植物与植食性昆虫化学互作研究进展

doi:10.13287/j.1001-9332.202007.017

摘要/Abstract

摘要： 植物与植食性昆虫之间存在着复杂的化学相互作用。一方面,当遭受植食性昆虫为害时,植物能识别植食性昆虫相关分子模式,触发早期信号事件和激素信号转导途径,并由此引起转录组与代谢组重组、直接和间接防御化合物含量升高,最后提高对植食性昆虫的抗性。另一方面,植食性昆虫也能识别植物的防御反应,并能通过分泌效应子、选贮、解毒以及降低敏感性等反防御措施抑制或适应植物的化学防御。深入剖析植物与植食性昆虫的化学互作,不仅可在理论上丰富对昆虫与植物互作关系的理解,而且可在实践上为作物害虫防控新技术的开发提供重要的理论与技术指导。

关键词: 植物, 植食性昆虫, 植食性昆虫分子相关模式, 效应子, 防御化合物

Abstract: There are complex chemical interactions between plants and phytophagous insects. On the one hand, when infested by phytophagous insects, plants can recognize herbivore-associated molecular patterns and trigger early signaling events and phytohormone-mediated signaling pathways. The activated signaling pathways thus result in the reconfiguration of transcriptomes and metabolomes as well as the increases in direct and indirect defensive compounds in plants, which in turn enhance the resistance of plants to phytophagous insects. On the other hand, phytophagous insects can recognize defense responses in plants and then inhibit or adapt to plant chemical defenses by secreting effector, sequestrating and detoxifying defensive compounds, and/or reducing sensitivity to defensive compounds. The deep analysis of chemical interactions between plant and phytophagous insects could improve the understanding of the relationship between insects and plants in theory and also provide important theoretical and technical guidance for the development of new technologies for crop pest control in practice.

Key words: plant, phytophagous insect, herbivore-associated molecular pattern, effector, defensive compound

张月白, 娄永根. 植物与植食性昆虫化学互作研究进展[J]. 应用生态学报, 2020, 31(7): 2151-2160.

ZHANG Yue-bai, LOU Yong-gen. Research progress in chemical interactions between plants and phytophagous insects[J]. Chinese Journal of Applied Ecology, 2020, 31(7): 2151-2160.

