Please wait a minute...
Journal of Integrative Agriculture  2016, Vol. 15 Issue (1): 135-144    DOI: 10.1016/S2095-3119(15)61072-3
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Insecticide induction of O-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren)
 ZHANG Bai-zhong, KONG Fan-chao, WANG Hua-tang, GAO Xi-wu, ZENG Xin-nian, SHI Xue-yan
1、College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, P.R.China
2、Department of Entomology, China Agricultural University, Beijing 100193, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  The red imported fire ant (Solenopsis invicta) is a global major invasive pest, and has caused significant economic, social and environmental impacts since its invasion to mainland of China in 2004. To date, chemical control has been the most effective measure. However, the long-term use of chemicals would lead to an unexpected rebound. To understand the risks and explore the mechanisms of detoxification or induction to insecticides in S. invicta, the O-demethylase activity and expression of cytochrome P450 genes of workers and queens, and the effects of chlorpyrifos and fipronil exposure in workers were investigated. Biochemical assays showed the O-demethylase activity of cytochrome P450 was significantly higher in workers than in queens (1.66-fold), and was significantly induced in workers exposed to chlorpyrifos and fipronil, reaching a maximum (3.00- and 1.95-fold) at 48 h and then decreasing dramatically compared to controls (exposed to acetone counterpart). The relative expression levels of 12 cytochrome P450 expressed sequence tags (ESTs) in workers were significantly higher than in queens (from 2.3- to 36.4-fold). Multiple cytochrome P450 genes (except 9E4) were co-up-regulated (from 1.5- to 2.86-fold) in workers exposed to fipronil. These results indicated that the increased O-demethylase activity may result from the increased transcription levels of cytochrome P450 related to detoxification of insecticides in S. invicta. It appears that cytochrome P450 plays an important role in enhanced metabolic detoxification of insecticides. At the same time, it also provides the theoretical basis for resistance management and rational usage of insecticides to control S. invicta.

Abstract  The red imported fire ant (Solenopsis invicta) is a global major invasive pest, and has caused significant economic, social and environmental impacts since its invasion to mainland of China in 2004. To date, chemical control has been the most effective measure. However, the long-term use of chemicals would lead to an unexpected rebound. To understand the risks and explore the mechanisms of detoxification or induction to insecticides in S. invicta, the O-demethylase activity and expression of cytochrome P450 genes of workers and queens, and the effects of chlorpyrifos and fipronil exposure in workers were investigated. Biochemical assays showed the O-demethylase activity of cytochrome P450 was significantly higher in workers than in queens (1.66-fold), and was significantly induced in workers exposed to chlorpyrifos and fipronil, reaching a maximum (3.00- and 1.95-fold) at 48 h and then decreasing dramatically compared to controls (exposed to acetone counterpart). The relative expression levels of 12 cytochrome P450 expressed sequence tags (ESTs) in workers were significantly higher than in queens (from 2.3- to 36.4-fold). Multiple cytochrome P450 genes (except 9E4) were co-up-regulated (from 1.5- to 2.86-fold) in workers exposed to fipronil. These results indicated that the increased O-demethylase activity may result from the increased transcription levels of cytochrome P450 related to detoxification of insecticides in S. invicta. It appears that cytochrome P450 plays an important role in enhanced metabolic detoxification of insecticides. At the same time, it also provides the theoretical basis for resistance management and rational usage of insecticides to control S. invicta.
Keywords:  Solenopsis invicta       P450 activity       gene expression       chlorpyrifos       fipronil       induction       detoxification  
Received: 22 January 2015   Accepted:
Fund: 

The authors are highly obliged to the National Natural Science Foundation of China (31071712) for the financial support given to the present research work.

About author:  ZHANG Bai-zhong, E-mail: baizhongok@163.com;

Cite this article: 

ZHANG Bai-zhong, KONG Fan-chao, WANG Hua-tang, GAO Xi-wu, ZENG Xin-nian, SHI Xue-yan. 2016. Insecticide induction of O-demethylase activity and expression of cytochrome P450 genes in the red imported fire ant (Solenopsis invicta Buren). Journal of Integrative Agriculture, 15(1): 135-144.

