"],"prefix":"10.1021","volume":"74","author":[{"given":"Fangfang","family":"Qi","sequence":"first","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaolong","family":"Qiu","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zitong","family":"Sang","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haolin","family":"Han","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guanghui","family":"Zhang","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Wei","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guoqiang","family":"Pan","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenzhen","family":"Zhang","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hengjia","family":"Zhang","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Congai","family":"Zhen","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7550-2150","authenticated-orcid":true,"given":"Jixing","family":"Xia","sequence":"additional","affiliation":[{"name":"China Agricultural University , , ,","place":["Beijing, China, 100193"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,9,2]]},"reference":[{"key":"2026091609090188400_cit1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1146\/annurev-ento-112408-085504","article-title":"Bemisia tabaci: a statement of species status","volume":"56","author":"De Barro","year":"2011","journal-title":"Annu. Rev. Entomol."},{"issue":"9","key":"2026091609090188400_cit2","doi-asserted-by":"publisher","first-page":"1808","DOI":"10.3390\/v13091808","article-title":"Factors determining\ntransmission of persistent viruses\nby Bemisia tabaci and emergence of new virus-vector\nrelationships","volume":"13","author":"Ghosh","year":"2021","journal-title":"Viruses"},{"issue":"1","key":"2026091609090188400_cit3","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1146\/annurev-virology-031413-085410","article-title":"Role of the insect\nsupervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses","volume":"2","author":"Gilbertson","year":"2015","journal-title":"Annu. Rev. Virol."},{"issue":"29","key":"2026091609090188400_cit4","doi-asserted-by":"publisher","first-page":"16928","DOI":"10.1073\/pnas.1820132117","article-title":"A plant DNA virus replicates\nin the salivary glands of its insect vector via recruitment of host\nDNA synthesis machinery","volume":"117","author":"He","year":"2020","journal-title":"Proc. Natl. Acad. Sci.\nU. S. A."},{"issue":"1","key":"2026091609090188400_cit5","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1146\/annurev-phyto-072910-095235","article-title":"Emerging virus diseases\ntransmitted by whiteflies","volume":"49","author":"Navas-Castillo","year":"2011","journal-title":"Annu. Rev. Phytopathol."},{"issue":"3","key":"2026091609090188400_cit6","doi-asserted-by":"publisher","first-page":"198","DOI":"10.3390\/insects12030198","article-title":"Bemisia tabaci on\nvegetables in the Southern United States:\nIncidence, Impact, and Management","volume":"12","author":"Li","year":"2021","journal-title":"Insects"},{"key":"2026091609090188400_cit7","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1146\/annurev-ento-120120-093940","article-title":"Whitefly-plant interactions:\nAn integrated\nmolecular perspective","volume":"69","author":"Morin","year":"2024","journal-title":"Annu. Rev. Entomol."},{"issue":"9","key":"2026091609090188400_cit8","doi-asserted-by":"publisher","first-page":"619","DOI":"10.3390\/insects11090619","article-title":"A review of the biology\nand control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to\nbiological control using entomopathogenic fungi","volume":"11","author":"Sani","year":"2020","journal-title":"Insects"},{"key":"2026091609090188400_cit9","doi-asserted-by":"publisher","first-page":"671286","DOI":"10.3389\/fpls.2021.671286","article-title":"Identification of a sulfatase that detoxifies glucosinolates\nin the phloem-feeding insect Bemisia tabaci and prefers\nindolic glucosinolates","volume":"12","author":"Manivannan","year":"2021","journal-title":"Front. Plant Sci."},{"key":"2026091609090188400_cit10","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.cois.2017.02.001","article-title":"Whitefly interactions\nwith plants","volume":"19","author":"Wang","year":"2017","journal-title":"Curr. Opin. Insect. Sci."