Plant secondary metabolites of four rangeland plant species and their effects on the activities of detoxification enzymes of Oedaleus asiaticus in a steppe grassland

doi:10.11686/cyxb2019128

Abstract

Abstract: Oedaleus asiaticus Bey-Bienko, a significant grasshopper pest species occurring in north China, has specific food preferences and adaptations. To explore the identity of the plant metabolites responsible for food preference, we measured the content of flavonoids, phenols, alkaloids, terpenoids, and tannins in the grassland species Stipa krylovii, Cleistogenes squarrosa, Leymus chinensis, and Artemisia frigida. The growth and detoxification enzyme activity of O. asiaticus feeding on the above four plant species with their different secondary metabolite profiles were also analyzed. The grass S. krylovii had low levels of secondary metabolites, while the grass L. chinensis and the herb A. frigida possessed the highest contents of the five measured plant secondary metabolites. Grasshoppers feeding on S. krylovii with low secondary metabolite levels, had greater growth and decreased reactive oxygen species (ROS) concentration and digestive enzyme activity then those feeding on L. chinensis and A. frigida. In summary, S. krylovii was the most favorable host plant among the plants tested, and enhanced the performance of the grasshopper species O. asiaticus. This study shows that grasshopper feeding preference is linked to low levels of secondary metabolites, and this information could aid in grasshopper control.

Key words: grass, grasshopper, plant secondary metabolites, growth, detoxification enzyme

CHEN De-xia, LIU Xu, LUO Lin-hua, HUANG Xun-bing, LÜ Shen-jin, LI Guang-yue, ZHANG Ze-hua. Plant secondary metabolites of four rangeland plant species and their effects on the activities of detoxification enzymes of Oedaleus asiaticus in a steppe grassland[J]. Acta Prataculturae Sinica, 2020, 29(1): 183-192.