Abbas N, Khan H A A, Shad S A. 2014. Cross-resistance,genetics, and realized heritability of resistance to fipronilin the house fly, Muscado mestica (Diptera: Muscidae):A potential vector for disease transmission. ParasitologyResearch, 113, 1343-1352

Alexia C P, Jaclyn B, Myriam R K, Jessica R, Emilie G C,Rodolphe P, Muhammad A R, Mark P, Chantal D V,Stéphane R, Jean P D 2013. The central role of mosquitocytochrome P450 CYP6Zs in insecticide detoxificationrevealed by functional expression and structural modelling.Biochemical Journal, 455, 75-85

Avicor S W, Wajidi M F F, El-garj F M A, Jaal Z, Yahaya Z S.2014. Insecticidal activity and expression of cytochromeP450 family 4 genes in aedesalbopictus after exposure topyrethroid Mosquito coils. The Protein Journal, 33, 457-464

Ay R, Yorulmaz S. 2010. Inheritance and detoxification enzymelevels in Tetranychus urticae Koch (Acari: Tetranychidae)strain selected with chlorpyrifos. Journal of Pest Science, 83, 85-93

Bloch G, Shpigler H, Wheeler D E, Robinson, G E. 2009.Endocrine influences on the organization of insect societies.Hormones, 2, 1027-1068

Bradford M M. 1976. A rapid sensitive method for thequantization of microgram quantities of protein utilizingthe principle of protein binding. Analytical Biochemistry,72, 248-254

Bradfield J Y, Lee Y H, Keeley L L 1991. Cytochrome P450family 4 in a cockroach: Molecular cloning and regulationby regulation by hypertrehalosemic hormone. Proceedingsof the National Academy of Sciences of the United Statesof America, 88, 4558-4562

Cornette R, Koshikawa S, Hojo M, Matsumoto T, Miura T. 2006.Caste-specific cytochrome P450 in the damp-wood termiteHodotermopsis sjostedti (Isoptera, Termopsidae). InsectMolecular Biology, 15, 235-244

Drees B M. 2006. A new technique for laboratory assessmentof red imported fire ant mound drench treatments.Southwestern Entomologist, 27, 177-183

Durham E W, Siegfried B D, Scharf M E. 2002. In vivo andin vitro metabolism of fipronil by larvae of the Europeancorn borer Ostrinia nubilalis. Pest Management Science,58, 799-804

El-Latif A O A, Kranthi K R, KranthiS, Sarwar A, SubrahmanyamB. 2014. Overexpression of cytochrome P450 CYP6B7mediated pyrethroid resistance in Indian strains of the cottonbollworm, Helicoverpa armigera (Hübner). Journal of PlantProtection Research, 54, 287-293

Festucci-Buselli R A, Carvalho-Dias A S, Oliveira-Andrade D,Caixeta-Nunes C, Li H M, Stuart J J, Muir W, Scharf M E,Pittendrigh B R. 2005. Expression of Cyp6g1 and Cyp12d1in DDT resistant and susceptible strains of Drosophilamelanogaster. Insect Molecular Biology, 14, 69-77

Feyereisen R. 2005. Insect cytochrome P450. ComprehensiveMolecular Insect Science, 4, 1-77

Gonzalez F J, Nebert D W. 1990. Evolution of the P450 genesuperfamily: Animal-plant ‘warfare’, molecular drive andhuman genetic differences in drug oxidation. Trends inGenetics, 6, 182-186

Greenberg L, Reierson D, Rust M K. 2003. Fipronil trials inCalifornia against the red imported fire ant, Solenopsisinvicta Buren, using sugar water consumption andmound counts as measures of ant abundance. Journal ofAgricultural and Urban Entomology, 20, 221-233

Guo Y, Zhang J, Ma E. 2014. Effect of sub-lethal doses ofchlorpyrifos on cytochrome P450 enzyme. Chinese Journalof Applied Entomology, 51, 702-707 (in Chinese)

Harrison T L, Zangerl A R, Schuler M A, Berenbaum M R. 2001.Developmental variation in cytochrome P450 expressionin Papilio polyxenes in response to xanthotoxin, a hostplant allelochemical. Archives of Insect Biochemistry andPhysiology, 48, 179-189

Huang C, Yao H, Ye G, Cheng J. 2006. Effects of sublethaldose of fipronil on detoxifying enzymes in the larvae of Chilosuppressalis and Sesamia inferens. Chinese Journal of RiceScience, 20, 447-450 (in Chinese)