},{"issue":"9","key":"2026091609090188400_cit11","doi-asserted-by":"publisher","first-page":"2635","DOI":"10.1093\/gbe\/evv170","article-title":"Metabolic\ncoevolution in the bacterial symbiosis of whiteflies and related plant\nsap-feeding insects","volume":"7","author":"Luan","year":"2015","journal-title":"Genome Biol. Evol."},{"issue":"10","key":"2026091609090188400_cit12","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evac141","article-title":"Multiple horizontal\nacquisitions of plant genes in\nthe whitefly Bemisia tabaci","volume":"14","author":"Gilbert","year":"2022","journal-title":"Genome Biol. Evol."},{"issue":"10","key":"2026091609090188400_cit13","doi-asserted-by":"publisher","first-page":"msad221","DOI":"10.1093\/molbev\/msad221","article-title":"Horizontally\ntransferred salivary protein promotes insect feeding by suppressing\nferredoxin-mediated plant defenses","volume":"40","author":"Wang","year":"2023","journal-title":"Mol. Biol.\nEvol."},{"issue":"7","key":"2026091609090188400_cit14","doi-asserted-by":"publisher","first-page":"1693","DOI":"10.1016\/j.cell.2021.02.014","article-title":"Whitefly hijacks\na plant detoxification gene that neutralizes plant toxins","volume":"184","author":"Xia","year":"2021","journal-title":"Cell"},{"issue":"8","key":"2026091609090188400_cit15","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1038\/nrg2386","article-title":"Horizontal gene transfer in eukaryotic evolution","volume":"9","author":"Keeling","year":"2008","journal-title":"Nat. Rev. Genet."},{"issue":"12","key":"2026091609090188400_cit16","doi-asserted-by":"publisher","first-page":"2226","DOI":"10.1093\/oxfordjournals.molbev.a004046","article-title":"Prokaryotic evolution in light of\ngene transfer","volume":"19","author":"Gogarten","year":"2002","journal-title":"Mol. Biol. 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Sci."},{"issue":"29","key":"2026091609090188400_cit21","doi-asserted-by":"publisher","first-page":"9965","DOI":"10.1073\/pnas.0708958105","article-title":"A protein\nfrom the salivary glands\nof the pea aphid, Acyrthosiphon pisum, is essential\nin feeding on a host plant","volume":"105","author":"Mutti","year":"2008","journal-title":"Proc. Natl. Acad.\nSci. U. S. A."},{"key":"2026091609090188400_cit22","doi-asserted-by":"publisher","first-page":"336","DOI":"10.3389\/fpls.2013.00336","article-title":"How phloem-feeding insects face the\nchallenge of phloem-located defenses","volume":"4","author":"Will","year":"2013","journal-title":"Front.\nPlant Sci."},{"issue":"4","key":"2026091609090188400_cit23","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1002\/ps.3689","article-title":"Plant resistance to aphid feeding:\nbehavioral, physiological,\ngenetic and molecular cues regulate aphid host selection and feeding","volume":"70","author":"Smith","year":"2014","journal-title":"Pest. Manag. Sci."},{"issue":"1","key":"2026091609090188400_cit24","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1038\/s41467-023-36403-5","article-title":"Planthopper salivary sheath protein\nLsSP1 contributes to manipulation of rice plant defenses","volume":"14","author":"Huang","year":"2023","journal-title":"Nat. Commun."},{"issue":"2","key":"2026091609090188400_cit25","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1073\/pnas.1714990116","article-title":"A salivary\neffector enables whitefly\nto feed on host plants by eliciting salicylic acid-signaling pathway","volume":"116","author":"Xu","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"Database issue","key":"2026091609090188400_cit26","doi-asserted-by":"publisher","first-page":"D227","DOI":"10.1093\/nar\/gkp971","article-title":"MEROPS: the peptidase\ndatabase","volume":"38","author":"Rawlings","year":"2009","journal-title":"Nucleic Acids Res."},{"issue":"13","key":"2026091609090188400_cit27","doi-asserted-by":"publisher","first-page":"3784","DOI":"10.1093\/nar\/gkg563","article-title":"ExPASy: The proteomics\nserver for in-depth protein\nknowledge and analysis","volume":"31","author":"Gasteiger","year":"2003","journal-title":"Nucleic Acids Res."