From trade-off to synergy: how nutrient status modulates plant resistance to herbivorous insects?

Abstract

The principle of the “growth-defense trade-off” governs how plants adjust their growth and defensive strategies in response to external factors, impacting interactions among plants, herbivorous insects, and their natural enemies. Mineral nutrients are crucial in modulating plant growth and development through their bottom-up effects. Emerging evidence has revealed complex regulatory networks that link mineral nutrients to plant defense responses, influencing the delicate balance between growth and defense against herbivores. This review aims to summarize recent advances that elucidate the impact of nutrient availability on plant defense responses. Particularly, we focus on how nutrient status shapes plant resistance to herbivores, delving into the molecular mechanisms underlying this physiological process. Moreover, the interplay between mineral nutrients and various herbivore defense mechanisms, including physical protection, plant hormone signaling, defensive metabolite production, and volatile organic compound emissions that deter herbivores or attract their natural enemies, are discussed. This comprehensive review sets the stage for future investigations into the intricate crosstalk between nutrient signaling and plant defense responses, which serves as a central mechanism to guide sustainable pest management approaches, thereby promoting balanced agroecosystem health and enhancing plant ecosystem productivity and resilience.

References

[1] Abd el-aziz M, Amin T, El-Barkey N. Macromolecular abnormalities in the adults of the potato tuber moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae) induced by larval feeding on irradiated potato tubers. Egyptian Academic Journal of Biological Sciences A, Entomology. 2008;1: 99–108.

[2] AcevedoFE, Rivera-VegaLJ, ChungSH, RayS, FeltonGW. Cues from chewing insects — the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol, 2015, 26: 80-86

[3] AlhousariF, GregerM. Silicon and Mechanisms of Plant Resistance to Insect Pests. Plants, 2018, 7: 33

[4] Ali AH, Abdelrahman M, El-Sayed MA. Alkaloid Role in Plant Defense Response to Growth and Stress. In: Jogaiah S, Abdelrahman M, editors. Bioactive Molecules in Plant Defense: Signaling in Growth and Stress; 2019. pp. 145–158.

[5] AllmannS, BaldwinIT. Insects Betray Themselves in Nature to Predators by Rapid Isomerization of Green Leaf Volatiles. Science, 2010, 329: 1075-1078

[6] BruceTJA, PickettJA. Perception of plant volatile blends by herbivorous insects – Finding the right mix. Phytochemistry, 2011, 72: 1605-1611

[7] Bryant JP, Clausen TP, Reichardt PB, McCarthy MC, Werner RA. Effect of nitrogen fertilization upon the secondary chemistry and nutritional value of quaking aspen (Populus tremuloides Michx.) leaves for the large aspen tortrix (Choristoneura conflictana (Walker)). Oecologia. 1987;73:513–7.

[8] CamargoELO, NascimentoLC, SolerM, SalazarMM, Lepikson-NetoJ, MarquesWL, AlvesA, TeixeiraPJPL, MieczkowskiP, CarazzolleMF, MartinezY, DeckmannAC, RodriguesJC, Grima-PettenatiJ, PereiraGAG. Contrasting nitrogen fertilization treatments impact xylem gene expression and secondary cell wall lignification in Eucalyptus. BMC Plant Biol, 2014, 14: 256

[9] CaoM, PlatreMP, TsaiH-H, ZhangL, NoboriT, ArmengotL, ChenY, HeW, BrentL, CollNS, EckerJR, GeldnerN, BuschW. Spatial IMA1 regulation restricts root iron acquisition on MAMP perception. Nature, 2024, 625: 750-759

[10] CeaseAJ, ElserJJ, FordCF, HaoS, KangL, HarrisonJF. Heavy Livestock Grazing Promotes Locust Outbreaks by Lowering Plant Nitrogen Content. Science, 2012, 335: 467-469

[11] ChamanME, CopajaSV, ArgandoñaVH. Relationships between Salicylic Acid Content, Phenylalanine Ammonia-lyase (PAL) Activity, and Resistance of Barley to Aphid Infestation. J Agr Food Chem, 2003, 51: 2227-2231

[12] Chen Y. Analyzing Blends of Herbivore-Induced Volatile Organic Compounds With Factor Analysis: Revisiting “Cotton Plant, Gossypium hirsutum L., Defense in Response to Nitrogen Fertilization.” J Econ Entomol. 2013;106:1053–7.

