{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T18:12:42Z","timestamp":1784743962274,"version":"3.55.0"},"reference-count":38,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T00:00:00Z","timestamp":1784678400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Weifang University of Science and Technology doctoral research initiation project","award":["2021KJBS02"],"award-info":[{"award-number":["2021KJBS02"]}]},{"name":"Shandong University Facility Horticulture Laboratory","award":["2018YY041"],"award-info":[{"award-number":["2018YY041"]}]},{"DOI":"10.13039\/100014103","name":"Key Research and Development Program of Shandong Province","doi-asserted-by":"crossref","award":["2019GNC106135"],"award-info":[{"award-number":["2019GNC106135"]}],"id":[{"id":"10.13039\/100014103","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>\n                    <jats:italic>Bemisia tabaci<\/jats:italic>\n                    (Gennadius) and\n                    <jats:italic>Aphis gossypii<\/jats:italic>\n                    (Glover) are two notorious pests of vegetables grown in greenhouses and their outbreaks can be devastating and cause a significant loss in yield and quality. The prevail and effective control of the pests mainly relies on frequent applications of pesticides, which is likely to negatively impact environments and human health through residue, resurgence, and resistance. To avoid negative \u201c3R\u201d issues brought forth by chemicals, entomopathogenic fungus such as\n                    <jats:italic>Metarhizium<\/jats:italic>\n                    sp. are widely used as biocontrol agents even if they are different in their population, adaptability and pathogenicity among various species and isolates collected from different insect hosts and environments. To screen for the entomopathogenic fungi with optimal pathogenicity against the piercing-sucking pests\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    and\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    , we have isolated, purified four strains (SG-A, SG-B, SG-C, and SG-D) of\n                    <jats:italic>Metarhizium<\/jats:italic>\n                    sp. using yellow mealworms (\n                    <jats:italic>Tenebrio molitor<\/jats:italic>\n                    ) as the bait, and identified them as\n                    <jats:italic>Metarhizium pinghaense<\/jats:italic>\n                    morphologically and molecularly. Bioassay results have indicated that four isolates of\n                    <jats:italic>M. pingshaense<\/jats:italic>\n                    infected both\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    and\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    with some differences in the virulence and median lethal time. Both\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    and\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    nymphs showed an increase in the mortality rate as the spore concentration rose. Four\n                    <jats:italic>M. pingshaense<\/jats:italic>\n                    strains also exhibited the different pathogenicity against\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    and\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    at various levels: At an inoculum concentration of 1\u2009\u00d7\u200910\n                    <jats:sup>8<\/jats:sup>\n                    conidia\/mL, the cumulative corrected mortality of\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    nymphs 8 days post-treatment ranked in the order: SG\u2011A\u2009&gt;\u2009SG\u2011C\u2009&gt;\u2009SG\u2011B\u2009=\u2009SG\u2011D. For\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    , the cumulative corrected mortality followed the order: SG\u2011A\u2009&gt;\u2009SG\u2011B\u2009&gt;\u2009SG\u2011D\u2009&gt;\u2009SG\u2011C.Strain SG-A demonstrated the maximized pathogenicity against nymphs of\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    and\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    8 days after the treatment (LC\n                    <jats:sub>50<\/jats:sub>\n                    \u2009=\u20097.00\u2009\u00d7\u200910\n                    <jats:sup>4<\/jats:sup>\n                    and 4.21\u2009\u00d7\u200910\n                    <jats:sup>5<\/jats:sup>\n                    conidia\/mL, respectively). At the spore concentration at 1\u2009\u00d7\u200910\n                    <jats:sup>8<\/jats:sup>\n                    conidia\/mL, its cumulatively corrected mortality reached 94.44% and 96.67% (LT\n                    <jats:sub>50<\/jats:sub>\n                    \u2009=\u20094.13 d and 2.61 d, respectively). Strain SG-C showed an optimal pathogenicity against\n                    <jats:italic>B. tabaci<\/jats:italic>\n                    nymphs only with a cumulative corrected mortality of 87.78% and an LT\n                    <jats:sub>50<\/jats:sub>\n                    at 4.30 d 8 days after the treatment. In contrast, strain SG-B exhibited relatively high pathogenicity against\n                    <jats:italic>A. gossypii<\/jats:italic>\n                    nymphs only with a cumulative corrected mortality of 72.22% and an LT\n                    <jats:sub>50<\/jats:sub>\n                    at 2.31 d 8 days after the treatment. Therefore,\n                    <jats:italic>M. pinghaense<\/jats:italic>\n                    SG-A should be a potential biocontrol agent to manage whiteflies and aphids at their nymph stage during the vegetable production season.