参考文献

[1] Erb M, Reymond P. Molecular interactions between plants and insect herbivores. Annual Review of Plant Biology, 2019, 70: 527-557
[2] Schuman MC, Baldwin IT. The layers of plant responses to insect herbivores. Annual Review of Entomology, 2016, 61: 373-394
[3] Alborn HT, Turings CJT, Jones TH, et al. An elicitor of plant volatiles from beet armyworm oral secretion. Science, 1997, 276: 945-949
[4] 禹海鑫, 叶文丰, 孙民琴, 等. 植物与植食性昆虫防御与反防御的三个层次. 生态学杂志, 2015, 34(1): 256-262 [Yu H-X, Ye W-F, Sun M-Q, et al. Three levels of defense and anti-defense responses between host plants and herbivorous insects. Chinese Journal of Ecology, 2015, 34(1): 256-262]
[5] Mattiacci L, Dicke M, Posthumus MA. β-Glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 1995, 92: 2036-2040
[6] Schmelz EA, Leclere S, Carroll MJ, et al. Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiology, 2007, 144: 793-805
[7] Iida J, Desaki Y, Hata K, et al. Tetranins: New putative spider mite elicitors of host plant defense. New Phytologist, 2019, 224: 875-885
[8] Shangguan XX, Zhang J, Liu BF, et al. A mucin-like protein of planthopper is required for feeding and induces immunity response in plants. Plant Physiology, 2018, 176: 552-565
[9] Liu Y, Wang WL, Guo GX, et al. Volatile emission in wheat and parasitism by Aphidius avenae after exogenous application of salivary enzymes of Sitobion avenae. Entomologia Experimentalis et Applicata, 2009, 130: 215-221
[10] Guo H, Wielsch N, Hafke JB, et al. A porin-like protein from oral secretions of Spodoptera littoralis larvae induces defense-related early events in plant leaves. Insect Biochemistry and Molecular Biology, 2013, 43: 849-858
[11] Chaudhary R, Atamian HS, Shen Z, et al. GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111: 8919-8924
[12] Bricchi I, Occhipinti A, Bertea CM, et al. Separation of early and late responses to herbivory in Arabidopsis by changing plasmodesmal function. The Plant Journal, 2013, 73: 14-25
[13] Gaquerel E, Weinhold A, Baldwin IT. Molecular intera-ctions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant's elicited volatile emissions. Plant Physiology, 2009, 149: 1408-1423
[14] Alborn HT, Hansen TV, Jones TH, et al. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104: 12976-12981
[15] Fatouros NE, Pashalidou FG, Aponte Cordero WV, et al. Anti-aphrodisiac compounds of male butterflies increase the risk of egg parasitoid attack by inducing plant synomone production. Journal of Chemical Ecology, 2009, 35: 1373-1381
[16] Yang J, Nakayama N, Toda K, et al. Structural determination of elicitors in Sogatella furcifera (Horváth) that induce Japonica rice plant varieties (Oryza sativa L.) to produce an ovicidal substance against S. furcifera eggs. Bioscience, Biotechnology, and Biochemistry, 2014, 78: 937-942
[17] Doss RP, Oliver JE, Proebsting WM, et al. Bruchins: Insect-derived plant regulators that stimulate neoplasm formation. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97: 6218-6223
[18] Abdul Malik NA, Kumar IS, Nadarajah K. Elicitor and receptor molecules: Orchestrators of plant defense and immunity. International Journal of Molecular Sciences, 2020, 21: 963, https://doi.org/10.3390/ijms21030963
[19] Gouhier-Darimont C, Schmiesing A, Bonnet C, et al. Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity. Journal of Experimental Botany, 2013, 64: 665-674
[20] Liu YQ, Wu H, Chen H, et al. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nature Biotechnology, 2015, 33: 301-305
[21] Prince DC, Drurey C, Zipfel C, et al. The leucine-rich repeat receptor-like kinase brassinosteroid insensitive1-associated kinase1 and the cytochrome P450 phytoalexin deficient3 contribute to innate immunity to aphids in Arabidopsis. Plant Physiology, 2014, 164: 2207-2219
[22] Hu LF, Ye M, Kuai P, et al. OsLRR-RLK1, an early responsive leucine-rich repeat receptor-like kinase, initiates rice defense responses against a chewing herbivore. New Phytologist, 2018, 219: 1097-1111
[23] Wu J, Baldwin IT. New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics, 2010, 44: 1-24
[24] Nguyen D, Rieu I, Mariani C, et al. How plants handle multiple stresses: Hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Molecular Biology, 2016, 91: 727-740
[25] Raja V, Majeed U, Kang H, et al. Abiotic stress: Interplay between ROS, hormones and MAPKs. Environmental and Experimental Botany, 2017, 137: 142-157
[26] Aldon D, Mbengue M, Christian M, et al. Calcium signalling in plant biotic interactions. International Journal of Molecular Sciences, 2018, 19: 665, doi: 10.3390/ijms19030665
[27] Bartram S, Jux A, Gleixner G, et al. Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry, 2006, 67: 1661-1672
[28] Boachon B, Junker RR, Miesch L, et al. CYP76C1 (Cytochrome P450)-mediated linalool metabolism and the formation of volatile and soluble linalool oxides in Arabidopsis flowers: A strategy for defense against floral antagonists. The Plant Cell, 2015, 2015: 315-399
