Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Panaxadiol saponins treatment caused the subtle variations in the global transcriptional state of Asiatic corn borer, Ostrinia furnacalis

  • Liu, Shuangli (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Xu, Yonghua (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Gao, Yugang (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Zhao, Yan (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Zhang, Aihua (College of Chinese Medicinal Materials, Jilin Agricultural University) ;
  • Zang, Liansheng (Institute of Biological Control, Jilin Agricultural University) ;
  • Wu, Chunsheng (College of Agronomy, Jilin Agricultural University) ;
  • Zhang, Lianxue (College of Chinese Medicinal Materials, Jilin Agricultural University)
  • Received : 2017.05.17
  • Accepted : 2017.12.05
  • Published : 2020.01.15
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Abstract

Background: The lepidopteran Asiatic corn borer (ACB), Ostrinia furnacalis (Guenee), has caused huge economic losses throughout the Asian-Western Pacific region. Usually, chemical pesticides are used for the control, but excessive use of pesticides has caused great harm. Therefore, the inartificial ecotypic pesticides to ACB are extremely essential. In our previous study, we found that panaxadiol saponins (PDS) can effectively reduce the harm of ACB by causing antifeedant activity. Therefore, it is necessary to reveal the biological molecular changes in ACB and the functionary mechanism of PDS. Methods: We analyzed the global transcription of ACB with different PDS concentration treatment (5 mg/mL, 10 mg/mL, and 25 mg/mL) by high-throughput sequencing and de novo transcriptome assembly method. Results: PDS treatment could cause the changes of many gene expressions which regulate its signal pathways. The genes in peroxisome proliferator-activated receptor (PPAR) signaling pathway were significantly downregulated, and then, the downstream fatty acid degradation pathway had also been greatly affected. Conclusion: Through this experiment, we hypothesized that the occurrence of antifeedant action of ACB is because the PDS brought about the downregulation of FATP and FABP, the key regulators in the PPAR, and the downregulation of FATP and FABP exerts further effects on the expression of SCD-1, ACBP, LPL, SCP-X, and ACO, which leads to the disorder of PPAR signaling pathway and the fatty acid degradation pathway. Not only that, PDS treatment leads to enzyme activity decrease by inhibiting the expression of genes associated with catalytic activity, such as cytochrome P450 and other similar genes.

Keywords

References

  1. Nafus DM, Schreiner IH. Review of the biology and control of the Asian corn borer, Ostrinia furnacalis (Lep: Pyralidae). Trop Pest Manage 1991;37:41-56. https://doi.org/10.1080/09670879109371535
  2. He K, Wang Z, Zhou D, Wen L, Song Y, Yao Z. Evaluation of transgenic Bt corn for resistance to the Asian corn borer (Lepidoptera: Pyralidae). J Econ Entomol 2003;96:935-40. https://doi.org/10.1603/0022-0493-96.3.935
  3. Zhang T, He K, Wang Z. Transcriptome comparison analysis of Ostrinia furnacalis in four developmental stages. Sci Rep 2016;6:e35008.
  4. Hernandez M, Margalida A. Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 2008;17:264-72. https://doi.org/10.1007/s10646-008-0193-1
  5. lqbal Z, Zia K, Ahrnad A. Pesticide abuse in Pakistan and associated human health and environmental risks. Pak J Agric Sci 1997;34:4.