Hu X P, Song D L, Scherer C W. 2005. Transfer of indoxacarbamong workers of Coptotermes formosanus (Isoptera:Rhinotermitidae): effects of dose, donor: Recipient ratioand post-exposure time. Pest Management Science, 61,1209-1214

Johnson R M, Pollock H S, Berenbaum M R 2009. Synergisticinteractions between in-hive miticides in Apis mellifera.Journal of Economic Entomology, 102, 474-479

Johnson R M, Wen Z, Schuler M A, Berenbaum M R. 2006.Mediation of pyrethroid insecticide toxicity to honeybees (Hymenoptera: Apidae) by cytochrome P450monooxygenases. Journal of Economic Entomology, 99,1046-1050

Kuriachan I, Vinson S B. 2000. A queen’s worker attractivenessinfluences her movement in polygynous colonies of the redimported fire ant (Hymenoptera: Formicidae) in responseto adverse temperatures. Environmental Entomology, 29,943-949

Liu N, Li T, Reid W R, Yang T, Zhang L. 2011. Multiplecytochrome P450 genes: Their constitutive overexpressionand permethrin induction in insecticide resistant mosquitoes,Culex quinquefasciatus. PLoS One, 6, e23403.

Liu N, Scott J G. 1998. Increased transcription of CYP6D1causes cytochrome P450-mediated insecticide resistancein house fly. Insect Biochemistry and Molecular Biology,28, 531-535

Liu N, Zhang L. 2004. CYP4AB1, CYP4AB2, and Gp-9 geneoverexpression associated with workers of the red importedfire ant, Solenopsis invicta Buren. Gene, 327, 81-87

Liu N, Zhu F. 2012. House fly ctyochrome P450s: Their rolein insecticide resistance and strategies in the isolation andcharacterization. In: Liu T X, Kang L, eds., Recent Advancesin Entomological Research. Springer, Berlin Heidelberg.pp. 246-257

Liu X, Liang P, Gao X, Shi X. 2006. Induction of the cytochromeP450 activity by plant allelochemicals in the cotton bollworm,Helicoverpa armigera (Hübner). Pesticide Biochemistry andPhysiology, 84, 127-134

Li X, Berenbaum M R, Schuler M A. 2002. Cytochrome P450and act in genes expressed in Helicoverpa zea andHelicoverpa armigera: paralogy/orthology identification,gene conversion and evolution. Insect Biochemistry andMolecular Biology, 32, 311-320

Li X, Schuler M A, Berenbaum M R. 2007. Molecularmechanisms of metabolic resistance to synthetic and naturalxenobiotics. Annual Review of Entomology, 52, 231-253

Loftin K, Hopkins J, Gavin J, Shanklin D. 2003. Evaluationof broadcast applications of various contact insecticidesagainst red imported fire ants, Solenopsis invicta Buren.Journal of Agricultural and Urban Entomology, 20, 151-156

Lu K H, Bradfield J Y, Keeley L L. 1995. Hypertrehalosemichormone-regulated gene expression for cytochrome P4504C1 in the fat body of the cockroach, Blaberus discoidalis.Archives of Insect Biochemistry and Physiology, 28, 79-90

Lu K H, Bradfield J Y, Keeley L L. 1999. Juvenile hormone inhibition of gene expression for cytochrome P4504C1 inadult females of the cockroach, Blaberusdis coidalis. InsectBiochemistry and Molecular Biology, 29, 667-673

Mao W, Rupasinghe S G, Johnson R M, Zangerla A R, SchulerbM A, Berenbaum M R. 2009. Quercetin-metabolizingCYP6AS enzymes of the pollinator Apis mellifera(Hymenoptera: Apidae). Comparative Biochemistry andPhysiology Part B (Biochemistry and Molecular Biology),154, 427-434

Mao W, Schuler M A, Berenbaum M R. 2011. CYP9Q-mediateddetoxification of acaricides in the honey bee (Apis mellifera).Proceedings of the National Academy of Sciences of theUnited States of America, 108, 12657-12662

Marr B, Schiuma G. 2003. Business performance measurement- Past, present and future. Management Decision, 41,680-687

Mata J, Marguerat S, Bähler J. 2005. Post-transcriptional controlof gene expression: a genome-wide perspective. Trends inBiochemical Sciences, 30, 506-514

