{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T04:08:09Z","timestamp":1790309289207,"version":"4.1.0"},"reference-count":93,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2022,11,10]],"date-time":"2022-11-10T00:00:00Z","timestamp":1668038400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003627","name":"Rural Development Administration of Korea","doi-asserted-by":"crossref","award":["PJ015778012022"],"award-info":[{"award-number":["PJ015778012022"]}],"id":[{"id":"10.13039\/501100003627","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Recently, pesticides have been suggested to be one of the factors responsible for the large-scale decline in honey bee populations, including colony collapse disorder. The identification of the genes that respond to pesticide exposure based on their expression is essential for understanding the xenobiotic detoxification metabolism in honey bees. For the accurate determination of target gene expression by quantitative real-time PCR, the expression stability of reference genes should be validated in honey bees exposed to various pesticides. Therefore, in this study, to select the optimal reference genes, we analyzed the amplification efficiencies of five candidate reference genes (<jats:italic>RPS5<\/jats:italic>, <jats:italic>RPS18<\/jats:italic>, <jats:italic>GAPDH<\/jats:italic>, <jats:italic>ARF1<\/jats:italic>, and <jats:italic>RAD1a<\/jats:italic>) and their expression stability values using four programs (geNorm, NormFinder, BestKeeper, and RefFinder) across samples of five body parts (head, thorax, gut, fat body, and carcass) from honey bees exposed to seven pesticides (acetamiprid, imidacloprid, flupyradifurone, fenitrothion, carbaryl, amitraz, and bifenthrin). Among these five candidate genes, a combination of <jats:italic>RAD1a<\/jats:italic> and <jats:italic>RPS18<\/jats:italic> was suggested for target gene normalization. Subsequently, expression levels of six genes (<jats:italic>AChE1<\/jats:italic>, <jats:italic>CYP9Q1<\/jats:italic>, <jats:italic>CYP9Q2<\/jats:italic>, <jats:italic>CYP9Q3<\/jats:italic>, <jats:italic>CAT<\/jats:italic>, and <jats:italic>SOD1<\/jats:italic>) were normalized with a combination of <jats:italic>RAD1a<\/jats:italic> and <jats:italic>RPS18<\/jats:italic> in the different body parts from honey bees exposed to pesticides. Among the six genes in the five body parts, the expression of <jats:italic>SOD1<\/jats:italic> in the head, fat body, and carcass was significantly induced by six pesticides. In addition, among seven pesticides, flupyradifurone statistically induced expression levels of five genes in the fat body.<\/jats:p>","DOI":"10.1371\/journal.pone.0277455","type":"journal-article","created":{"date-parts":[[2022,11,10]],"date-time":"2022-11-10T18:39:07Z","timestamp":1668105547000},"page":"e0277455","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["Validation of quantitative real-time PCR reference genes and spatial expression profiles of detoxication-related genes under pesticide induction in honey bee, Apis mellifera"],"prefix":"10.1371","volume":"17","author":[{"given":"YeongHo","family":"Kim","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyemin","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"JooHeon","family":"Cha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Si Hyeock","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0003-6604","authenticated-orcid":true,"given":"Young Ho","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,11,10]]},"reference":[{"issue":"1","key":"pone.0277455.ref001","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/s10661-008-0518-9","article-title":"Impact assessment of pesticide residues in fish of Ganga river around Kolkata in West Bengal","volume":"157","author":"M Aktar","year":"2009","journal-title":"Environ Monit Assess"},{"issue":"6","key":"pone.0277455.ref002","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1016\/j.trac.2011.02.008","article-title":"Properties and determination of pesticides in fruits and vegetables","volume":"30","author":"J Fenik","year":"2011","journal-title":"TrAC\u2014Trends Anal Chem"},{"key":"pone.0277455.ref003","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.cropro.2016.11.036","article-title":"SYNOPS-WEB, an online tool for environmental risk assessment to evaluate pesticide strategies on field level","volume":"97","author":"J Strassemeyer","year":"2017","journal-title":"J Crop Prot"},{"issue":"3","key":"pone.0277455.ref004","first-page":"1112","article-title":"Agriculture development, pesticide application and its impact on the environment","volume":"18","author":"M Tudi","year":"2021","journal-title":"Int J Environ Res"},{"key":"pone.0277455.ref005","unstructured":"FAO. Consumption of pesticides worldwide from 1990 to 2019: Luc\u00eda Fern\u00e1ndez; 2021 [updated 27 September 2021]. Available from: https:\/\/www.statista.com\/statistics\/1263077\/global-pesticide-agricultural-use\/."