\n                  <\/jats:p>","DOI":"10.1371\/journal.pone.0338072","type":"journal-article","created":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T17:21:54Z","timestamp":1784740914000},"page":"e0338072","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["In vitro isolation and identification of entomopathogenic fungus (Metarhizium pinghaense) and assessment of its virulence against whiteflies and aphids"],"prefix":"10.1371","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-0619-683X","authenticated-orcid":true,"given":"Haiyan","family":"Hu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yali","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunyan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ranran","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fangyu","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1872-2584","authenticated-orcid":true,"given":"Xiaoan","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,7,22]]},"reference":[{"issue":"3","key":"pone.0338072.ref001","doi-asserted-by":"crossref","first-page":"198","DOI":"10.3390\/insects12030198","article-title":"Bemisia tabaci on Vegetables in the Southern United States: Incidence, Impact, and Management","volume":"12","author":"Y Li","year":"2021","journal-title":"Insects"},{"issue":"11","key":"pone.0338072.ref002","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.3390\/insects13111033","article-title":"Establishment of Toxicity and Susceptibility Baseline of Broflanilide for Aphis gossypii Glove","volume":"13","author":"R Li","year":"2022","journal-title":"Insects"},{"key":"pone.0338072.ref003","doi-asserted-by":"crossref","first-page":"106138","DOI":"10.1016\/j.pestbp.2024.106138","article-title":"Baseline susceptibility, risk assessment of resistance, changes in insecticides sensitivity and fitness after selection of dimpropyridaz in Aphis gossypii Glover (Hemiptera: Aphididae)","volume":"205","author":"J Shang","year":"2024","journal-title":"Pestic Biochem Physiol"},{"key":"pone.0338072.ref004","doi-asserted-by":"crossref","first-page":"140634","DOI":"10.1016\/j.ijbiomac.2025.140634","article-title":"Transcription factor CREB\/ATF regulates overexpression of CYP6CY14 conferring resistance to cycloxaprid in Aphis gossypii","volume":"303","author":"W Dong","year":"2025","journal-title":"Int J Biol Macromol"},{"key":"pone.0338072.ref005","doi-asserted-by":"crossref","first-page":"109653","DOI":"10.1016\/j.ecoenv.2019.109653","article-title":"Insecticidal efficacy of three benzoate derivatives against Aphis gossypii and its predator Chrysoperla carnea","volume":"184","author":"MM Mostafiz","year":"2019","journal-title":"Ecotoxicol Environ Saf"},{"key":"pone.0338072.ref006","doi-asserted-by":"crossref","first-page":"106272","DOI":"10.1016\/j.pestbp.2024.106272","article-title":"Cytochrome P450 CYP6EM1 confers resistance to thiamethoxam in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) via detoxification metabolism","volume":"208","author":"M Huang","year":"2025","journal-title":"Pestic Biochem Physiol"},{"issue":"11","key":"pone.0338072.ref007","doi-asserted-by":"crossref","first-page":"907","DOI":"10.3390\/insects15110907","article-title":"Evaluation of Different Mode of Action Insecticides for the Control of Bemisia tabaci; Enhancement of Pesticide Efficacy","volume":"15","author":"J Dunn","year":"2024","journal-title":"Insects"},{"issue":"9","key":"pone.0338072.ref008","doi-asserted-by":"crossref","first-page":"670","DOI":"10.3390\/insects15090670","article-title":"Susceptibility of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) Mediterranean Populations Found in S\u00e3o Paulo, Brazil to 11 Insecticides and Characterization of Their Endosymbionts","volume":"15","author":"L Alvarez D de","year":"2024","journal-title":"Insects"},{"issue":"2","key":"pone.0338072.ref009","doi-asserted-by":"crossref","first-page":"283","DOI":"10.3390\/microorganisms13020283","article-title":"Parasitism by Entomopathogenic Fungi and Insect Host Defense Strategies","volume":"13","author":"D