},{"issue":"3","key":"2026091609090188400_cit28","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1161\/HYPERTENSIONAHA.113.02141","article-title":"Cathepsin\nK activity controls injury-related vascular repair in mice","volume":"63","author":"Hu","year":"2014","journal-title":"Hypertension"},{"issue":"6116","key":"2026091609090188400_cit29","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1126\/science.1229663","article-title":"Natively\ninhibited\nTrypanosoma brucei cathepsin B structure determined by using an X-ray\nlaser","volume":"339","author":"Redecke","year":"2013","journal-title":"Science."},{"issue":"1","key":"2026091609090188400_cit30","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1186\/s13071-017-2005-z","article-title":"Proteases of haematophagous\narthropod vectors are involved in blood-feeding, yolk formation and\nimmunity\u2500a review","volume":"10","author":"Santiago","year":"2017","journal-title":"Parasit. Vectors"},{"issue":"6","key":"2026091609090188400_cit31","doi-asserted-by":"publisher","first-page":"2075","DOI":"10.1002\/ps.7384","article-title":"Heat shock protein 70 and Cathepsin\nB genes are involved in the thermal tolerance of Aphis gossypii","volume":"79","author":"Liu","year":"2023","journal-title":"Pest. Manag. Sci."},{"issue":"1","key":"2026091609090188400_cit32","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.1432-1033.1990.tb19324.x","article-title":"Purification and characterization of a cysteine proteinase\nfrom silkworm eggs","volume":"193","author":"Kageyama","year":"1990","journal-title":"Eur. J. Biochem."},{"issue":"4","key":"2026091609090188400_cit33","doi-asserted-by":"publisher","first-page":"S230","DOI":"10.1074\/mcp.m116.063495","article-title":"Host plants indirectly\ninfluence plant virus transmission by altering gut cysteine protease\nactivity of aphid vectors","volume":"16","author":"Pinheiro","year":"2017","journal-title":"Mol. Cell. Proteomics"},{"issue":"1","key":"2026091609090188400_cit34","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1186\/s13059-016-1145-3","article-title":"Rapid transcriptional plasticity of duplicated gene\nclusters enables a clonally reproducing aphid to colonise diverse\nplant species. Genome","volume":"18","author":"Mathers","year":"2017","journal-title":"Biol."},{"issue":"24","key":"2026091609090188400_cit35","doi-asserted-by":"publisher","first-page":"4826","DOI":"10.1016\/j.cub.2020.09.020","article-title":"An aphid-secreted salivary\nprotease activates plant\ndefense in phloem","volume":"30","author":"Guo","year":"2020","journal-title":"Curr. Biol."},{"issue":"15","key":"2026091609090188400_cit36","doi-asserted-by":"publisher","first-page":"4212","DOI":"10.1093\/jxb\/erae496","article-title":"RD21-like\nproteases: key effector hubs in plant-pathogen\ninteractions","volume":"76","author":"Huang","year":"2025","journal-title":"J. Exp. Bot."},{"issue":"12","key":"2026091609090188400_cit37","doi-asserted-by":"publisher","first-page":"4407","DOI":"10.1073\/pnas.1200068109","article-title":"Population bulk segregant mapping\nuncovers resistance mutations and the mode of action of a chitin synthesis\ninhibitor in arthropods","volume":"109","author":"Van Leeuwen","year":"2012","journal-title":"Proc. Natl. Acad. Sci.\nU. S. A."},{"issue":"1","key":"2026091609090188400_cit38","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1186\/s12864-017-3706-6","article-title":"Genome-wide analysis\nof ATP-binding cassette (ABC) transporters in the sweetpotato whitefly, Bemisia tabaci","volume":"18","author":"Tian","year":"2017","journal-title":"BMC Genomics"},{"issue":"4","key":"2026091609090188400_cit39","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1093\/jxb\/erj088","article-title":"Salivary\nsecretions by aphids interacting with proteins of phloem wound responses","volume":"57","author":"Tjallingii","year":"2006","journal-title":"J. Exp. Bot."},{"issue":"7","key":"2026091609090188400_cit40","doi-asserted-by":"publisher","first-page":"1549","DOI":"10.1038\/nprot.2014.092","article-title":"Tobacco rattle virus-based virus-induced gene silencing\nin Nicotiana benthamiana","volume":"9","author":"Senthil-Kumar","year":"2014","journal-title":"Nat.