Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Amino acid, fatty acid, and carbohydrate metabolomic profiles with ginsenoside-induced insecticidal efficacy against Ostrinia furnacalis (Guenee)

  • Liu, Shuangli (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Wang, Xiaohui (Research Center of Agricultural Environment and Resources, Jilin Academy of Agricultural Sciences) ;
  • Zhang, Rui (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Song, Mingjie (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Zhang, Nanqi (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Li, Wanying (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Wang, Yingping (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Xu, Yonghua (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University) ;
  • Zhang, Lianxue (National & Local Joint Engineering Research Center for Ginseng Breeding and Application (Jilin), Jilin Agricultural University)
  • Received : 2018.09.26
  • Accepted : 2019.04.23
  • Published : 2020.07.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Previous studies have shown the insecticidal efficacy of ginsenosides. In the present study, we aimed to investigate the metabolic mechanism related to the inhibitory effect of panaxadiol saponins (PDSs) against the Asian corn borer Ostrinia furnacalis (Guenee). Methods: Third instar larvae of O. furnacalis were fed normal diets with different concentrations of PDSs for 4 days. The consumption index, relative growth rate, approximate digestibility, and conversion of ingested and digested food were recorded. A targeted gas chromatographye-mass spectrometry assay was performed to detect the profiles of amino acids, fatty acids, and carbohydrates in larvae of O. furnacalis. In addition, the activity of detoxification-related enzymes was determined. Results and Conclusions: PDSs decreased the consumption index, relative growth rate, approximate digestibility, and conversion of ingested and digested food in the 3rd instar larvae of O. furnacalis in a dose-dependent manner. PDSs decreased 15 free amino acids, 16 free fatty acids, and 5 carbohydrates and increased the levels of palmitoleic acid, palmitic acid, and 9-octadecenoic acid in the 3rd instar larvae. The activity of detoxification-related enzymes, such as acetylcholinesterase, glutathione S-transferase, cytochrome P450, carboxylesterase, trehalase, acid phosphatase, and alkaline phosphatase, was reduced in a dose-dependent manner in the 3rd instar larvae exposed to PDSs. These data confirmed the inhibitory effect of PDSs against growth, food utilization, and detoxification in the 3rd instar larvae of O. furnacalis and the potential for using PDSs as an efficient tool for insect pest management for O. furnacalis larvae.

Keywords

References

  1. Augustin JM, Kuzina V, Andersen SB, Bak S. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 2011;42:435-57. https://doi.org/10.1016/0031-9422(95)00882-9
  2. Golawska S, Lukasik I, Golawski A, Kapusta I, Janda B. Alfalfa (Medicago sativa L.) apigenin glycosides and their effect on the pea aphid (Acyrthosiphon pisum). Pol J Environ Stud 2010;19:913-9.
  3. Zhang AH, Liu ZQ, Lei FJ, Fu JF, Zhang XX, Ma WL, Zhang LX. Antifeedant and oviposition-deterring activity of total ginsenosides against Pieris rapae. Saudi J Biol Sci 2017;24:1751-3. https://doi.org/10.1016/j.sjbs.2017.11.005
  4. 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 Compl Alt 2015;2015:451828.
  5. Yu S, Zhou X, Fan L, Xu C, Fei Z, Jing L, Zhao H, Dai Y, Liu S, Yan F. Microbial transformation of ginsenoside Rb1, Re and Rg1 and its contribution to the improved anti-inflammatory activity of ginseng. Sci Rep 2017;7:1-10. https://doi.org/10.1038/s41598-016-0028-x
  6. Bak DH, Kim HD, Kim YO, Park CG, Han SY, Kim JJ. Neuroprotective effects of 20(S)-Protopanaxadiol against glutamate-induced mitochondrial dysfunction in Pc12 cells. Int J Mol Med 2016;37:378-86. https://doi.org/10.3892/ijmm.2015.2440
  7. Yang XD, Yang YY, Ouyang DS, Yang GP. A review of biotransformation and pharmacology of ginsenoside compound K. Fitoterapia 2015;100:208-20. https://doi.org/10.1016/j.fitote.2014.11.019
  8. Park EK, Choo MK, Han MJ, Kim DH. Ginsenoside Rh1 possesses antiallergic and anti-inflammatory activities. Int Arch Allergy Imm 2004;133:113-20. https://doi.org/10.1159/000076383
  9. Wang J, Hou Y, Jia Z, Xie X, Liu J, Kang Y, Wang X, Jia W. Metabonomics approach to comparing the anti-stress effects of four Panax ginseng components in rats. J Proteome Res 2018;17:813-21. https://doi.org/10.1021/acs.jproteome.7b00559
  10. Zhang N, Na LI, Jia-Lin LI, Kun MA, Cui L, Pharmacy CO, University B. Hypoglycemic effect of extract from Panax ginseng and Acanthopanax senticosus on streptozotocin-induced diabetic mice. Nat Prod Res Dev 2014;10:293-7.