},{"key":"pone.0277455.ref006","volume-title":"Honey bee colony collapse disorder","author":"R. Johnson","year":"2010"},{"issue":"6229","key":"pone.0277455.ref007","doi-asserted-by":"crossref","first-page":"1255957","DOI":"10.1126\/science.1255957","article-title":"Bee declines driven by combined stress from parasites, pesticides, and lack of flowers","volume":"347","author":"D Goulson","year":"2015","journal-title":"Science"},{"issue":"2","key":"pone.0277455.ref008","first-page":"499","article-title":"Climate change: impact on honey bee populations and diseases","volume":"27","author":"Y Le Conte","year":"2008","journal-title":"Rev sci tech"},{"issue":"4","key":"pone.0277455.ref009","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1098\/rsbl.2009.0986","article-title":"Diet effects on honeybee immunocompetence","volume":"6","author":"C Alaux","year":"2010","journal-title":"Biol Lett"},{"issue":"10","key":"pone.0277455.ref010","doi-asserted-by":"crossref","first-page":"e13181","DOI":"10.1371\/journal.pone.0013181","article-title":"Iridovirus and microsporidian linked to honey bee colony decline","volume":"5","author":"JJ Bromenshenk","year":"2010","journal-title":"PLoS One"},{"key":"pone.0277455.ref011","unstructured":"VanEngelsdorp D, Foster DC, Frazier M, Ostiguy N, Hayes J. \" Fall-dwindle disease\": Investigations into the causes of sudden and alarming colony losses experience by beekeepers in the fall of 2006: Florida Department of Agriculture; 2007 [updated 15 December 2006]. Available from: https:\/\/www.fdacs.gov\/content\/download\/24049\/file\/fall_dwindle_report.pdf\/."},{"issue":"1","key":"pone.0277455.ref012","first-page":"125","article-title":"Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder","volume":"67","author":"L Chensheng","year":"2014","journal-title":"Bull Insectology"},{"issue":"8","key":"pone.0277455.ref013","doi-asserted-by":"crossref","first-page":"e6481","DOI":"10.1371\/journal.pone.0006481","article-title":"Colony collapse disorder: a descriptive study","volume":"4","author":"D VanEngelsdorp","year":"2009","journal-title":"PLoS One"},{"key":"pone.0277455.ref014","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1146\/annurev.ento.52.110405.091440","article-title":"The sublethal effects of pesticides on beneficial arthropods","volume":"52","author":"N Desneux","year":"2007","journal-title":"Annu Rev Entomol"},{"issue":"10","key":"pone.0277455.ref015","first-page":"1799","article-title":"Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees","volume":"216","author":"SM Williamson","year":"2013","journal-title":"J Exp Biol"},{"issue":"1","key":"pone.0277455.ref016","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1023\/A:1022575315413","article-title":"Behavioural effects of pesticides in bees\u2013their potential for use in risk assessment","volume":"12","author":"HM Thompson","year":"2003","journal-title":"Ecotoxicology"},{"issue":"1","key":"pone.0277455.ref017","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep00326","article-title":"Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee","volume":"2","author":"J Aufauvre","year":"2012","journal-title":"Sci Rep"},{"issue":"2","key":"pone.0277455.ref018","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1093\/jee\/99.2.253","article-title":"A survey of pesticide residues in pollen loads collected by honey bees in France","volume":"99","author":"M-P Chauzat","year":"2006","journal-title":"J Econ Entomol"},{"issue":"3","key":"pone.0277455.ref019","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1007\/s00128-009-9762-0","article-title":"Residues of pesticides in honeybee (Apis mellifera carnica) bee bread and in pollen loads from treated apple orchards","volume":"83","author":"MI Smodi\u0161 \u0160kerl","year":"2009","journal-title":"Bull Environ Contam