Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (8): 1685-1694.doi: 10.3864/j.issn.0578-1752.2022.08.018

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles    

Effects of Sublethal Doses of Imidacloprid on the Expression of Neurometabolic Genes in Apis cerana cerana

QIU YiLei(),WU Fan,ZHANG Li,LI HongLiang()   

  1. College of Life Sciences, China Jiliang University/Zhejiang Provincial Key Laboratory of Biometrology and Inspection & Quarantine, Hangzhou 310018
  • Received:2021-11-02 Accepted:2021-11-15 Online:2022-04-16 Published:2022-05-11
  • Contact: HongLiang LI E-mail:qiuyil96@163.com;hlli@cjlu.edu.cn

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Abstract:

【Background】The target of neonicotinoid insecticides is the acetylcholine receptor in the nervous system of insects. Due to its good systemicity and low toxicity to humans and animals, it has been widely used in agricultural production. Thus there is still a low residue in plants, and this sublethal dose residue can still cause adverse effects on the behavior and nervous system of flower-visiting insects like bees.【Objective】The objective of this study is to clarify the effect of sublethal dose imidacloprid (a kind of neonicotinoid insecticides) on the nervous physiological and metabolism system of Apis cerana cerana.【Method】In this study, the worker bees were treated with two sublethal concentration gradient doses of 5 and 10 μg·L-1 imidacloprid for 10 days (three biological replicates). After total RNA was extracted, the resulting library was analyzed by RNA-seq. Throughput sequencing, and the bioinformatics technology was used to assemble and annotate the sequence de novo, and the differentially expressed genes (DEGs) after sublethal doses imidacloprid treatment were analyzed by clustering and enrichment. Finally, real-time fluorescence quantitative PCR (RT-qPCR) technology was used to verify the DEGs related to the nervous and metabolic systems.【Result】A total of 9 sequencing libraries were obtained, the ratio of effective sequencing data exceeded 94.45%. From the obtained 37 364 unigenes, 571 DEGs were identified. The enrichment analysis of GO and KEGG found that the DEGs were mainly related to multiple pathways such as protein translation, redox, oxidative phosphorylation, and ribosome, indicating that sublethal doses of imidacloprid had an impact on multiple physiological processes and metabolic pathways of A. c. cerana. Nine DEGs (e.g. neuropeptide F (NPF), neuropeptide SIFamide receptor (SIFaR), phosphoinositide 3-dependent kinases (PDK1), A-kinase anchoring protein 1 (AKAP1), carbonic anhydrase 3 (CA3), superoxide dismutase 2 (SOD2), NADH dehydrogenase [ubiquinone] 1 alpha subcomplex subunit 10 (ND42), cuticle protein 12 (CP12), and odorant-binding protein (OBP17)) related to nerve signal transmission and metabolic function were selected for RT-qPCR verification. Their expression patterns were completely consistent with the transcriptome results.【Conclusion】The sublethal dose of imidacloprid can affect lots of aspects of A. c. cerana such as nerve signal transduction, cellular respiration, immune response, maintenance of homeostasis, and olfactory perception.

Key words: Apis cerana cerana, sublethal dose, imidacloprid, RNA-seq, RT-qPCR

Table 1

Real-time fluorescence quantitative PCR (RT-qPCR) primers"