Morrison L W, Porter S D. 2003. Positive association betweendensities of the red imported fire ant, Solenopsis invicta(Hymenoptera: Formicidae), and generalized ant andarthropod diversity. Environmental Entomology, 32,548-554

Nebert D W, Gonzalez F J. 1987. P450 genes: structure,evolution, and regulation. Annual Review of Biochemistry,56, 945-993

Okey A B. 1990. Enzyme induction in the cytochrome P-450system. Pharmacology &Therapeutics, 45, 241-298

Passera L, Aron S, Vargo E L, Keller L. 2001. Queen control ofsex ratio in fire ants. Science, 293, 1308-1310

Pavek P, Dvorak Z. 2008. Xenobiotic-induced transcriptionalregulation of xenobiotic metabolizing enzymes of thecytochrome P450 superfamily in human extrahepatictissues. Current Drug Metabolism, 9, 129-143

Pennisi E. 2001. Queens, not workers, rule the ant nest.Science, 293, 1239-1241

Pfaffl M W. 2001. A new mathematical model for relativequantification in real-time RT-PCR. Nucleic Acids Research,29, e45-e45.

Pilling E D, Bromleychallenor K A C, Walker C H, Jepson PC. 1995. Mechanism of synergism between the pyrethroidinsecticide λ-cyhalothrin and the imidazole fungicideprochloraz, in the honeybee (Apis mellifera L.). PesticideBiochemistry and Physiology, 51, 1-11

Rakotondravelo M L, Anderson T D, Charlton R E, Zhu K Y.2006. Sublethal effects of three pesticides on activity ofselected target and detoxification enzymes in the aquaticmidge, Chironomus tentans (Diptera: Chironomidae).Archives of Environmental Contamination and Toxicology,51, 360-366

Rao A, Vinson S B. 2004. Ability of resident ants to destructsmall colonies of Solenopsis invicta (Hymenoptera:Formicidae). Environmental Entomology, 33, 587-598

Rose R L, Barbhaiya L, Roe R M, Rock G C, Hodgson E. 1995.Cytochrome P450-associated insecticide resistance andthe development of biochemical diagnostic assays inHeliothis virescens. Pesticide Biochemistry and Physiology,51, 178-191

Saner C, Weibel B, Würgler F E, Sengstag C. 1996.Metabolism of promutagens catalyzed by Drosophilamelanogaster CYP6A2 enzyme in Saccharomycescerevisiae. Environmental and Molecular Mutagenesis,27, 46-58

Scharf M E, Parimi S, Meinke L J, Chandler L D, Siegfried B D.2001. Expression and induction of three family 4 cytochromeP450 (CYP4) genes identified from insecticide-resistant andsusceptible western corn rootworms, Diabrotica virgiferavirgifera. Insect Molecular Biology, 10, 139-146

Scott J G. 2008. Insect cytochrome P450s: thinking beyonddetoxification. Recent Advances in Insect Physiology,Toxicology and Molecular Biology, 1, 17-124

Shang Q, Pan Y, Fang K, Xi J, Brennana J A. 2012. Biochemicalcharacterization of acetylcholinesterase, cytochrome P450and cross-resistance in an omethoate-resistant strain ofAphis gossypii Glover. Crop Protection, 31, 15-20

Sutherland T D, Unnithan G C, Feyereisen R. 2000. Terpenoidω-hydroxylase (CYP4C7) messenger RNA levels in thecorpora allata: A marker for ovarian control of juvenilehormone synthesis in Diploptera punctata. Journal of InsectPhysiology, 46, 1219-1227

Tang J, Li J, Shao Y, Yang B, Liu Z. 2010. Fipronil resistancein the whitebacked planthopper (Sogatella furcifera):possible resistance mechanisms and cross-resistance. PestManagement Science, 66, 121-125

Tarver M R, Coy M R, Scharf M E. 2012. Cyp15F1: A novelcytochrome p450 gene linked to juvenile hormonedependentcaste differention in the termite reticulitermesflavipes. Archives of Insect Biochemistry and Physiology,80, 92-108

Tay J W, Neoh K B, Lee C Y. 2014. The roles of the queen,brood, and worker castes in the colony growth dynamicsof the pharaoh ant Monomorium pharaonis (Hymenoptera:Formicidae). Myrmecological News, 20, 87-94