Toxicol"},{"key":"pone.0277455.ref020","doi-asserted-by":"crossref","first-page":"2321","DOI":"10.1016\/j.chemosphere.2015.10.135","article-title":"Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada","volume":"144","author":"G Codling","year":"2016","journal-title":"Chemosphere"},{"issue":"6359","key":"pone.0277455.ref021","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1126\/science.aan3684","article-title":"A worldwide survey of neonicotinoids in honey","volume":"358","author":"EA Mitchell","year":"2017","journal-title":"Science"},{"issue":"7","key":"pone.0277455.ref022","doi-asserted-by":"crossref","first-page":"e0199995","DOI":"10.1371\/journal.pone.0199995","article-title":"Pesticide residue survey of pollen loads collected by honeybees (Apis mellifera) in daily intervals at three agricultural sites in South Germany","volume":"13","author":"F B\u00f6hme","year":"2018","journal-title":"PLoS One"},{"issue":"1","key":"pone.0277455.ref023","doi-asserted-by":"crossref","first-page":"75","DOI":"10.2144\/05391RV01","article-title":"Real-time PCR for mRNA quantitation","volume":"39","author":"ML Wong","year":"2005","journal-title":"Biotechniques"},{"issue":"3","key":"pone.0277455.ref024","doi-asserted-by":"crossref","first-page":"e17762","DOI":"10.1371\/journal.pone.0017762","article-title":"Robust RT-qPCR data normalization: validation and selection of internal reference genes during post-experimental data analysis","volume":"6","author":"D Ling","year":"2011","journal-title":"PLoS One"},{"issue":"9","key":"pone.0277455.ref025","doi-asserted-by":"crossref","first-page":"e106800","DOI":"10.1371\/journal.pone.0106800","article-title":"Identification and validation of reference genes for quantitative real-time PCR in Drosophila suzukii (Diptera: Drosophilidae)","volume":"9","author":"Y Zhai","year":"2014","journal-title":"PLoS One"},{"issue":"3","key":"pone.0277455.ref026","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1007\/s13592-012-0184-3","article-title":"Suitability of three common reference genes for quantitative real-time PCR in honey bees","volume":"44","author":"T Reim","year":"2013","journal-title":"Apidologie"},{"issue":"4","key":"pone.0277455.ref027","first-page":"251","article-title":"Evaluation of quantitative real-time PCR reference genes for the investigation of gene expression profiles in honeybee developmental stages","volume":"36","author":"Y Kim","year":"2021","journal-title":"J Apic"},{"issue":"7","key":"pone.0277455.ref028","doi-asserted-by":"crossref","first-page":"e0200369","DOI":"10.1371\/journal.pone.0200369","article-title":"Validation of quantitative real-time PCR reference genes for the determination of seasonal and labor-specific gene expression profiles in the head of Western honey bee, Apis mellifera","volume":"13","author":"K Moon","year":"2018","journal-title":"PLoS One"},{"issue":"1","key":"pone.0277455.ref029","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1673\/031.008.3301","article-title":"Reference gene selection for insect expression studies using quantitative real-time PCR: The head of the honeybee, Apis mellifera, after a bacterial challenge","volume":"8","author":"B Scharlaken","year":"2008","journal-title":"J Insect Sci"},{"issue":"1","key":"pone.0277455.ref030","first-page":"1","article-title":"Reference gene selection for qRT-PCR analysis of season-and tissue-specific gene expression profiles in the honey bee Apis mellifera","volume":"10","author":"JH Jeon","year":"2020","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0277455.ref031","doi-asserted-by":"crossref","first-page":"16140","DOI":"10.1038\/s41598-020-73125-w","article-title":"Evaluation of the expression stability of reference genes in Apis mellifera under pyrethroid treatment","volume":"10","author":"P Wieczorek","year":"2020","journal-title":"Sci Rep"},{"key":"pone.0277455.ref032","first-page":"1","article-title":"Selection of stable reference genes for real-time quantitative PCR in honey bee pesticide toxicity studies","author":"S Kim","year":"2021","journal-title":"J Apic Res"},{"issue":"11","key":"pone.0277455.ref033","doi-asserted-by":"crossref","first-page":"e0188004","DOI":"10.1371\/journal.pone.0188004","article-title":"Resilience of honeybee colonies via common stomach: A model of self-regulation of foraging","volume":"12","author":"T Schmickl","year":"2017","journal-title":"PloS one"},{"issue":"1900","key":"pone.0277455.ref034","doi-asserted-by":"crossref","first-page":"20190433","DOI":"10.1098\/rspb.2019.0433","article-title":"Lethal