基因
Gene 		编码蛋白
Coding protein		 引物名称
Primer name		 引物序列
Primer sequence (5′→3′)
NPF 神经肽F
Neuropeptide F		 NPFq-F CATTGTTGGCTTCGTTGTTGGT
NPFq-R GCATTGCGTTGCATCAGAAGTC
SIFaR 神经肽SIFamide受体
Neuropeptide SIFamide receptor		 SIFaRq-F CGGCAAGATCAGGTACTACGAGAC
SIFaRq-R CGACGAGTTGTTGTTGTTGTTGTTG
PDK1 3-磷酸肌醇依赖性蛋白激酶
Phosphoinositide 3-dependent kinases		 PDK1q-F ACGACGAGGACACCACCACTAC
PDK1q-R TGCTTCTCCAATCGGTTCCTGATCT
AKAP1 激酶（PRKA）锚蛋白1
A-kinase anchoring protein 1		 AKAP1q-F GAGCAGACAGAGTTGATCCAGGTG
AKAP1q-R TCGTCAGTTTGTATGCCAGAATCGT
CA3 碳酸酐酶
Carbonic anhydrase 3		 CA3q-F GCCATTGGAACAACGACGGTGAG
CA3q-R TCGTATGTATCGGTCGCCAGAGG
SOD2 超氧化物歧化酶
Superoxide dismutase 2		 SOD2q-F ATACCGTTGCCATTCAAGGTTCTG
SOD2q-R CACATCATTCCAATTCACGACATCA
ND42 NADH脱氢酶亚基
NADH dehydrogenase [ubiquinone] 1 alpha subcomplex subunit 10		 ND42q-F GCCACCACCAACACATGATGAA
ND42q-R ACGACATGATTCTGGTAATTGAGGA
CP12 昆虫表皮蛋白
Cuticle protein 12		 CP12q-F CCTCGATGTTACTGGTAGCTTCTCC
CP12q-R CGAAACAAGATTGATGGTGGGATGA
OBP17 气味结合蛋白17
Odorant-binding protein 17		 OBP17q-F CGTTGATGATGGCAAGATC
OBP17q-R TCAGAGATAGGTGAACATTGG
β-actin 肌动蛋白（内参）
Actin (reference)		 β-actinq-F TCCTGCTATGTATGTCGC
β-actinq-R AGTTGCCATTTCCTGTTC

Fig. 1

Clustering heat map of DEGs The abscissa represents different samples, and the ordinate represents different DEGs. The darker the color, the greater the difference in the gene among different samples"

Fig. 2

Histogram of DEGs GO enrichment"

Fig. 3

Scatter plot of DEGs KEGG enrichment Rich factor represents the number of differential genes located in the KEGG/the total number of genes located in the KEGG. The greater the Rich factor value, the greater the degree of KEGG enrichment. The closer the color of the dot is to red, the greater the degree of renaturation, and the size of the dot represents the number of genes enriched in the pathway"

Fig. 4

Transcriptome sequencing and RT-qPCR verification results of 9 DEGs The column height is the mean±SEM. The LSD method was used for one-way analysis of variance. * indicates a significant difference, P<0.05"