  11. Xu YJ, Luo F, Gao Q, Shang Y, Wang C. Metabolomics reveals insect metabolic responses associated with fungal infection. Anal Bioanal Chem 2015;407:4815-21. https://doi.org/10.1007/s00216-015-8648-8
  12. Dawkar VV, Chikate YR, More TH, Gupta VS, Giri AP. The expression of proteins involved in digestion and detoxification are regulated in Helicoverpa armigera to cope up with chlorpyrifos insecticide. Insect Sci 2016;23:68-77. https://doi.org/10.1111/1744-7917.12177
  13. Hoi KK, Daborn PJ, Battlay P, Robin C, Batterham P, O'Hair RA, Donald WA. Dissecting the insect metabolic machinery using twin ion mass spectrometry: a single P450 enzyme metabolizing the insecticide imidacloprid in vivo. Anal Chem 2014;86:3525-32. https://doi.org/10.1021/ac404188g
  14. Feyereisen R. Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Manag Sci 2015;71:793-800. https://doi.org/10.1002/ps.3895
  15. Feng L, Liu XM, Cao FR, Wang LS, Chen YX, Pan RL, Liao YH, Wang Q, Chang Q. Anti-stress effects of ginseng total saponins on hindlimb-unloaded rats assessed by a metabolomics study. J Ethnopharmacol 2016;188:39-47. https://doi.org/10.1016/j.jep.2016.04.028
  16. Abdelazim A, Khater S, Ali H, Shalaby S, Afifi M, Saddick S, Alkaladi A, Almaghrabi OA. Panax ginseng improves glucose metabolism in streptozotocin-induced diabetic rats through 5' adenosine mono phosphate kinase up-regulation. Saudi J Biol Sci 2018. https://doi.org/10.1016/j.sjbs.2018.06.001.
  17. Yang H, Piao X, Zhang L, Song S, Xu y. Ginsenosides from the stems and leaves of Panax ginseng show antifeedant activity against Plutella xylostella (Linnaeus). Ind Crops Prod 2018;124:412-7. https://doi.org/10.1016/j.indcrop.2018.07.054
  18. Guo J, He K, Bai S, Zhang T, Zhao J, Wang Z. Physiological responses induced by Ostrinia furnacalis (Lepidoptera: Crambidae) feeding in maize and their effects on O. furnacalis performance. J Econ Entomol 2017;110:739-47. https://doi.org/10.1093/jee/tox060
  19. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54. https://doi.org/10.1006/abio.1976.9999
  20. Barazzoni R, Nep D, Biolo G, Bischoff S, Boirie Y, Cederholm T, Cuerda C, Delzenne N, Leon SM, Ljungqvist O. Carbohydrates and insulin resistance in clinical nutrition: recommendations from the ESPEN expert group. Clin Nutr 2017;36:355-63. https://doi.org/10.1016/j.clnu.2016.09.010
  21. Humbert B, Bleis P, Martin L, Dumon H, Darmaun D, Nguyen P. Effects of dietary protein restriction and amino acids deficiency on protein metabolism in dogs. J Anim Physiol Animal Nutrition 2001;85:255-62. https://doi.org/10.1046/j.1439-0396.2001.00324.x
  22. Ruan T, Li L, Lyu Y, Luo Q, Wu B. Effect of methionine deficiency on oxidative stress and apoptosis in the small intestine of broilers. Acta Vet Hung 2018;66:52-65. https://doi.org/10.1556/004.2018.006
  23. Pan X, Lu K, Qi S, Zhou Q. The content of amino acids in artificial diet influences the development and reproduction of Brown planthopper, Nilaparvata lugens (StAl). Arch Insect Biochem 2014;86:75-84. https://doi.org/10.1002/arch.21162
  24. Zhu H, He A, Chen L, Qin J, Li E, Li Q, Wang H, Zhang T, Su X. Effects of dietary lipid level and N-3/N-6 fatty acid ratio on growth, fatty acid composition and lipid peroxidation in Russian sturgeon Acipenser gueldenstaedtii. Aquacult Nutr 2016;23:879-90. https://doi.org/10.1111/anu.12454
  25. Piccinetti CC, Grasso L, Maradonna F, Radaelli G, Ballarin C, Chemello G, Evjemo JO, Carnevali O, Olivotto I. Growth and stress factors in ballan wrasse (Labrus bergylta) larval development. Aquac Res 2017;48:2567-80. https://doi.org/10.1111/are.13093
  26. Ahmad G. Increased glutamate and homocysteine and decreased glutamine levels in autism: a review and strategies for future studies of amino acids in autism. Dis Markers 2013;35:281-6. https://doi.org/10.1155/2013/536521
  27. Lertratanangkoon K, Orkiszewski RS, Scimeca JM. Methyl-donor deficiency due to chemically induced glutathione depletion. Cancer Res 1996;56:995-1005.