[13] ChenS, ZhangL, CaiX, LiX, BianL, LuoZ, LiZ, ChenZ, XinZ. (E)-Nerolidol is a volatile signal that induces defenses against insects and pathogens in tea plants. Hortic Res, 2020, 7: 52

[14] ChiniA, MonteI, ZamarreñoAM, García-MinaJM, SolanoR. Evolution of the jasmonate ligands and their biosynthetic pathways. New Phytol, 2023, 238: 2236-2246

[15] ComadiraG, RasoolB, KarpinskaB, MorrisJ, VerrallSR, HedleyPE, FoyerCH, HancockRD. Nitrogen deficiency in barley (Hordeum vulgare) seedlings induces molecular and metabolic adjustments that trigger aphid resistance. J Exp Bot, 2015, 66: 3639-3655

[16] Connick VJ. The impact of silicon fertilisation on the chemical ecology of grapevine, Vitis vinifera; constitutive and induced chemical defences against arthropod pests and their natural enemies. Charles Sturt University; 2011.

[17] CuiJ-R, BingX-L, TangY-J, LiuF, RenL, ZhouJ-Y, LiuH-H, WangM-K, HoffmannAA, HongX-Y. A conserved protein disulfide isomerase enhances plant resistance against herbivores. Plant Physiol, 2022, 191: 660-678

[18] D’alessandroM, ErbM, TonJ, BrandenburgA, KarlenD, ZopfiJ, TurlingsTCJ. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ, 2014, 37: 813-826

[19] De MoraesCM, MescherMC, TumlinsonJH. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature, 2001, 410: 577-580

[20] DebonaD, CruzMFA, RodriguesFA. Calcium-triggered accumulation of defense-related transcripts enhances wheat resistance to leaf blast. Trop Plant Pathol, 2017, 42: 309-314

[21] DelphiaCM, MescherMC, De MoraesCM. Induction of Plant Volatiles by Herbivores with Different Feeding Habits and the Effects of Induced Defenses on Host-Plant Selection by Thrips. J Chem Ecol, 2007, 33: 997-1012

[22] DiC, NingC, HuangL-Q, WangC-Z. Design of larval chemical attractants based on odorant response spectra of odorant receptors in the cotton bollworm. Insect Biochem Mol Biol, 2017, 84: 48-62

[23] DivekarPA, NarayanaS, DivekarBA, KumarR, GadratagiBG, RayA, SinghAK, RaniV, SinghV, SinghAK, KumarA, SinghRP, MeenaRS, BeheraTK. Plant Secondary Metabolites as Defense Tools against Herbivores for Sustainable Crop Protection. Int J Mol Sci, 2022, 23: 2690

[24] DudarevaN, KlempienA, MuhlemannJK, KaplanI. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol, 2013, 198: 16-32

[25] Duran-FloresD, HeilM. Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol, 2016, 32: 77-87

[26] EngelberthJ, AlbornHT, SchmelzEA, TumlinsonJH. Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci U S A, 2004, 101: 1781-1785

[27] ErbM, ReymondP. Molecular Interactions Between Plants and Insect Herbivores. Annu Rev Plant Biol, 2019, 70: 527-557

[28] ErbM, ZüstT, RobertCAM. Using plant chemistry to improve interactions between plants, herbivores and their natural enemies: challenges and opportunities. Curr Opin Biotechnol, 2021, 70: 262-265

[29] GencerN, KumralN, Seidi ArslanM, PehlevanB. Attraction responses of ladybird beetle Hippodamia variegata (Goeze, 1777) (Coleoptera: Coccinellidae) to single and binary mixture of synthetic herbivore-induced plant volatiles in laboratory tests. Turkish Journal of Entomology, 2017, 41: 17-26

[30] GongB, ZhangG. Interactions between plants and herbivores: A review of plant defense. Acta Ecol Sin, 2014, 34: 325-336

[31] GouinguenéSP, TurlingsTCJ. The Effects of Abiotic Factors on Induced Volatile Emissions in Corn Plants. Plant Physiol, 2002, 129: 1296-1307

[32] Goussain MM, Prado E, Moraes JC. Effect of silicon applied to wheat plants on the biology and probing behaviour of the greenbug Schizaphis graminum (Rond.) (Hemiptera: Aphididae). Neotropical Entomology. 2005;34:807–13.