and sublethal synergistic effects of a new systemic pesticide, flupyradifurone (Sivanto\u00ae), on honeybees","volume":"286","author":"S Tosi","year":"2019","journal-title":"Proc R Soc B"},{"key":"pone.0277455.ref035","first-page":"014795","article-title":"Long-term field experiment on the impacts of the neonicotinoid dinotefuran and the organophosphate fenitrothion on a honeybee colony","author":"T Yamada","year":"2015","journal-title":"bioRxiv"},{"issue":"1","key":"pone.0277455.ref036","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13765-019-0415-7","article-title":"Effect of transient exposure to carbaryl wettable powder on the gut microbial community of honey bees","volume":"62","author":"K Nogrado","year":"2019","journal-title":"Appl Biol Chem"},{"issue":"3","key":"pone.0277455.ref037","doi-asserted-by":"crossref","first-page":"297","DOI":"10.2478\/jvetres-2018-0043","article-title":"Amitraz marker residues in honey from honeybee colonies treated with Apiwarol","volume":"62","author":"K Pohorecka","year":"2018","journal-title":"J Vet Res"},{"issue":"3","key":"pone.0277455.ref038","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1002\/etc.67","article-title":"Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica","volume":"29","author":"PL Dai","year":"2010","journal-title":"Environ Toxicol Chem"},{"issue":"1","key":"pone.0277455.ref039","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep16224","article-title":"Forager bees (Apis mellifera) highly express immune and detoxification genes in tissues associated with nectar processing","volume":"5","author":"RL Vannette","year":"2015","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0277455.ref040","first-page":"1","article-title":"Expression of acetylcholinesterase 1 is associated with brood rearing status in the honey bee, Apis mellifera","volume":"7","author":"YH Kim","year":"2017","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0277455.ref041","first-page":"1","article-title":"Differential expression of acetylcholinesterase 1 in response to various stress factors in honey bee workers","volume":"9","author":"S Kim","year":"2019","journal-title":"Sci Rep"},{"issue":"11","key":"pone.0277455.ref042","doi-asserted-by":"crossref","first-page":"e48838","DOI":"10.1371\/journal.pone.0048838","article-title":"Molecular and kinetic properties of two acetylcholinesterases from the western honey bee, Apis mellifera","volume":"7","author":"YH Kim","year":"2012","journal-title":"PLoS One"},{"issue":"4","key":"pone.0277455.ref043","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.cbpb.2009.08.008","article-title":"Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae)","volume":"154","author":"W Mao","year":"2009","journal-title":"Comp Biochem Physiol B, Biochem Mol Biol"},{"issue":"7","key":"pone.0277455.ref044","doi-asserted-by":"crossref","DOI":"10.1016\/j.cub.2018.02.045","article-title":"Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides","volume":"28","author":"C Manjon","year":"2018","journal-title":"Curr Biol"},{"issue":"31","key":"pone.0277455.ref045","doi-asserted-by":"crossref","first-page":"12657","DOI":"10.1073\/pnas.1109535108","article-title":"CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera)","volume":"108","author":"W Mao","year":"2011","journal-title":"Proc Natl Acad Sci"},{"issue":"1","key":"pone.0277455.ref046","doi-asserted-by":"crossref","first-page":"11779","DOI":"10.1038\/srep11779","article-title":"Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine","volume":"5","author":"EEd Rand","year":"2015","journal-title":"Sci Rep"},{"issue":"5","key":"pone.0277455.ref047","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1111\/j.1365-2583.2006.00695.x","article-title":"Genes of the antioxidant system of the honey bee: annotation and phylogeny","volume":"15","author":"M Corona","year":"2006","journal-title":"Insect Mol Biol"},{"issue":"3","key":"pone.0277455.ref048","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1007\/s00040-008-0995-4","article-title":"Mortality rates of honey bees in the wild","volume":"55","author":"R. Dukas","year":"2008","journal-title":"Insectes Soc"},{"issue":"3","key":"pone.0277455.ref049","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1007\/s13592-019-00645-4","article-title":"Gene expression, sperm viability, and queen (Apis mellifera) loss following pesticide exposure under