Terriere L C .1983. Enzyme induction gene amplification, andinsect resistance to insecticides. In: Georghiou G P, SaitoT, eds., Pest Resistance to Pesticides. Plenum Press, NewYork. pp. 265-297

Terriere L C. 1984. Induction of detoxication enzymes in insects.Annual Review of Entomology, 29, 71-88

Tufts D M, Hunter W B, Bextine B. 2014. Solenopsis invictavirus (sinv-1) infection and insecticide interactions in thered imported fire ant (Hymenoptera: Formicidae). FloridaEntomologist, 97, 1251-1254

Vinson S B. 1997. Invasion of the red imported fire ant(Hymenoptera: Formicidae ) spread, biology and impact.American Entomologist, 43, 23-39

Wang L, Lu Y, Xu Y, Zeng L. 2013. The current status ofresearch on Solenopsis invicta Buren (Hymenoptera:Formicidae) in Mainland China. Journal of InvertebratePathology, 114, 1-6

Wee C W, Lee S F, Robin C, Heckel D G. 2008. Identification of candidate genes for fenvalerate resistance in Helicoverpaarmigera using cDNA-AFLP. Insect Molecular Biology, 17,351-360

Wu Y. 2011. Direct electrochemistry of cytochrome P450 6A1in mimic bio-membrane and its application for pesticidessensing. Sensors and Actuators (B Chemical),156,773-778

Xie M, You M. 2011. Effects of fipronil on detoxifying enzymeactivity in Plutella xylostella. Chinese Journal of AppliedEntomology, 48, 1728-1733. (in Chinese)

Yang X, Li X, Zhang Y. 2013. Molecular cloning and expressionof CYP9A61: Achlorpyrifos-ethyl and lambda-cyhalothrininduciblecytochrome P450 cDNA from Cydia pomonella.International Journal of Molecular Sciences, 14, 24211-24229

Yang Y, Yue L, Chen S, Wu Y. 2008. Functional expressionof Helicoverpa armigera CYP9A12 and CYP9A14 inSaccharomyces cerevisiae. Pesticide Biochemistry andPhysiology, 92, 101-105

Yu R, Guo Y, Ma E, Guo Y. 2012. Effect of sublethal dosesof malathion and carbaryl on the P450 genes of Locustamigratoria. Chinese Journal of Applied Entomology, 49,693-699. (in Chinese)

Zhou J, Zhang G, Zhou Q. 2012. Molecular characterizationof cytochrome P450 CYP6B47 cDNAs and 5′-flankingsequence from Spodoptera litura (Lepidoptera: Noctuidae):Its response to lead stress. Journal of Insect Physiology,58, 726-736.

Zhu F, Li T, Zhang L, Liu N. 2008. Co-up-regulation of threeP450 genes in response to permethrin exposure inpermethrin resistant house flies, Muscado mestica. BMCPhysiology, 8, 18.
[1] Qing Li, Zhuangzhuang Sun, Zihan Jing, Xiao Wang, Chuan Zhong, Wenliang Wan, Maguje Masa Malko, Linfeng Xu, Zhaofeng Li, Qin Zhou, Jian Cai, Yingxin Zhong, Mei Huang, Dong Jiang. Time-course transcriptomic information reveals the mechanisms of improved drought tolerance by drought priming in wheat[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2902-2919.
[2] Ting Pan, Ruiting Guo, Weiwei Wang, Xing Liu, Bing Xia, Linshu Jiang, Ming Liu. Mechanism of mitigating on Deoxynivalenol-induced intestinal toxicity in swine and its dietary regulation strategy[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2449-2464.
[3] Lijun Ma, Juan Tang, Qinghe Zhang, Bingli Gao, Cheng Qu, Ran Wang, Chen Luo. Involvement of the cytochrome P450 genes CYP6DW3 and CYP4C64 in afidopyropen resistance in Bemisia tabaci Mediterranean (Q biotype)[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1905-1915.
[4] Xuemei Hou, Meimei Shi, Zhuohui Zhang, Yandong Yao, Yihua Li, Changxia Li, Wenjin Yu, Chunlei Wang, Weibiao Liao. DNA demethylation is involved in nitric oxide-induced flowering in tomato[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1769-1785.
[5] Lijiao Ge, Weihao Miao, Kuolin Duan, Tong Sun, Xinyan Fang, Zhiyong Guan, Jiafu Jiang, Sumei Chen, Weimin Fang, Fadi Chen, Shuang Zhao. Comparative transcriptome analysis identifies key regulators of nitrogen use efficiency in chrysanthemum[J]. >Journal of Integrative Agriculture, 2025, 24(1): 176-195.
[6] Zhengyuan Xu, Lingzhen Ye, Qiufang Shen, Guoping Zhang. Advances in the study of waterlogging tolerance in plants[J]. >Journal of Integrative Agriculture, 2024, 23(9): 2877-2897.
[7] Jia Chen, Xinran Zhang, Ziqi He, Dongwei Xiong, Miao Long. Damage on intestinal barrier function and microbial detoxification of deoxynivalenol: A review[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2507-2524.
[8] YANG Wei-bing, ZHANG Sheng-quan, HOU Qi-ling, GAO Jian-gang, WANG Han-Xia, CHEN Xian-Chao, LIAO Xiang-zheng, ZHANG Feng-ting, ZHAO Chang-ping, QIN Zhi-lie.