[29] Thomas AM, Williams RS, Swarthout RF. Distribution of the specialist aphid Uroleucon nigrotuberculatum (Homoptera: Aphididae) in response to host plant semiochemical induction by the gall fly Eurosta solidaginis (Diptera: Tephritidae). Environmental Entomology, 2019, 48: 1138-1148
[30] Huang XX, Xiao YT, Köllner TG, et al. The terpene synthase gene family in Gossypium hirsutum harbors a linalool synthase GhTPS12 implicated in direct defence responses against herbivores. Plant, Cell & Environment, 2018, 41: 261-274
[31] 戈林泉, 周国鑫, 王祺, 等. 水稻β-石竹烯合成酶基因OsCAS的克隆鉴定、原核表达及其遗传转化. 浙江大学学报, 2009, 35(4): 365-371 [Ge L-Q, Zhou G-X, Wang Q, et al. Cloning and prokaryotic expression of rice gene encoding β-caryophyllene synthase and its genetic transformation. Journal of Zhejiang University, 2009, 35(4): 365-371]
[32] Cheng A, Xiang C, Li JX, et al. The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry, 2007, 68: 1632-1641
[33] Mumm R, Schrank K, Wegener R, et al. Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. Journal of Chemical Ecology, 2003, 29: 1235-1252
[34] Schmelz EA, Huffaker A, Sims JW, et al. Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins. The Plant Journal, 2014, 79: 659-678
[35] Dafoe NJ, Huffaker A, Vaughan MM, et al. Rapidly induced chemical defenses in maize stems and their effects on short-term growth of Ostrinia nubilalis. Journal of Chemical Ecology, 2011, 37: 984-991
[36] Schmelz EA, Kaplan F, Huffaker A, et al. Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108: 5455-5460
[37] Murakami S, Nakata R, Aboshi T, et al. Insect-induced daidzein, formononetin and their conjugates in soybean leaves. Metabolites, 2014, 4: 532-546
[38] Li Z, Guan XM, Michaud JP, et al. Quercetin interacts with Cry1Ac protein to affect larval growth and survival of Helicoverpa armigera. Pest Management Science, 2016, 72: 1359-1365
[39] Steinly BA, Berenbaum M. Histopathological effects of tannins on the midgut epithelium of Papilio polyxenes and Papolio glaucus. Entomologia Experimentalis et Applicata, 1985, 39: 3-9
[40] Barbehenn R, Weir Q, Salminen J. Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. Journal of Chemical Ecology, 2008, 34: 748-756
[41] Golawska S, Lukasik I, Golawski A, et al. Alfalfa (Medicago sativa L.) apigenin glycosides and their effect on the pea aphid (Acyrthosiphon pisum). Polish Journal of Environmental Studies, 2010, 19: 913-919
[42] Treutter D. Significance of flavonoids in plant resistance: A review. Environmental Chemistry Letters, 2006, 4: 147-157
[43] Mithofer A, Boland W. Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology, 2012, 63: 431-450
[44] Steppuhn A, Gase K, Krock B, et al. Nicotine's defensive function in nature. PLoS Biology, 2004, 2(10): e382
[45] Bown AW, Macgregor KB, Shelp BJ. Gamma-aminobutyrate: Defense against invertebrate pests? Trends in Plant Science, 2006, 11: 424-427
[46] Bones AM, Rossiter JT. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiologia Plantarum, 1996, 97: 194-208
[47] Schlaeppi K, Bodenhausen N, Buchala A, et al. The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. The Plant Journal, 2008, 55: 774-786
[48] Alamgir KM, Hojo Y, Christeller JT, et al. Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory. Plant, Cell & Environment, 2016, 39: 453-466
[49] Kaur H, Heinzel N, Schoettner M, et al. R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiology, 2010, 152: 1731-1747
[50] Bowles DJ. Defense-related proteins in higher-plants. Annual Review of Biochemistry, 1990, 59: 873-907
[51] Tanpure RS, Barbole RS, Dawkar VV, et al. Improved tolerance against Helicoverpa armigera in transgenic tomato over-expressing multi-domain proteinase inhibitor gene from Capsicum annuum. Physiology and Molecular Biology of Plants, 2017, 23: 597-604
[52] Chen H, Wilkerson CG, Kuchar JA, et al. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102: 19237-19242
[53] Kang J, Wang L, Giri A, et al. Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. The Plant Cell, 2006, 18: 3303-3320
[54] Chen MS, Wu JX, Zhang GH. Inducible direct plant defense against insect herbivores: A review. Insect Science, 2008, 15: 101-114
[55] Bhonwong A, Stout MJ, Attajarusit J, et al. Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). Journal of Chemical Ecology, 2009, 35: 28-38
[56] Matsui K, Kurishita S, Hisamitsu A, et al. A lipid-hydrolysing activity involved in hexenal formation. Biochemical Society Transactions, 2000, 28: 857-860
[57] Engelberth J, Engelberth M. The costs of green leaf vola-tile-induced defense priming: Temporal diversity in growth responses to mechanical wounding and insect herbivory. Plants, 2019, 8: 23
[58] Matsui K. Green leaf volatiles: Hydroperoxide lyase pathway of oxylipin metabolism. Current Opinion in Plant Biology, 2006, 9: 274-280