laboratory and field conditions","volume":"50","author":"V Chaimanee","year":"2019","journal-title":"Apidologie"},{"issue":"4","key":"pone.0277455.ref050","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1007\/s13592-020-00751-8","article-title":"Effect of environmental heavy metals on the expression of detoxification-related genes in honey bee Apis mellifera","volume":"51","author":"G Gizaw","year":"2020","journal-title":"Apidologie"},{"issue":"7","key":"pone.0277455.ref051","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2002-3-7-research0034","article-title":"Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes","volume":"3","author":"J Vandesompele","year":"2002","journal-title":"Genome Biol"},{"issue":"15","key":"pone.0277455.ref052","doi-asserted-by":"crossref","first-page":"5245","DOI":"10.1158\/0008-5472.CAN-04-0496","article-title":"Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets","volume":"64","author":"CL Andersen","year":"2004","journal-title":"Cancer Res"},{"issue":"6","key":"pone.0277455.ref053","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1023\/B:BILE.0000019559.84305.47","article-title":"Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper\u2013Excel-based tool using pair-wise correlations","volume":"26","author":"MW Pfaffl","year":"2004","journal-title":"Biotechnol Lett"},{"issue":"1","key":"pone.0277455.ref054","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s11103-012-9885-2","article-title":"miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs","volume":"80","author":"F Xie","year":"2012","journal-title":"Plant Mol Biol"},{"issue":"9","key":"pone.0277455.ref055","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT\u2013PCR","volume":"29","author":"MW Pfaffl","year":"2001","journal-title":"Nucleic Acids Res"},{"issue":"43","key":"pone.0277455.ref056","article-title":"Performance of some estimators of relative variability","volume":"5","author":"R Ospina","year":"2019","journal-title":"Front Appl Math Stat"},{"key":"pone.0277455.ref057","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1590\/S1806-37562015000000133","article-title":"Analysis of the stability of housekeeping gene expression in the left cardiac ventricle of rats submitted to chronic intermittent hypoxia","volume":"42","author":"GS Julian","year":"2016","journal-title":"J Bras Pneumol"},{"issue":"5","key":"pone.0277455.ref058","doi-asserted-by":"crossref","first-page":"e98162","DOI":"10.1371\/journal.pone.0098162","article-title":"Evaluation of reference genes for gene expression analysis using quantitative RT-PCR in Azospirillum brasilense","volume":"9","author":"M McMillan","year":"2014","journal-title":"PLoS One"},{"issue":"4","key":"pone.0277455.ref059","doi-asserted-by":"crossref","first-page":"e32265","DOI":"10.1371\/journal.pone.0032265","article-title":"Validation of reference genes for the relative quantification of gene expression in human epicardial adipose tissue","volume":"7","author":"K Chechi","year":"2012","journal-title":"PLoS One"},{"issue":"2","key":"pone.0277455.ref060","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2007-8-2-r19","article-title":"qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data","volume":"8","author":"J Hellemans","year":"2007","journal-title":"Genome Biol"},{"issue":"11","key":"pone.0277455.ref061","doi-asserted-by":"crossref","first-page":"e112177","DOI":"10.1371\/journal.pone.0112177","article-title":"Selection of reference genes for quantitative real-time PCR normalization in Panax ginseng at different stages of growth and in different organs","volume":"9","author":"J Liu","year":"2014","journal-title":"PloS one"},{"issue":"2","key":"pone.0277455.ref062","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.ab.2009.12.008","article-title":"Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber","volume":"399","author":"H Wan","year":"2010","journal-title":"Anal Biochem"},{"issue":"2","key":"pone.0277455.ref063","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.aspen.2020.01.008","article-title":"Evaluation of reference genes for gene expression studies using quantitative real-time PCR in Drosophila melanogaster after chemical exposures","volume":"23","author":"Y Kim","year":"2020","journal-title":"J Asia Pac Entomol"},{"issue":"1","key":"pone.0277455.ref064","doi-asserted-by":"crossref","first-page":"13291","DOI":"10.1038\/s41598-019-49479-1","article-title":"Evaluation