  6. Aktar MW, Sengupta D, Chowdhury A. Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2009;2:1-12. https://doi.org/10.2478/v10102-009-0001-7
  7. Liroff RA. Balancing risks of DDT and Malaria in the global POPs treaty. 2000.
  8. Brouwer A, Longnecker MP, Birnbaum LS, Cogliano J, Kostyniak P, Moore J, Schantz S, Winneke G. Characterization of potential endocrine-related health effects at low-dose levels of exposure to PCBs. Environ Health Perspect 1999;107:639-49. https://doi.org/10.1289/ehp.99107s4639
  9. Hurley PM. Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environ Health Perspect 1998;106:437-45. https://doi.org/10.1289/ehp.98106437
  10. Isman MB. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 2006;51:45-66. https://doi.org/10.1146/annurev.ento.51.110104.151146
  11. Jia L, Zhao Y. Current evaluation of the millennium phytomedicineeginseng (I): etymology, pharmacognosy, phytochemistry, marketand regulations. Curr Med Chem 2009;16:2475-84. https://doi.org/10.2174/092986709788682146
  12. Park JG, Kang WS, Park KT, Park DJ, Aravinthan A, Kim JH, Cho JY. Anticancer effect of joboksansam, Korean wild ginseng germinated from bird feces. J Ginseng Res 2016;40:304-8. https://doi.org/10.1016/j.jgr.2016.02.002
  13. Xu T, Shen X, Yu H, Sun L, Lin W, Zhang C. Water-soluble ginseng oligosaccharides protect against scopolamine-induced cognitive impairment by functioning as an antineuroinflammatory agent. J Ginseng Res 2016;40:211-9. https://doi.org/10.1016/j.jgr.2015.07.007
  14. Zhang AH, Tan SQ, Zhao Y, Lei FJ, Zhang LX. Effects of total ginsenosides on the feeding behavior and two enzymes activities of mythimna separata (Walker) larvae. Evid Based Complement Alternat Med 2015;45:1828.
  15. Pan L, Ren L, Chen F, Feng Y, Luo Y. Antifeedant activity of Ginkgo biloba secondary metabolites against Hyphantria cunea larvae: mechanisms and applications. Plos One 2016;11:e0155682. https://doi.org/10.1371/journal.pone.0155682
  16. Li SQ, Fang YL, Zhang ZN. Studies and applications of botanical insect antifeedants. Entomol Knowl 2005;5:491-6.
  17. Khater HF. Prospects of botanical Biopesticides in insect pest management. J ApplPharm Sci 2012;3:641-56.
  18. Chen Y, Zhong X, Chen L. Chinese herbal medicine resources with Bacteriostatic and insecticidal activities and their application as pesticides. Agric Sci Technol 2013;14:1307-14. 18.
  19. Han JY, Zhang LZ, Ji MS. Research progress of botanical insecticides. Chin Agric Sci Bull 2011;27:229-33.
  20. Vos RM, Van Bladeren PJ. Glutathione S-transferases in relation to their role in the biotransformation of xenobiotics. Chem Biol Interact 1990;75:241-65. https://doi.org/10.1016/0009-2797(90)90069-Y
  21. Zhang AH, Tan SQ, Zhao Y, Lei FJ, Zhang LX. Effects of total ginsenosides on the feeding behavior and two enzymes activities of mythimna separata (Walker) larvae. Evidence-Based Complementary Altern Med 2015:e451828.
  22. Xu K, Zhang Y, Wang Y, Ling P, Xie X, Jiang C, Zhang Z, Lian XY. Ginseng Rb fraction protects glia, neurons and cognitive function in a rat model of neurodegeneration. Plos One 2014;9:e101077. https://doi.org/10.1371/journal.pone.0101077
  23. Niu YP, Qian XD, Wang WX. Effect of panaxadiol saponin and panaxtrol saponin on proliferation of human bone marrow hemopoietic progenitor cells. Chin J Integr Med2004;24:127-129, 32.
  24. Zhong GG, Sun CW, Li YY, Qi H, Zhao CY, Jiang Y, Wang XM, Yang SJ, Li H. Calcium channel blockade and anti-free-radical actions of panaxadiol saponins Rb1, Rb2, Rb3, Rc, and Rd. Acta Pharmacol Sinica 1995;16:255-60.