[59] 胡国文, 梁天锡, 刘光杰, 等. 抗白背飞虱水稻品种挥发性次生物质的提取、组分鉴定与生测. 中国水稻科学, 1994(4): 223-230 [Hu G-W, Liang T-X, Liu G-J, et al. The extraction, chemical analysis and bioassays of secondary volatiles from rice varieties susceptible and resistant to the white backed planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacidae). Chinese Journal of Rice Science, 1994(4): 223-230]
[60] 周强, 徐涛, 张古忍, 等. 虫害诱导的水稻挥发物对褐飞虱的趋避作用. 昆虫学报, 2003, 46(6): 739-744 [Zhou Q, Xu T, Zhang G-Z, et al. Repellent effects of herbivore-induced rice volatiles on the brown planthopper, Nilaparvata lugens Stl. Acta Entomologica Sinica, 2003, 46(6): 739-744]
[61] De Moraes CM, Mescher MC, Tumlinson JH. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature, 2001, 410: 577-580
[62] Reddy GVP, Guerrero A. Interactions of insect pheromones and plant semiochemicals. Trends in Plant Science, 2004, 9: 253-261
[63] Whitman DW, Eller FJ. Orientation of Microplitis croceipes (Hymenoptera, Braconidae) to green leaf volatiles: Dose-response curves. Journal of Chemical Ecology, 1992, 18: 1743-1753
[64] Shiojiri K, Ozawa R, Kugimiya S, et al. Herbivore-specific, density-dependent induction of plant volatiles: Honest or “cry wolf” signals? PLoS One, 2010, 5(8): e121618
[65] Shiojiri K, Kishimoto K, Ozawa R, et al. Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103: 16672-16676
[66] Liu JL, Du HT, Ding X, et al. Mechanisms of callose deposition in rice regulated by exogenous abscisic acid and its involvement in rice resistance to Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pest Management Science, 2017, 73: 2559-2568
[67] Hao PY, Liu CX, Wang YY, et al. Herbivore-induced callose deposition on the sieve plates of rice: An important mechanism for host resistance. Plant Physiology, 2008, 146: 1810-1820
[68] Zhou YD, Sun LT, Wang S, et al. A key ABA hydrolase gene, OsABA8ox3 is involved in rice resistance to Nilaparvata lugens by affecting callose deposition. Journal of Asia-Pacific Entomology, 2019, 22: 625-631
[69] Ahmad S, Veyrat N, Gordon-Weeks R, et al. Benzo-xazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiology, 2011, 157: 317-327
[70] Mukanganyama S, Figueroa CC, Hasler JA, et al. Effects of DIMBOA on detoxification enzymes of the aphid Rhopalosiphum padi (Homoptera: Aphididae). Journal of Insect Physiology, 2003, 49: 223-229
[71] Houseman JG, Campos F, Thie N, et al. Effect of the maize-derived compounds DIMBOA and MBOA on growth and digestive processes of european corn-borer (Lepidoptera, Pyralidae). Journal of Economic Entomology, 1992, 85: 669-674
[72] Tzin V, Lindsay PL, Christensen SA, et al. Genetic mapping shows intraspecific variation and transgressive segregation for caterpillar-induced aphid resistance in maize. Molecular Ecology, 2015, 24: 5739-5750
[73] Eichenseer H, Mathews MC, Powell JS, et al. Survey of a salivary effector in caterpillars: Glucose oxidase variation and correlation with host range. Journal of Chemical Ecology, 2010, 36: 885-897
[74] Wu S, Peiffer M, Luthe DS, et al. ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS One, 2012, 7(7): e41947
[75] Schmelz EA, Huffaker A, Carroll MJ, et al. An amino acid substitution inhibits specialist herbivore production of an antagonist effector and recovers insect-induced plant defenses. Plant Physiology, 2012, 160: 1468-1478
[76] Will T, Tjallingii WF, Thonnessen A, et al. Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104: 10536-10541
[77] Naessens E, Dubreuil G, Giordanengo P, et al. A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Current Biology, 2015, 25: 1898-1903
[78] Chung SH, Rosa C, Scully ED, et al. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110: 15728-15733
[79] Ray S, Alves PCMS, Ahmad I, et al. Turnabout is fair play: Herbivory-induced plant chitinases excreted in fall armyworm frass suppress herbivore defenses in maize. Plant Physiology, 2016, 171: 694-706
[80] Becerra JX. Synchronous coadaptation in an ancient case of herbivory. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100: 12804-12807
[81] Kumar P, Pandit SS, Steppuhn A, et al. Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46's role in a nicotine-mediated antipredator herbivore defense. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111: 1245-1252
[82] Dunse KM, Kaas Q, Guarino RF, et al. Molecular basis for the resistance of an insect chymotrypsin to a potato type II proteinase inhibitor. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107: 15016-15021
[83] Dobler S, Dalla S, Wagschal V, et al. Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109: 13040-13045
[84] Wybouw N, Dermauw W, Tirry L, et al. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLife, 2014, 3: e2365
[85] Li X, Baudry J, Berenbaum MR, 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: 2939-2944