  28. Oz HS, Chen TS, Neuman M. Methionine deficiency and hepatic injury in a dietary steatohepatitis model. Digest Dis Sci 2008;53:767-76. https://doi.org/10.1007/s10620-007-9900-7
  29. Pardo V, Gonzalez-Rodriguez A, Muntane J, Kozma SC, Valverde AM. Role of hepatocyte S6k1 in palmitic acid-induced endoplasmic reticulum stress, lipotoxicity, insulin resistance and in oleic acid-induced protection. Food Chem Toxicol 2015;80:298-309. https://doi.org/10.1016/j.fct.2015.03.029
  30. Lovejoy JC. Dietary fatty acids and insulin resistance. Curr Atheroscler Rep 1999;1:215-20. https://doi.org/10.1007/s11883-999-0035-5
  31. Watkins SM, Reifsnyder PR, Pan HJ, German JB, Leiter EH. Lipid metabolomewide effects of the ppargamma agonist rosiglitazone. J Lipid Res 2002;43:1809-17. https://doi.org/10.1194/jlr.M200169-JLR200
  32. Wong K, Cheung C, Chao C, Su T, Leung Y. The protective effects of catechin on palmitic acid-induced cytotoxicity in mouse brain endothelial cell. South Med J 2015;74:521-3. https://doi.org/10.1097/00007611-198105000-00001
  33. Geng Y, Ying W, Xiao-Min C, Yuan Y, Min Y, Qi-Bing X. Identification of palmitoleic acid controlled by mtor signaling as a biomarker of polymyositis. J Imm Res 2017;2017:1-7.
  34. Fernandeziglesias A, Quesada H, Diaz S, Pajuelo D, Blade C, Arola L, Salvado MJ, Mulero M. Combination of grape seed proanthocyanidin extract and docosahexaenoic acid-rich oil increases the hepatic detoxification by GST mediated GSH conjugation in a lipidic postprandial state. Food Chem 2014;165:14-20. https://doi.org/10.1016/j.foodchem.2014.05.057
  35. Pavlidi N, Vontas J, Leeuwen TV. The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors. Curr Opin Insect Sci 2018;27:97-102. https://doi.org/10.1016/j.cois.2018.04.007
  36. Zhu J, Huan C, Si G, Yang H, Yin L, Ren Q, Ren B, Fu R, Miao M, Ren Z. The acetylcholinesterase (ache) inhibition analysis of medaka (Oryzias latipes) in the exposure of three insecticides. Pak J Pharm Sci 2015;28:671-4.
  37. Lee I, Eriksson P, Fredriksson A, Buratovic S, Viberg H. Developmental neurotoxic effects of two pesticides: behavior and neuroprotein studies on endosulfan and cypermethrin. Toxicology 2015;335:1-10. https://doi.org/10.1016/j.tox.2015.06.010
  38. Wegener G, Tschiedel V, Schloder P, Ando O. The toxic and lethal effects of the trehalase inhibitor trehazolin in locusts are caused by hypoglycaemia. J Exp Biol 2003;206:1233-40. https://doi.org/10.1242/jeb.00217
  39. Bilal M, Freed S, Ashraf MZ, Zaka SM, Khan MB. Activity of acetylcholinesterase and acid and alkaline phosphatases in different insecticide-treated Helicoverpa armigera (Hubner). Environ Sci Pollut Res 2018;25:22903-10. https://doi.org/10.1007/s11356-018-2394-3
  40. Selin-Rani S, Senthil-Nathan S, Revathi K, Chandrasekaran R, Thanigaivel A, Vasantha-Srinivasan P, Ponsankar A, Edwin ES, Pradeepa V. Toxicity of Alangium salvifolium Wang chemical constituents against the tobacco cutworm Spodoptera litura Fab. Pestic Biochem Physiol 2016;126:92-101. https://doi.org/10.1016/j.pestbp.2015.08.003