  25. Xie XS, Liu HC, Yang M, Zuo C, Deng Y, Fan JM. Ginsenoside Rb1, a panoxadiol saponin against oxidative damage and renal interstitial fibrosis in rats with unilateral ureteral obstruction. Chin J Integr Med 2009;15:133-40. https://doi.org/10.1007/s11655-009-0133-9
  26. Wang J, Cui C, Fu L, Xiao Z, Xie N, Liu Y, Yu L, Wang H, Luo B. Genomic expression profiling and bioinformatics analysis on diabetic nephrology with ginsenoside Rg3. Mol Med Rep 2016;14:1162-72. https://doi.org/10.3892/mmr.2016.5349
  27. Kim TH, Lee SM. The effects of ginseng total saponin, panaxadiol and panaxatriol on ischemia/reperfusion injury in isolated rat heart. Food Chem Toxicol 2010;48:1516-20. https://doi.org/10.1016/j.fct.2010.03.018
  28. Song X, Bao S, Wu L, Hu S. Ginseng stem-leaf saponins (GSLS) and mineral oil act synergistically to enhance the immune responses to vaccination against foot-and-mouth disease in mice. Vaccine 2009;27:51-5. https://doi.org/10.1016/j.vaccine.2008.10.030
  29. Muller-Schwarze D. Leaf Disk test: Bioassay of Effect of Tannins on insect feeding behavior. New York: Springer; 2009.
  30. Nathan SS, Sehoon K. Effects of Melia azedarach L. extract on the teak defoliator Hyblaea puera Cramer(Lepidoptera: hyblaeidae). Crop Prot 2006;25:287-91. https://doi.org/10.1016/j.cropro.2005.03.023
  31. Zhang YW, Li Yan. Cytochrome P450 research review. J Jilin Med Coll 2005;26:4-6.
  32. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011;29:644-52. https://doi.org/10.1038/nbt.1883
  33. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005;21:3674-6. https://doi.org/10.1093/bioinformatics/bti610
  34. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011;12:323. https://doi.org/10.1186/1471-2105-12-323
  35. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010;26:136-8. https://doi.org/10.1093/bioinformatics/btp612
  36. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 2003;100:9440-5. https://doi.org/10.1073/pnas.1530509100
  37. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010;28:511-5. https://doi.org/10.1038/nbt.1621
  38. Tamayo P, Slonim D, Mesirov J, Zhu Q, Kitareewan S, Dmitrovsky E, Lander ES, Golub TR. Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci U S A 1999;96:2907-12. https://doi.org/10.1073/pnas.96.6.2907
  39. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010;11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
  40. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008;36:480-4.
  41. Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005;21:3787-93. https://doi.org/10.1093/bioinformatics/bti430
  42. Nie S, Xu L, Wang Y, Huang D, Muleke EM, Sun X, Wang R, Xie Y, Gong Y, Liu L. Identification of bolting-related microRNAs and their targets reveals complex miRNA-mediated flowering-time regulatory networks in radish (Raphanus sativus L.). Sci Rep 2015;5:e14034.