[33] Grafton-CardwellEE, StelinskiLL, StanslyPA. Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Annu Rev Entomol, 2013, 58: 413-432

[34] Hall CR, Waterman JM, Vandegeer RK, Hartley SE, Johnson SN. The Role of Silicon in Antiherbivore Phytohormonal Signalling. Front Plant Sci. 2019; 10. https://doi.org/10.3389/fpls.2019.01132

[35] HanP, LavoirA-V, Rodriguez-SaonaC, DesneuxN. Bottom-Up Forces in Agroecosystems and Their Potential Impact on Arthropod Pest Management. Annu Rev Entomol, 2022, 67: 239-259

[36] Hansen AK, Pers D, Russell JA. Chapter Five - Symbiotic solutions to nitrogen limitation and amino acid imbalance in insect diets. In: Oliver KM, Russell JA, editors. Adv In Insect Phys; 2020. pp. 161–205.

[37] HatanoE, SaveerAM, Borrero-EcheverryF, StrauchM, ZakirA, BengtssonM, IgnellR, AndersonP, BecherPG, WitzgallP, DekkerT. A herbivore-induced plant volatile interferes with host plant and mate location in moths through suppression of olfactory signalling pathways. BMC Biol, 2015, 13: 75

[38] HeJ, LiuY, YuanD, DuanM, LiuY, ShenZ, YangC, QiuZ, LiuD, WenP, HuangJ, FanD, XiaoS, XinY, ChenX, JiangL, WangH, YuanL, WanJ. An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc Natl Acad Sci U S A, 2020, 117: 271-277

[39] HeZ, WebsterS, HeSY. Growth-defense trade-offs in plants. Curr Biol, 2022, 32: R634-R639

[40] Holzmueller EJ, Jose S, Jenkins MA. Influence of calcium, potassium, and magnesium on Cornus florida L. density and resistance to dogwood anthracnose. Plant Soil. 2007;290:189–99.

[41] HuL, WuZ, RobertCAM, OuyangX, ZüstT, MestrotA, XuJ, ErbM. Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth. Proc Natl Acad Sci U S A, 2021, 118

[42] HuS, YuK, YanJ, ShanX, XieD. Jasmonate perception: Ligand-receptor interaction, regulation, and evolution. Mol Plant, 2023, 16: 23-42

[43] HuangW-Q, ZengG, ZhiJ-R, QiuX-Y, YinZ-J. Exogenous Calcium Suppresses the Oviposition Choices of Frankliniella occidentalis (Thysanoptera: Thripidae) and Promotes the Attraction of Orius similis (Hemiptera: Anthocoridae) by Altering Volatile Blend Emissions in Kidney Bean Plants. Insects, 2022, 13: 1127

[44] IslamT, MooreBD, JohnsonSN. Silicon suppresses a ubiquitous mite herbivore and promotes natural enemy attraction by altering plant volatile blends. J Pest Sci, 2022, 95: 423-434

[45] IslamT, MooreBD, JohnsonSN. Silicon fertilisation affects morphological and immune defences of an insect pest and enhances plant compensatory growth. J Pest Sci, 2023, 96: 41-53

[46] JausetAM, SarasúaMJ, AvillaJ, AlbajesR. Effect of nitrogen fertilization level applied to tomato on the greenhouse whitefly. Crop Prot, 2000, 19: 255-261

[47] JhuM-Y, SinhaNR. Parasitic Plants: An Overview of Mechanisms by Which Plants Perceive and Respond to Parasites. Annu Rev Plant Biol, 2022, 73: 433-455

[48] JiangN, FanX, LinW, WangG, CaiK. Transcriptome Analysis Reveals New Insights into the Bacterial Wilt Resistance Mechanism Mediated by Silicon in Tomato. Int J Mol Sci, 2019, 20: 761

[49] Jin J, Zhao M, Jing T, Zhang M, Lu M, Yu G, Wang J, Guo D, Pan Y, Hoffmann TD, Schwab W, Song C. Volatile compound-mediated plant–plant interactions under stress with the tea plant as a model. Hortic Res. 2023;10:uhad143.