Zhang","year":"2025","journal-title":"Microorganisms"},{"issue":"7","key":"pone.0338072.ref010","doi-asserted-by":"crossref","first-page":"6048","DOI":"10.3390\/ijms24076048","article-title":"Insecticide Resistance and Its Management in Two Invasive Cryptic Species of Bemisia tabaci in China","volume":"24","author":"Q Wang","year":"2023","journal-title":"Int J Mol Sci"},{"issue":"3","key":"pone.0338072.ref011","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1002\/ps.7274","article-title":"Imidacloprid-resistant Aphis gossypii populations are more common in cotton-dominated landscapes","volume":"79","author":"JW Mahas","year":"2023","journal-title":"Pest Manag Sci"},{"issue":"3","key":"pone.0338072.ref012","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.biocontrol.2007.08.001","article-title":"Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types","volume":"43","author":"de Faria MR","year":"2007","journal-title":"Biological Control"},{"issue":"1","key":"pone.0338072.ref013","article-title":"Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum","volume":"7","author":"Q Gao","year":"2011","journal-title":"PLoS Genet"},{"key":"pone.0338072.ref014","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1146\/annurev-ento-031616-035509","article-title":"Insect pathogenic fungi: Genomics, molecular interactions, and genetic improvements","volume":"62","author":"C Wang","year":"2017","journal-title":"Annu Rev Entomol"},{"issue":"4","key":"pone.0338072.ref015","doi-asserted-by":"crossref","first-page":"117","DOI":"10.3390\/insects10040117","article-title":"First Screening of Entomopathogenic Nematodes and Fungus as Biocontrol Agents against an Emerging Pest of Sugarcane, Cacosceles newmannii (Coleoptera: Cerambycidae)","volume":"10","author":"M Javal","year":"2019","journal-title":"Insects"},{"issue":"1","key":"pone.0338072.ref016","first-page":"50","article-title":"Differential Susceptibility of Bagrada hilaris (Hemiptera: Pentatomidae) to Different Species of Fungal Pathogens","volume":"113","author":"AA Barrera-L\u00f3pez","year":"2020","journal-title":"J Econ Entomol"},{"issue":"7","key":"pone.0338072.ref017","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0255029","article-title":"Pathogenicity of local and exotic entomopathogenic fungi isolates against different life stages of red palm weevil (Rhynchophorus ferrugineus)","volume":"16","author":"KD Sutanto","year":"2021","journal-title":"PLoS One"},{"issue":"4","key":"pone.0338072.ref018","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1603\/0022-0493-95.4.675","article-title":"Pathogenicity of Beauveria bassiana, Metarhizium anisopliae (Deuteromycotina: Hyphomycetes), and other entomopathogenic fungi against Lygus lineolaris (Hemiptera: Miridae)","volume":"95","author":"H Liu","year":"2002","journal-title":"J Econ Entomol"},{"key":"pone.0338072.ref019","doi-asserted-by":"crossref","first-page":"106350","DOI":"10.1016\/j.pestbp.2025.106350","article-title":"Insecticidal effect and mechanism of Metarhizium anisopliae ZHKUJGZ1 against Solenopsis invicta (Hymenoptera: Formicidae)","volume":"209","author":"S Meng","year":"2025","journal-title":"Pestic Biochem Physiol"},{"issue":"2","key":"pone.0338072.ref020","doi-asserted-by":"crossref","DOI":"10.1002\/arch.70020","article-title":"Metarhizium anisopliae JEF-197 Loses Glucose Metabolism in Surviving Japanese Pine Sawyer Beetle Against the Fungal Pathogen","volume":"118","author":"G Song","year":"2025","journal-title":"Arch Insect Biochem Physiol"},{"issue":"1","key":"pone.0338072.ref021","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1080\/21501203.2018.1524799","article-title":"Isolation of Metarhizium spp. from rhizosphere soils of wild plants reflects fungal diversity in soil but not plant specificity","volume":"10","author":"O Nishi","year":"2018","journal-title":"Mycology"},{"issue":"2","key":"pone.0338072.ref022","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1111\/1574-6968.12470","article-title":"Characterization and comparison of Metarhizium strains isolated from Rhynchophorus ferrugineus","volume":"355","author":"A Cito","year":"2014","journal-title":"FEMS Microbiol Lett"},{"key":"pone.0338072.ref023","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.pmpp.2017.06.004","article-title":"Virulence of selected indigenous Metarhizium pingshaense (Ascomycota: Hypocreales) isolates against the rice leaffolder, Cnaphalocrocis medinalis (Guen\u00e8e) (Lepidoptera: Pyralidae)","volume":"101","author":"SA Kirubakaran","year":"2018","journal-title":"Physiological and Molecular Plant Pathology"},{"key":"pone.0338072.ref024","volume-title":"Methods for Isolation of Entomopathogenic Fungi from the Soil Environment","author":"NV Meyling","year":"2007"},{"key":"pone.0338072.ref025","doi-asserted-by":"crossref","first-page":"1164511","DOI":"10.3389\/fmicb.2023.1164511","article-title":"Isolation of a highly