  43. Xu L, Wang Y, Liu W, Wang J, Zhu X, Zhang K, Yu R, Wang R, Xie Y, Zhang W, et al. De novo sequencing of root transcriptome reveals complex cadmiumresponsive regulatory networks in radish (Raphanus sativus L.). Plant Sci 2015;236:313-23. https://doi.org/10.1016/j.plantsci.2015.04.015
  44. Xu Y, Zhu X, Gong Y, Xu L, Wang Y, Liu L. Evaluation of reference genes for gene expression studies in radish (Raphanus astivus L.) using quantitative real-time PCR. Biochem Biophys Res Commun 2012;424:398-403. https://doi.org/10.1016/j.bbrc.2012.06.119
  45. Ahmed T, Raza SH, Maryam A, Setzer W, Braidy N, Nabavi SF, de Oliveira MR, Nabavi SM. Ginsenoside Rb1 as neuroprotective agent: a review. Brain Res Bull 2016;125:30-43. https://doi.org/10.1016/j.brainresbull.2016.04.002
  46. Hwang SH, Lee BH, Choi SH, Kim HJ, Won KJ, Lee HM, Rhim H, Kim HC, Nah SY. Effects of gintonin on the proliferation, migration, and tube formation of human umbilical-vein endothelial cells: involvement of lysophosphatidic-acid receptors and vascular-endothelial-growth-factor signaling. J Ginseng Res 2016;40:325-33. https://doi.org/10.1016/j.jgr.2015.10.002
  47. Lee SE, Park YS. Korean Red Ginseng water extract inhibits COX-2 expression by suppressing p38 in acrolein-treated human endothelial cells. J Ginseng Res 2014;38:34-9. https://doi.org/10.1016/j.jgr.2013.11.004
  48. Yuan HD, Kim JT, Kim SH, Chung SH. Ginseng and diabetes: the evidences from in vitro, animal and human studies. J Ginseng Res 2012;36:27-39. https://doi.org/10.5142/jgr.2012.36.1.27
  49. Liu Y, Shen D, Zhou F, Wang G, An C. Identification of immunity-related genes in Ostrinia furnacalis against entomopathogenic fungi by RNA-seq analysis. Plos One 2014;9:e86436. https://doi.org/10.1371/journal.pone.0086436
  50. Liu S, Wei W, Chu Y, Zhang L, Shen J, An C. De novo transcriptome analysis of wing development-related signaling pathways in Locusta migratoria manilensis and Ostrinia furnacalis (Guenee). Plos One 2014;9:e106770. https://doi.org/10.1371/journal.pone.0106770
  51. Zhu JY, Yang P, Zhang Z, Wu GX, Yang B. Transcriptomic immune response of Tenebrio molitor pupae to parasitization by Scleroderma guani. Plos One 2013;8:e54411. https://doi.org/10.1371/journal.pone.0054411
  52. Karatolos N, Pauchet Y, Wilkinson P, Chauhan R, Denholm I, Gorman K, Nelson DR, Bass C, ffrench-Constant RH, Williamson MS. Pyrosequencing the transcriptome of the greenhouse whitefly, Trialeurodes vaporariorum reveals multiple transcripts encoding insecticide targets and detoxifying enzymes. BMC Genomics 2011;12:56. https://doi.org/10.1186/1471-2164-12-56
  53. Jiang RW, Lau KM, Hon PM, Mak TC, Woo KS, Fung KP. Chemistry and biological activities of caffeic acid derivatives from Salvia miltiorrhiza. Curr Med Chem 2005;12:237-46. https://doi.org/10.2174/0929867053363397
  54. Cases S, Smith SJ, Zheng YW, Myers HM, Lear SR, Sande E, Novak S, Collins C, Welch CB, Lusis AJ, et al. Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc Natl Acad Sci U S A 1998;95:13018-23. https://doi.org/10.1073/pnas.95.22.13018
  55. Leung KW, Wong AS. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5:20. https://doi.org/10.1186/1749-8546-5-20
  56. Tu LH, Ma J, Liu HP, Wang RR, Luo J. The neuroprotective effects of ginsenosides on calcineurin activity and tau phosphorylation in SY5Y cells. Cell Mol Neurobiol 2009;29:1257-64. https://doi.org/10.1007/s10571-009-9421-3
  57. Feyereisen R. Insect P450 enzymes. Annu Rev Entomol 1999;44:507-33. https://doi.org/10.1146/annurev.ento.44.1.507
  58. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI. The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem Soc Trans 2006;34:1256-60. https://doi.org/10.1042/BST0341256
  59. Henderson GL, Harkey MR, Gershwin ME, Hackman RM, Stern JS, Stresser DM. Effects of ginseng components on c-DNA-expressed cytochrome P450 enzyme catalytic activity. Life Sci 1999;65:209-14.