[1] LO N, GLOAG R S, ANDERSON D L, OLDROYD B P. A molecular phylogeny of the genus Apis suggests that the giant honey bee of the Philippines, A. breviligula Maa, and the plains honey bee of southern India, A. indica Fabricius, are valid species. Systematic Entomology, 2010, 35(2): 226-233.
doi: 10.1111/j.1365-3113.2009.00504.x
[2] MILLAR N S, DENHOLM I. Nicotinic acetylcholine receptors: Targets for commercially important insecticides. Invertebrate Neuroscience, 2007, 7(1): 53-66.
doi: 10.1007/s10158-006-0040-0
[3] RADLOFF S E, HEPBURN C, HEPBURN H R, FUCHS S, HADISOESILO S, TAN K, ENGEL M S, KUZNETSOV V. Population structure and classification of Apis cerana. Apidologie, 2010, 41(6): 589-601.
doi: 10.1051/apido/2010008
[4] 蔺哲广, 孟飞, 郑火青, 周婷, 胡福良. 新烟碱类杀虫剂对蜜蜂健康的影响. 昆虫学报, 2014, 57(5): 607-615.
LIN Z G, MENG F, ZHENG H Q, ZHOU T, HU F L. Effects of neonicotinoid insecticides on honeybee health. Acta Entomologica Sinica, 2014, 57(5): 607-615. (in Chinese)
[5] SUCHAIL S, GUEZ D, BELZUNCES L P. Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environmental Toxicology and Chemistry, 2000, 19(7): 1901-1905.
doi: 10.1002/etc.5620190726
[6] BONMATIN J M, MOINEAU I, CHARVET R, COLIN M E, FLECHE C, BENGSCH E R. Behaviour of imidacloprid in fields. Toxicity for honey bees//LICHTFOUSE E, SCHWARZBAUER J, ROBERT D. Environmental Chemistry. Green Chemistry and Pollutants in Ecosystems. Springer Berlin Heidelberg, 2005: 483-494.
[7] NISHIMURA K, KANDA Y, OKAZAWA A, UENO T. Relationship between insecticidal and neurophysiological activities of imidacloprid and related compounds. Pesticide Biochemistry and Physiology, 1994, 50(1): 51-59.
doi: 10.1006/pest.1994.1057
[8] KRUPKE C, HUNT G, EITZER B, ANDINO G, GIVEN K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE, 2012, 7(1): e29268.
[9] CRESSWELL J. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology, 2011, 20(1): 149-157.
doi: 10.1007/s10646-010-0566-0
[10] BRYDEN J, GILL R J, MITTON R A, RAINE N E, JANSEN V A. Chronic sublethal stress causes bee colony failure. Ecology Letters, 2013, 16(12): 1463-1469.
doi: 10.1111/ele.12188
[11] STONER K A, EITZER B D. Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS ONE, 2012, 7(6): e39114.
[12] STONER K A, EITZER B D. Using a hazard quotient to evaluate pesticide residues detected in pollen trapped from honey bees (Apis mellifera) in Connecticut. PLoS ONE, 2013, 8(10): e77550.
[13] MULLIN C A, FRAZIER M, FRAZIER J L, ASHCRAFT S, SIMONDS R, VANENGELSDORP D, PETTIS J S. High levels of miticides and agrochemicals in north American apiaries: Implications for honey bee health. PLoS ONE, 2010, 5(3): e9754.
doi: 10.1371/journal.pone.0009754
[14] NICODEMO D, MAIOLI M A, MEDEIROS H C D, GUELFI M, BALIEIRA K V B, DE JONG D, MINGATTO F E. Fipronil and imidacloprid reduce honeybee mitochondrial activity. Environmental Toxicology and Chemistry, 2014, 33(9): 2070-2075.
doi: 10.1002/etc.2655
[15] 周婷, 宋怀磊, 王强, 代平礼, 吴艳艳, 孙继虎. 吡虫啉对意大利蜜蜂脑乙酰胆碱受体分布的影响. 昆虫学报, 2013, 56(11): 1258-1266.
ZHOU T, SONG H L, WANG Q, DAI P L, WU Y Y, SUN J H. Effects of imidacloprid on the distribution of nicotine acetylcholiine receptors in the brain of adult honeybee (Apis mellifera ligustica). Acta Entomologica Sinica, 2013, 56(11): 1258-1266. (in Chinese)