\nProtoc."},{"issue":"5","key":"2026091609090188400_cit41","doi-asserted-by":"publisher","first-page":"gix018","DOI":"10.1093\/gigascience\/gix018","article-title":"Genome sequencing of the sweetpotato\nwhitefly Bemisia tabaci MED\/Q","volume":"6","author":"Xie","year":"2017","journal-title":"GigaScience"},{"issue":"1","key":"2026091609090188400_cit42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.48130\/TP-2023-0003","article-title":"Research progress on\nhorizontal gene transfer and its functions in insects","volume":"2","author":"Xing","year":"2023","journal-title":"Trop. Plants"},{"issue":"6","key":"2026091609090188400_cit43","doi-asserted-by":"publisher","first-page":"1785","DOI":"10.1093\/gbe\/evw119","article-title":"Horizontal\ngene transfer contributes to the evolution of arthropod herbivory","volume":"8","author":"Wybouw","year":"2016","journal-title":"Genome Biol. Evol."},{"issue":"7","key":"2026091609090188400_cit44","doi-asserted-by":"publisher","DOI":"10.1016\/j.heliyon.2024.e29201","article-title":"Roles of herbivorous insects salivary\nproteins","volume":"10","author":"Ma","year":"2024","journal-title":"Heliyon"},{"key":"2026091609090188400_cit45","doi-asserted-by":"publisher","first-page":"6552","DOI":"10.1016\/j.csbj.2022.11.040","article-title":"Structure determinants\ndefining the specificity of papain-like cysteine proteases","volume":"20","author":"Petushkova","year":"2022","journal-title":"Comput. Struct. Biotechnol. J."},{"issue":"3","key":"2026091609090188400_cit46","doi-asserted-by":"publisher","first-page":"609","DOI":"10.18388\/abp.2004_3547","article-title":"Multifunctional role of plant cysteine\nproteinases","volume":"51","author":"Grudkowska","year":"2004","journal-title":"Acta. Biochim. Polym."},{"issue":"4","key":"2026091609090188400_cit47","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1111\/nph.14117","article-title":"Papain-like cysteine proteases as\nhubs in plant immunity","volume":"212","author":"Misas-Villamil","year":"2016","journal-title":"New Phytol."},{"issue":"1","key":"2026091609090188400_cit48","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1186\/1471-2229-10-227","article-title":"Significance\nof Cuscutain, a cysteine protease from Cuscuta reflexa, in host-parasite\ninteractions","volume":"10","author":"Bleischwitz","year":"2010","journal-title":"BMC Plant Biol."},{"issue":"1","key":"2026091609090188400_cit49","doi-asserted-by":"publisher","first-page":"17836","DOI":"10.1038\/s41598-022-20741-3","article-title":"Common resistance mechanisms are\ndeployed by plants\nagainst sap-feeding herbivorous insects: insights from a meta-analysis\nand systematic review","volume":"12","author":"Leybourne","year":"2022","journal-title":"Sci. Rep."},{"issue":"29","key":"2026091609090188400_cit50","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.adv1447","article-title":"Aphid effectors\nsuppress plant immunity via recruiting defense proteins to processing\nbodies","volume":"11","author":"Liu","year":"2025","journal-title":"Sci. Adv."}],"container-title":["Journal of Agricultural\nand Food Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jafc.6c05658","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/36\/28230\/68198511\/acs.jafc.6c05658.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jafcau\/article-pdf\/74\/36\/28230\/68198511\/acs.jafc.6c05658.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T13:31:58Z","timestamp":1789565518000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jafcau\/article\/74\/36\/28230\/5405200\/Plant-Derived-BtHCYP-Promotes-Phloem-Feeding-and"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,2]]},"references-count":50,"journal-issue":{"issue":"36","published-online":{"date-parts":[[2026,9,2]]},"published-print":{"date-parts":[[2026,9,16]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jafc.6c05658","relation":{},"ISSN":["0021-8561","1520-5118"],"issn-type":[{"value":"0021-8561","type":"print"},{"value":"1520-5118","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,2]]}}}