and validation of reference genes for quantitative real-time PCR in Helopeltis theivora Waterhouse (Hemiptera: Miridae)","volume":"9","author":"Z Wang","year":"2019","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0277455.ref065","doi-asserted-by":"crossref","first-page":"10362","DOI":"10.1038\/s41598-020-67035-0","article-title":"Validation of reference genes for the normalization of RT-qPCR gene expression in Acanthamoeba spp","volume":"10","author":"M K\u00f6hsler","year":"2020","journal-title":"Sci Rep"},{"issue":"1","key":"pone.0277455.ref066","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1746-6148-3-7","article-title":"Expression stability of commonly used reference genes in canine articular connective tissues","volume":"3","author":"D Ayers","year":"2007","journal-title":"BMC Vet Res"},{"issue":"1","key":"pone.0277455.ref067","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12896-021-00685-8","article-title":"Optimizations for identifying reference genes in bone and cartilage bioengineering","volume":"21","author":"F Xiong","year":"2021","journal-title":"BMC Biotechnol"},{"issue":"4","key":"pone.0277455.ref068","doi-asserted-by":"crossref","first-page":"1350","DOI":"10.1016\/j.aspen.2018.10.014","article-title":"Evaluation of reference genes for quantitative real-time PCR to investigate seasonal and labor-specific expression profiles of the honey bee abdomen","volume":"21","author":"K Moon","year":"2018","journal-title":"J Asia Pac Entomol"},{"issue":"1","key":"pone.0277455.ref069","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.taap.2004.11.003","article-title":"Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos","volume":"206","author":"D Qiao","year":"2005","journal-title":"Toxicol Appl Pharmacol"},{"issue":"22","key":"pone.0277455.ref070","doi-asserted-by":"crossref","first-page":"6049","DOI":"10.1016\/S0021-9258(18)63504-5","article-title":"Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein)","volume":"244","author":"JM McCord","year":"1969","journal-title":"J Biol Chem"},{"key":"pone.0277455.ref071","first-page":"1","volume-title":"Superoxide dismutase in biology and medicine","author":"I. Fridovich","year":"1982","edition":"1"},{"issue":"2","key":"pone.0277455.ref072","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.envpol.2004.05.035","article-title":"Effects of some environmental parameters on catalase activity measured in the mussel (Mytilus galloprovincialis) exposed to lindane","volume":"133","author":"A Khessiba","year":"2005","journal-title":"Environ Pollut"},{"key":"pone.0277455.ref073","volume-title":"Freshwater biological indicators of pesticide contamination","author":"C Schriever","year":"2008"},{"issue":"1","key":"pone.0277455.ref074","doi-asserted-by":"crossref","first-page":"36","DOI":"10.3390\/insects2010036","article-title":"Metabolic resistance in bed bugs","volume":"2","author":"P Mamidala","year":"2011","journal-title":"Insects"},{"key":"pone.0277455.ref075","volume-title":"Methods for assessing exposure of insects","author":"V Landa","year":"1991"},{"issue":"1","key":"pone.0277455.ref076","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1051\/apido:2001001","article-title":"Antioxidant enzymes in the honey bee, Apis mellifera","volume":"33","author":"GF Weirich","year":"2002","journal-title":"Apidologie"},{"issue":"11","key":"pone.0277455.ref077","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1134\/S0006297914110066","article-title":"Unexpectedly strong effect of caffeine on the vitality of western honeybees (Apis mellifera)","volume":"79","author":"A Strachecka","year":"2014","journal-title":"Biochem (Mosc)"},{"issue":"1","key":"pone.0277455.ref078","first-page":"129","article-title":"Curcumin stimulates biochemical mechanisms of Apis mellifera resistance and extends the apian life-span","volume":"59","author":"AJ Strachecka","year":"2015","journal-title":"J Apic Sci"},{"issue":"5","key":"pone.0277455.ref079","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1007\/s13592-018-0583-1","article-title":"Imidacloprid-induced oxidative stress in honey bees and the antioxidant action of caffeine","volume":"49","author":"KVB Balieira","year":"2018","journal-title":"Apidologie"},{"issue":"1","key":"pone.0277455.ref080","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1007\/s13592-014-0308-z","article-title":"Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states","volume":"46","author":"P