[16] SCHNEIDER C W, TAUTZ J, GRÜNEWALD B, FUCHS S. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE, 2012, 7(1): e30023.
[17] WILLIAMSON S M, WRIGHT G A. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. The Journal of Experimental Biology, 2013, 216(10): 1799-1807.
[18] TAN K, CHEN W, DONG S, LIU X, WANG Y, NIEH J C. Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS ONE, 2014, 9(7): e102725.
[19] WU-SMART J, SPIVAK M. Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Scientific Reports, 2016, 6: 32108.
[20] 代平礼, 周婷, 王强, 吴艳艳, 耿文龙, 宋怀磊. 吡虫啉对意大利蜜蜂学习行为的影响. 农药, 2013, 52(7): 512-514.
DAI P L, ZHOU T, WANG Q, WU Y Y, GENG W L, SONG H L. Effects of imidacloprid on learning performance of Apis mellifera ligustica. Agrochemicals, 2013, 52(7): 512-514. (in Chinese)
[21] YANG E C, CHANG H C, WU W Y, CHEN Y W. Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE, 2012, 7(11): e49472.
[22] ALBURAKI M, BOUTIN S, MERCIER P L, LOUBLIER Y, CHAGNON M, DEROME N. Neonicotinoid-coated Zea mays seeds indirectly affect honeybee performance and pathogen susceptibility in field trials. PLoS ONE, 2015, 10(5): e0125790.
[23] CHAUZAT M P, CARPENTIER P, MARTEL A C, BOUGEARD S, COUGOULE N, PORTA P, LACHAIZE J, MADEC F, AUBERT M, FAUCON J P. Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environmental Entomology, 2009, 38(3): 514-523.
doi: 10.1603/022.038.0302
[24] CHRISTEN V, BACHOFER S, FENT K. Binary mixtures of neonicotinoids show different transcriptional changes than single neonicotinoids in honeybees (Apis mellifera). Environmental Pollution, 2017, 220: 1264-1270.
doi: 10.1016/j.envpol.2016.10.105
[25] FENT K, SCHMID M, HETTICH T, SCHMID S. The neonicotinoid thiacloprid causes transcriptional alteration of genes associated with mitochondria at environmental concentrations in honey bees. Environmental Pollution, 2020, 266(1): 115297.
[26] 黄一村, 时敏, 陈学新. 昆虫神经肽F的研究进展. 应用昆虫学报, 2015, 52(6): 1315-1325.
HUANG Y C, SHI M, CHEN X X. Advances in research on insect neuropeptide F. Chinese Journal of Applied Entomology, 2015, 52(6): 1315-1325. (in Chinese)
[27] LINGO P, ZHAO Z, SHEN P. Co-regulation of cold-resistant food acquisition by insulin- and neuropeptide Y-like systems in Drosophila melanogaster. Neuroscience, 2007, 148(2): 371-374.
doi: 10.1016/j.neuroscience.2007.06.010
[28] KRASHES M, DASGUPTA S, VREEDE A, WHITE B, ARMSTRONG J, WADDELL S. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell, 2009, 139(2): 416-427.
doi: 10.1016/j.cell.2009.08.035
[29] HERMANN C, YOSHII T, DUSIK V, HELFRICH-FOERSTER C. Neuropeptide F immunoreactive clock neurons modify evening locomotor activity and free-running period in Drosophila melanogaster. The Journal of Comparative Neurology, 2012, 520(5): 970-987.
doi: 10.1002/cne.22742
[30] LEE G, BAHN J H, PARK J H.Sex- and clock-controlled expression of the neuropeptide F gene in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33): 12580-12585.
[31] XU J, LI M, SHEN P. A G-protein-coupled neuropeptide Y-like receptor suppresses behavioral and sensory response to multiple stressful stimuli in Drosophila. The Journal of Neuroscience, 2010, 30(7): 2504-2512.
doi: 10.1523/JNEUROSCI.3262-09.2010
[32] AYUB M, HERMIZ M, LANGE A B, ORCHARD I. SIFamide influences feeding in the chagas disease vector, Rhodnius prolixus. Frontiers in Neuroscience, 2020, 14: 134.