  60. Kim DS, Kim Y, Jeon JY, Kim MG. Effect of Red Ginseng on cytochrome P450 and P-glycoprotein activities in healthy volunteers. J Ginseng Res 2016;40:375-81. https://doi.org/10.1016/j.jgr.2015.11.005
  61. Huang JT,Welch JS, Ricote M, Binder CJ, WillsonTM, Kelly C, WitztumJL, Funk CD, Conrad D, Glass CK. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 1999;400:378-82. https://doi.org/10.1038/22572
  62. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem 1995;270:12953-6. https://doi.org/10.1074/jbc.270.22.12953
  63. Willson TM, Cobb JE, Cowan DJ, Wiethe RW, Correa ID, Prakash SR, Beck KD, Moore LB, Kliewer SA, Lehmann JM. The structure-activity relationship between peroxisome proliferator-activated receptor gamma agonism and the antihyperglycemic activity of thiazolidinediones. J Med Chem 1996;39:665-8. https://doi.org/10.1021/jm950395a
  64. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK. The peroxisome proliferatoractivated receptor-gamma is a negative regulator of macrophage activation. Nature 1998;391:79-82. https://doi.org/10.1038/34178
  65. Mu Q, Fang X, Li X, Zhao D, Mo F, Jiang G, Yu N, Zhang Y, Guo Y, Fu M, et al. Ginsenoside Rb1 promotes browning through regulation of PPARgamma in 3T3-L1 adipocytes. Biochem Biophys Res Commun 2015;466:530-5. https://doi.org/10.1016/j.bbrc.2015.09.064
  66. Wei S, Li W, Yu Y, Yao FAL, Lan X, Guan F, Zhang M, Chen L. Ginsenoside Compound K suppresses the hepatic gluconeogenesis via activating adenosine-5'monophosphate kinase: a study in vitro and in vivo. Life Sci 2015;139:8-15. https://doi.org/10.1016/j.lfs.2015.07.032
  67. Mollah ML, Kim GS, Moon HK, Chung SK, Cheon YP, Kim JK, Kim KS. Antiobesity effects of wild ginseng (Panax ginseng C.A. Meyer) mediated by PPARgamma, GLUT4 and LPL in ob/ob mice. Phytother Res 2009;23:220-5. https://doi.org/10.1002/ptr.2593
  68. Han KL, Jung MH, Sohn JH, Hwang JK. Ginsenoside 20S-protopanaxatriol (PPT) activates peroxisome proliferator-activated receptor gamma (PPARgamma) in 3T3-L1 adipocytes. Biol Pharm Bull 2006;29:110-3. https://doi.org/10.1248/bpb.29.110
  69. Banz WJ, Iqbal MJ, Bollaert M, Chickris N, James B, Higginbotham DA, Peterson R, Murphy L. Ginseng modifies the diabetic phenotype and genes associated with diabetes in the male ZDF rat. Phytomedicine 2007;14:681-9. https://doi.org/10.1016/j.phymed.2007.06.003
  70. Zou H. Study on the function of SlGSTE1 in feeding plants of Spodoptera litura. South China Normal University; 2013.
  71. Wu H, Zhang GA, Zeng S, Lin KC. Extraction of allyl isothiocyanate from horseradish (Armoracia rusticana) and its fumigant insecticidal activity on four stored-product pests of paddy. Pest Manage Sci 2009;65:1003-8. https://doi.org/10.1002/ps.1786
  72. Bergamo P, Luongo D, Maurano F, Mazzarella G, Stefanile R, Rossi M. Conjugated linoleic acid enhances glutathione synthesis and attenuates pathological signs in MRL/MpJ-Fas(lpr) mice. J Lipid Res 2006;47:2382-91. https://doi.org/10.1194/jlr.M600187-JLR200
  73. Waxman DJ. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch Biochem Biophys 1999;369:11-23. https://doi.org/10.1006/abbi.1999.1351