Chakrabarti","year":"2015","journal-title":"Apidologie"},{"issue":"3","key":"pone.0277455.ref081","doi-asserted-by":"crossref","first-page":"104","DOI":"10.3390\/toxics10030104","article-title":"Toxicity of the pesticides imidacloprid, difenoconazole and glyphosate alone and in binary and ternary mixtures to winter honey bees: effects on survival and antioxidative defenses","volume":"10","author":"E Pal","year":"2022","journal-title":"Toxics"},{"key":"pone.0277455.ref082","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1007\/978-3-642-59549-3_14","volume-title":"Biochemical sites of insecticide action and resistance","author":"G Smagghe","year":"2001"},{"issue":"4","key":"pone.0277455.ref083","doi-asserted-by":"crossref","first-page":"1201","DOI":"10.1111\/1751-7915.13579","article-title":"Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract","volume":"13","author":"Y Wu","year":"2020","journal-title":"Microb Biotechnol"},{"key":"pone.0277455.ref084","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.jinsphys.2016.10.017","article-title":"The metabolic fate of nectar nicotine in worker honey bees","volume":"98","author":"E Esther","year":"2017","journal-title":"J Insect Physiol"},{"issue":"3","key":"pone.0277455.ref085","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/0048-3575(84)90029-4","article-title":"Detoxication capacity in the honey bee, Apis mellifera L","volume":"22","author":"S Yu","year":"1984","journal-title":"Pestic Biochem Physiol"},{"issue":"2","key":"pone.0277455.ref086","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.gene.2016.02.016","article-title":"Characterization of an Apis cerana cerana cytochrome P450 gene (AccCYP336A1) and its roles in oxidative stresses responses","volume":"584","author":"M Zhu","year":"2016","journal-title":"Gene"},{"key":"pone.0277455.ref087","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.cois.2015.03.005","article-title":"Xenobiotic detoxification pathways in honey bees","volume":"10","author":"MR Berenbaum","year":"2015","journal-title":"Curr Opin Insect Sci"},{"issue":"1","key":"pone.0277455.ref088","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.ibmb.2012.11.004","article-title":"Which acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta?","volume":"43","author":"YH Kim","year":"2013","journal-title":"Insect Biochem Mol Biol"},{"issue":"4","key":"pone.0277455.ref089","doi-asserted-by":"crossref","first-page":"e19063","DOI":"10.1371\/journal.pone.0019063","article-title":"A soluble acetylcholinesterase provides chemical defense against xenobiotics in the pinewood nematode","volume":"6","author":"JS Kang","year":"2011","journal-title":"PLoS One"},{"key":"pone.0277455.ref090","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ibmb.2014.03.001","article-title":"Induction of soluble AChE expression via alternative splicing by chemical stress in Drosophila melanogaster","volume":"48","author":"YH Kim","year":"2014","journal-title":"Insect Biochem Mol Biol"},{"key":"pone.0277455.ref091","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1016\/j.scitotenv.2017.09.226","article-title":"A 3-year survey of Italian honey bee-collected pollen reveals widespread contamination by agricultural pesticides","volume":"615","author":"S Tosi","year":"2018","journal-title":"Sci Total Environ"},{"issue":"1","key":"pone.0277455.ref092","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/s11356-014-3470-y","article-title":"Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites","volume":"22","author":"N Simon-Delso","year":"2015","journal-title":"Environ Sci Pollut Res Int"},{"issue":"14","key":"pone.0277455.ref093","article-title":"Effects of flight activity and age on oxidative damage in the honey bee, Apis mellifera","volume":"221","author":"JW Margotta","year":"2018","journal-title":"J Exp Biol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0277455","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,10]],"date-time":"2022-11-10T18:40:30Z","timestamp":1668105630000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0277455"}},"subtitle":[],"editor":[{"given":"J. Joe","family":"Hull","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,11,10]]},"references-count":93,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2022,11,10]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0277455","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,10]]}}}