References

[1] Franzke A, Unsicker S B, Specht J, et al. Being a generalist herbivore in a diverse world: How do diets from different grasslands influence food plant selection and fitness of the grasshopper, Chorthippus parallelus? Ecological Entomology, 2010, 35(2): 126-138.
[2] Simon J C, D’Alençon E, Guy E, et al. Genomics of adaptation to host-plants in herbivorous insects. Briefings in Functional Genomics, 2015, 14(6): 413-423.
[3] Baldwin I T.An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiology, 2001, 127(4): 1449-1458.
[4] Despres L, David J P, Gallet C.The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology & Evolution, 2007, 22: 298-307.
[5] Nylin S, Slove J, Janz N.Host plant utilization, host range oscillations and diversification in nymphalid butterflies: A phylogenetic investigation. Evolution, 2014, 68(1): 105-124.
[6] Schoonhoven L M, Vanloon J J A, Dicke M. Insect-plant biology. Oxford: Oxford University Press, 2005.
[7] Zhao D X, Gao J L, Chen Z M.Research progress of behavioral orientation of phytophagous insects to their host plants. Chinese Journal of Tropical Agriculture, 2004, 4(2): 62-68.
赵冬香, 高景林, 陈宗懋. 植食性昆虫对寄主植物的定向行为研究进展. 热带农业科学, 2004, 24(2): 62-68.
[8] Güsewell S, Koerselman W.Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology Evolution & Systematics, 2002, 5(1): 37-61.
[9] Oleksyninst J, Reich P B, Zytkowiak R, et al. Needle nutrients in geographically diverse Pinus sylvestris L. populations. Annals of Forest Science, 2002, 59(1): 1-18.
[10] Roy A, Iii W B W, Vogel H, et al. Diet dependent metabolic responses in three generalist insect herbivores Spodoptera spp. Insect Biochemistry & Molecular Biology, 2016, 71: 91-105.
[11] Wang H, He X Q, Ji R.Selection mechanisms of Calliptamus italicus on four different host plant. Chinese Journal of Ecology, 2010, 29(12): 2401-2407.
王晗, 何雪青, 季荣. 意大利蝗对四种寄主植物的选择机制. 生态学杂志, 2010, 29(12): 2401-2407.
[12] Huang X B, Zhang Y, Cao G C, et al. Effect on growth and fecundity in Calliptamus italicus by Medicago sativa and Artemisia frigida Willd. Sp. Pl. Journal of Environmental Entomology, 2013, 35(5): 617-622.
黄训兵, 张洋, 曹广春, 等. 冷蒿和苜蓿对意大利蝗生长及生殖力的影响. 环境昆虫学报, 2013, 35(5): 617-622.
[13] Cease A J, Elser J J, Ford C F, et al. Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science, 2012, 335: 467-469.
[14] Li Z Z, Shen H J, Jiang Q G, et al. A study on the activities of endogenous enzymes of protective system in some insects. Acta Entomologica Sinica, 1994, 37(4): 399-403.
李周直, 沈惠娟, 蒋巧根, 等. 几种昆虫体内保护酶系统活力的研究. 昆虫学报, 1994, 37(4): 399-403.
[15] Misra J R, Horner M A, Lam G, et al. Transcriptional regulation of xenobiotic detoxification in Drosophila. Genes & Development, 2011, 25(17): 1796-1806.
[16] Li X, Baudry J, Berenbaum M R, et al. Structural and functional divergence of insect CYP6B proteins: From specialist to generalist cytochrome P450. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(9): 2939-2944.
[17] Wen Z, Pan L, Berenbaum M R, et al. Metabolism of linear and angular furanocoumarins by Papilio polyxenes CYP6B1 co-expressed with NADPH cytochrome P450 reductase. Insect Biochemistry & Molecular Biology, 2003, 33(9): 937-947.
[18] Yang S, Wu H, Xie J, et al. Depressed performance and detoxification enzyme activities of Helicoverpa armigera, fed with conventional cotton foliage subjected to methyl jasmonate exposure. Entomologia Experimentalis Et Applicata, 2013, 147(2): 186-195.
[19] Zhang W Z, He B, Cao G C, et al. Quantitative analysis of the effects of Stipa krylovii and Leymus chinensis on the factors of vitality of Oedaleus asiaticus. Acta Prataculturae Sinica, 2013, 22(5): 302-309.
张未仲, 贺兵, 曹广春, 等. 针茅及羊草对亚洲小车蝗生活力影响的定量分析. 草业学报, 2013, 22(5): 302-309.
[20] Huang X B, Wu H H, Qin X H, et al. Comprehensive evaluation and risk assessment of grasshoppers habitat based on projection pursuit model. Acta Prataculturae Sinica, 2015, 24(5): 25-33.
黄训兵, 吴惠惠, 秦兴虎, 等. 基于投影寻踪模型的草原蝗虫栖境评价及风险评估. 草业学报, 2015, 24(5): 25-33.
[21] Huang X B, Mcneill M R, Ma J C, et al. Biological and ecological evidences suggest Stipa krylovii (Pooideae), contributes to optimal growth performance and population distribution of the grasshopper Oedaleus asiaticus. Bulletin of Entomological Research, 2017, 107(3): 401-409.
[22] Huang X B, Mcneill M, Zhang Z H.Quantitative analysis of plant consumption and preference by Oedaleus asiaticus (Acrididae: Oedipodinae) in changed plant communities consisting of three grass species. Environmental Entomology, 2016, 45(1): 163-170.
[23] Whitman D W.Biology of grasshoppers. New York: John Wiley & Sons, 1990: 357-391.
[24] Whitman D W, Ananthrakrishnan T N.Phenotypic plasticity of insects: Mechanisms and consequences. Enfield: Science Publishers, 2009.
[25] Wu H H, Xu Y H, Cao G C, et al. Ecological effects of typical grassland types in Inner Mongolia on grasshopper community. Scientia Agricultura Sinica, 2012, 45(20): 4178-4186.
吴惠惠, 徐云虎, 曹广春, 等. 内蒙古典型草原草地类型对蝗虫群落优势种群的生态效应. 中国农业科学, 2012, 45(20): 4178-4186.
[26] Pauchet Y, Wilkinson P, Vogel H, et al. Pyrosequencing the Manduca sexta larval midgut transcriptome: Messages for digestion, detoxification and defence. Insect Molecular Biology, 2010, 19(1): 61-75.
[27] Zhang W H, Liu G J.A review on plant secondary substances in plant resistance to insect pests. Chinese Bulletin of Botany, 2003, 20(5): 522-530.
张文辉, 刘光杰. 植物抗虫性次生物质的研究概况. 植物学报, 2003, 20(5): 522-530.
[28] Herde M, Howe G A.Host plant-specific remodeling of midgut physiology in the generalist insect herbivore Trichoplusia ni. Insect Biochemistry & Molecular Biology, 2014, 50(1): 58-67.
[29] Ragland G J, Almskaar K, Vertacnik K L, et al. Differences in performance and transcriptome-wide gene expression associated with Rhagoletis (Diptera: Tephritidae) larvae feeding in alternate host fruit environments. Molecular Ecology, 2015, 24(11): 2759-2776.
[30] Zhao C Z, Zhou W, Wang K M, et al. The CCA analysis between grasshopper and plant community in upper reaches of Heihe River. Acta Ecologica Sinica, 2011, 31(12): 3384-3390.
赵成章, 周伟, 王科明, 等. 黑河上游蝗虫与植被关系的CCA分析. 生态学报, 2011, 31(12): 3384-3390.
[31] Ibanez S, Moretti M.Plant functional traits reveal the relative contribution of habitat and food preferences to the diet of grasshoppers. Oecologia, 2013, 173(4): 1459-1470.
[32] Han J G, Zhang Y J, Wang C J, et al. Rangeland degradation and restoration management in China. Rangeland Journal, 2008, 30(2): 233-239.
[33] Stige L C, Chan K S, Zhang Z, et al. Thousand-year-long Chinese time series reveals climatic forcing of decadal locust dynamics. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(41): 16188-16193.
[34] Liu G H, Wang G J, Wang S P, et al. Study on the diet composition and trophic niche of main herbivores in the Inner Mongolia typical steppe-Taking Leymus chinensis community as example. Acta Prataculturae Sinica, 2013, 22(1): 103-111.
刘贵河, 王国杰, 汪诗平, 等. 内蒙古典型草原主要草食动物食性及其营养生态位研究-以羊草群落为例. 草业学报, 2013, 22(1): 103-111.
[35] Cook S M, Khan Z R, Pickett J A.The use of push-pull strategies in integrated pest management. Annual Review of Entomology, 2007, 52: 375-400.