doi: 10.3389/fnins.2020.00134
[33] SELLAMI A, VEENSTRA J A. SIFamide acts on fruitless neurons to modulate sexual behavior in Drosophila melanogaster. Peptides, 2015, 74: 50-56.
doi: 10.1016/j.peptides.2015.10.003
[34] PARK S, SONN J Y, OH Y, LIM C, CHOE J. SIFamide and SIFamide receptor define a novel neuropeptide signaling to promote sleep in Drosophila. Molecules and Cells, 2014, 37(4): 295-301.
doi: 10.14348/molcells.2014.2371
[35] MARTELLI C, PECH U, KOBBENBRING S, PAULS D, BAHL B, SOMMER M V, POORYASIN A, BARTH J, ARIAS C W P, VASSILIOU C,et al. SIFamide translates hunger signals into appetitive and feeding behavior in Drosophila. Cell Reports, 2017, 20(2): 464-478.
doi: 10.1016/j.celrep.2017.06.043
[36] FELICIELLO A, GOTTESMAN M, AVVEDIMENTO E. The biological functions of A-Kinase anchor proteins. Journal of Molecular Biology, 2001, 308(2): 99-114.
doi: 10.1006/jmbi.2001.4585
[37] RINALDI L, SEPE M, DONNE R D, CONTE K, ARCELLA A, BORZACCHIELLO D, AMENTE S, DE VITA F, PORPORA M, GARBI C,et al. Mitochondrial AKAP 1 supports mTOR pathway and tumor growth. Cell Death and Disease, 2017, 8(6): e2842.
doi: 10.1038/cddis.2017.241
[38] SCHIATTARELLA G G, CATTANEO F, CARRIZZO A, PAOLILLO R, BOCCELLA N, AMBROSIO M, DAMATO A, PIRONTI G, FRANZONE A, RUSSO G,et al.Akap1 regulates vascular function and endothelial cells behavior. Hypertension, 2018, 71(3): 507-517.
doi: 10.1161/HYPERTENSIONAHA.117.10185
[39] OKUN J G, LUMMEN P, BRANDT U. Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH: ubiquinone oxidoreductase). The Journal of Biological Chemistry, 1999, 274(5): 2625-2630.
doi: 10.1074/jbc.274.5.2625
[40] VANHAESEBROECK B, ALESSI D R. The PI3K-PDK1 connection: More than just a road to PKB. The Biochemical Journal, 2000, 346(3): 561-576.
doi: 10.1042/bj3460561
[41] SUN Z, YAO Y, YOU M, LIU J, GUO W, QI Z, WANG Z, WANG F, YUAN W, YU S. The kinase PDK1 is critical for promoting T follicular helper cell differentiation. eLife, 2021, 10: e61406.
[42] WANG H L, ZHU Z M, WANG H, YANG S L, ZHAO S H, LI K. Molecular characterization and association analysis of porcine CA3. Cytogenetic and Genome Research, 2006, 115(2): 129-133.
doi: 10.1159/000095232
[43] SOWDEN J, SMITH H, MORRISON K, EDWARDS Y.Sequence comparisons and functional studies of the proximal promoter of the carbonic anhydrase 3 (CA3) gene. Gene, 1998, 214(1/2): 157-165.
doi: 10.1016/S0378-1119(98)00201-7
[44] BAUTISTA M A M, BHANDARY B, WIJERATNE A J, MICHEL A P, HOY C W, MITTAPALLI O. Evidence for trade-offs in detoxification and chemosensation gene signatures in Plutella xylostella. Pest Management Science, 2015, 71(3): 423-432.
doi: 10.1002/ps.3822
[45] 殷玲, 吉挺, 李冠华, 牛德芳. 中华蜜蜂OBP17基因CDS序列及其表达与抗螨性状的相关性. 江苏农业科学, 2015, 43(11): 45-48.
YIN L, JI T, LI G H, NIU D F. The CDS sequence of OBP17 gene of Apis cerana cerana and its correlation of resistance to Varroa destructor. Jiangsu Agricultural Sciences, 2015, 43(11): 45-48. (in Chinese)
[46] 吴帆. 中华蜜蜂气味结合蛋白配基结合特征和OBP12与吡虫啉结合机理研究[D]. 杭州: 中国计量大学, 2016.
WU F. Study binding characterization of Chinese honeybee’s (Apis cerana cerana) odorant binding proteins with ligands and binding mechanism of OBP 12 with imidacloprid (Hymenoptera: Apidae)[D]. Hangzhou: China Jiliang University, 2016. (in Chinese)
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