Transcriptomic and metabolomic analysis provides insights into lignin biosynthesis and accumulation and differences in lodging resistance in hybrid wheat [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1105-1117.

[9] Xiaoyan Cui, Ke Yang, Weiyun Zhang, Liyang Zhang, Ding Li, Wei Wu, Yun Hu, Tingting Li, Xugang Luo. Dietary manganese supplementation inhibits abdominal fat deposition possibly by regulating gene expression and enzyme activity involved in lipid metabolism in the abdominal fat of broilers[J]. >Journal of Integrative Agriculture, 2024, 23(12): 4161-4171.
[10] Muhammad Mobeen Tahir, Li Fan, Zhimin Liu, Humayun Raza, Usman Aziz, Asad Shehzaib, Shaohuan Li, Yinnan He, Yicen Lu, Xiaoying Ren, Dong Zhang, Jiangping Mao. Physiological and molecular mechanisms of cytokinin involvement in nitrate-mediated adventitious root formation in apples[J]. >Journal of Integrative Agriculture, 2024, 23(12): 4046-4057.
[11] Atiqur RAHMAN, Md. Hasan Sofiur RAHMAN, Md. Shakil UDDIN, Naima SULTANA, Shirin AKHTER, Ujjal Kumar NATH, Shamsun Nahar BEGUM, Md. Mazadul ISLAM, Afroz NAZNIN, Md. Nurul AMIN, Sharif AHMED, Akbar HOSAIN. Advances in DNA methylation and its role in cytoplasmic male sterility in higher plants[J]. >Journal of Integrative Agriculture, 2024, 23(1): 1-19.
[12] ZHAO Shu-ping, DENG Kang-ming, ZHU Ya-mei, JIANG Tao, WU Peng, FENG Kai, LI Liang-jun.

Optimization of slow-release fertilizer application improves lotus rhizome quality by affecting the physicochemical properties of starch [J]. >Journal of Integrative Agriculture, 2023, 22(4): 1045-1057.

[13] MA Yu-xin, ZHOU Zhi-jun, CAO Hong-zhe, ZHOU Fan, SI He-long, ZANG Jin-ping, XING Ji-hong, ZHANG Kang, DONG Jin-gao. Identification and expression analysis of sugar transporter family genes reveal the role of ZmSTP2 and ZmSTP20 in maize disease resistance[J]. >Journal of Integrative Agriculture, 2023, 22(11): 3458-3473.
[14] ZHANG Yan-mei, AO De, LEI Kai-wen, XI Lin, Jerry W SPEARS, SHI Hai-tao, HUANG Yan-ling, YANG Fa-long. Dietary copper supplementation modulates performance and lipid metabolism in meat goat kids[J]. >Journal of Integrative Agriculture, 2023, 22(1): 214-221.
[15] JIANG Yong, MA Xin-yan, XIE Ming, ZHOU Zheng-kui, TANG Jing, CHANG Guo-bin, CHEN Guo-hong, HOU Shui-sheng. Dietary threonine deficiency affects expression of genes involved in lipid metabolism in adipose tissues of Pekin ducks in a genotype-dependent manner[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2691-2699.
No Suggested Reading articles found!