virulent Metarhizium strain targeting the tea pest, Ectropis obliqua","volume":"14","author":"J Zhao","year":"2023","journal-title":"Front Microbiol"},{"issue":"6","key":"pone.0338072.ref026","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"S Kumar","year":"2018","journal-title":"Mol Biol Evol"},{"key":"pone.0338072.ref027","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.jip.2015.06.010","article-title":"Metarhizium pingshaense applied as a seed treatment induces fungal infection in larvae of the white grub Anomala cincta","volume":"130","author":"AJ Pe\u00f1a-Pe\u00f1a","year":"2015","journal-title":"J Invertebr Pathol"},{"key":"pone.0338072.ref028","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.simyco.2020.04.001","article-title":"Revisiting Metarhizium and the description of new species from Thailand","volume":"95","author":"S Mongkolsamrit","year":"2020","journal-title":"Stud Mycol"},{"issue":"11","key":"pone.0338072.ref029","doi-asserted-by":"crossref","DOI":"10.1016\/j.heliyon.2021.e08277","article-title":"Virulence and horizontal transmission of Metarhizium anisopliae by the adults of the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) and the efficacy of oil formulations against its nymphs","volume":"7","author":"VM Paradza","year":"2021","journal-title":"Heliyon"},{"key":"pone.0338072.ref030","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1093\/jee\/18.2.265a","article-title":"A method of computing the effectiveness of an insecticide","volume":"18","author":"WS Abbott","year":"1925","journal-title":"J Econ Entomol"},{"key":"pone.0338072.ref031","doi-asserted-by":"crossref","first-page":"126645","DOI":"10.1016\/j.micres.2020.126645","article-title":"Characterization and biocontrol potential of a naturally occurring isolate of Metarhizium pingshaense infecting Conogethes punctiferalis","volume":"243","author":"CM Senthil Kumar","year":"2021","journal-title":"Microbiol Res"},{"issue":"4","key":"pone.0338072.ref032","doi-asserted-by":"crossref","first-page":"512","DOI":"10.3852\/07-202","article-title":"A multilocus phylogeny of the Metarhizium anisopliae lineage","volume":"101","author":"JF Bischoff","year":"2009","journal-title":"Mycologia"},{"key":"pone.0338072.ref033","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.simyco.2020.04.001","article-title":"Revisiting Metarhizium and the description of new species from Thailand","volume":"95","author":"S Mongkolsamrit","year":"2020","journal-title":"Stud Mycol"},{"issue":"4","key":"pone.0338072.ref034","doi-asserted-by":"crossref","first-page":"3625","DOI":"10.1002\/ps.70484","article-title":"Functional characterization of Hsk1 and Chit1 genes in the virulence of Metarhizium guizhouense Xct1 via CRISPR-Cas9-mediated gene editing","volume":"82","author":"J Wei","year":"2026","journal-title":"Pest Manag Sci"},{"issue":"1","key":"pone.0338072.ref035","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1186\/s13104-022-06004-4","article-title":"Extracellular enzyme activity of entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae and their pathogenicity potential as a bio-control agent against whitefly pests, Bemisia tabaci and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)","volume":"15","author":"A Gebremariam","year":"2022","journal-title":"BMC Res Notes"},{"issue":"3","key":"pone.0338072.ref036","first-page":"127","article-title":"Infectivity of five Metarhizium anisopliae (Deuteromycota: Hyphomycetales) strains on whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) infesting brinjal, Solanum melongena (Solanaceae)","volume":"6","author":"L Norhelina","year":"2013","journal-title":"AJ Entomol"},{"issue":"11","key":"pone.0338072.ref037","article-title":"Potential of Cameroonian isolates of Beauveria bassiana and Metarhizium anisopliae for the biocontrol of the banana aphid, Pentalonia nigronervosa, vector of banana bunchy top virus","volume":"19","author":"AC Enoh","year":"2024","journal-title":"PLoS One"},{"key":"pone.0338072.ref038","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0065-2296(05)40006-3","article-title":"Fungal pathogens of insects: Cuticle degrading enzymes and toxins","volume":"40","author":"AK Charnley","year":"2003","journal-title":"Adv Bot Res"}],"container-title":["PLOS One"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0338072","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T17:22:06Z","timestamp":1784740926000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0338072"}},"subtitle":[],"editor":[{"given":"Rachid","family":"Bouharroud","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,7,22]]},"references-count":38,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2026,7,22]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0338072","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,22]]}}}