[50] JoernA, ProvinT, BehmerST. Not just the usual suspects: Insect herbivore populations and communities are associated with multiple plant nutrients. Ecology, 2012, 93: 1002-1015

[51] JohnsonSN, ReynoldsOL, GurrGM, EsveldJL, MooreBD, ToryGJ, GherlendaAN. When resistance is futile, tolerate instead: silicon promotes plant compensatory growth when attacked by above- and belowground herbivores. Biol Lett, 2019, 15: 20190361

[52] Kline DL, Allan SA, Bernier UR, Welch CH. Evaluation of the enantiomers of 1-octen-3-ol and 1-octyn-3-ol as attractants for mosquitoes associated with a freshwater swamp in Florida, U.S.A. Med Vet Entomol. 2007;21:323–31.

[53] Kong Y, Wang G, Chen X, Li L, Zhang X, Chen S, He Y, Hong G. OsPHR2 modulates phosphate starvation-induced OsMYC2 signalling and resistance to Xanthomonas oryzae pv. oryzae. Plant Cell Environ. 2021;44:3432–44.

[54] KvedarasOL, KeepingMG. Silicon impedes stalk penetration by the borer Eldana saccharina in sugarcane. Entomol Exp Appl, 2007, 125: 103-110

[55] KvedarasOL, AnM, ChoiYS, GurrGM. Silicon enhances natural enemy attraction and biological control through induced plant defences. Bull Entomol Res, 2010, 100: 367-371

[56] LahaD, JohnenP, AzevedoC, DynowskiM, WeißM, CapolicchioS, MaoH, IvenT, SteenbergenM, FreyerM, GauglerP, de CamposMKF, ZhengN, FeussnerI, JessenHJ, Van WeesSCM, SaiardiA, SchaafG. VIH2 Regulates the Synthesis of Inositol Pyrophosphate InsP8 and Jasmonate-Dependent Defenses in Arabidopsis. Plant Cell, 2015, 27: 1082-1097

[57] Le Gall M, Word ML, Thompson N, Beye A, Cease AJ. Nitrogen fertilizer decreases survival and reproduction of female locusts by increasing plant protein to carbohydrate ratio. J Anim Ecol. 2020;89:2214–21.

[58] LewandowskaM, KeylA, FeussnerI. Wax biosynthesis in response to danger: its regulation upon abiotic and biotic stress. New Phytol, 2020, 227: 698-713

[59] LiZ-X, WangD-X, ShiW-X, WengB-Y, ZhangZ, SuS-H, SunY-F, TanJ-F, XiaoS, XieR-H. Nitrogen-mediated volatilisation of defensive metabolites in tomato confers resistance to herbivores. Plant Cell Environ, 2024, 47: 3227-3240

[60] LinS-C, LiY, HuF-Y, WangC-L, KuangY-H, SungC-L, TsaiS-F, YangZ-W, LiC-P, HuangS-H, LiaoC-T, HechanovaSL, JenaKK, ChuangW-P. Effect of nitrogen fertilizer on the resistance of rice near-isogenic lines with BPH resistance genes. Bot Stud, 2022, 63: 16

[61] LinY, LinX, DingC, XiaM, XueR, SunZ, ChenD, Zhu-SalzmanK, ZengR, SongY. Priming of rice defense against a sap-sucking insect pest brown planthopper by silicon. J Pest Sci, 2022, 95: 1371-1385

[62] LiuF, XiangS, YangX, SunS. Comparison of leaf mass per area, photosynthetic capacity and chemical defense traits of four evergreen broad-leaved tree species under contrasting light conditions. Chin J App Environ Biol, 2010, 16: 462-467

[63] LiuJ, ZhuJ, ZhangP, HanL, ReynoldsOL, ZengR, WuJ, ShaoY, YouM, GurrGM. Silicon Supplementation Alters the Composition of Herbivore Induced Plant Volatiles and Enhances Attraction of Parasitoids to Infested Rice Plants. Front Plant Sci, 2017, 8: 1265

[64] LiuZ, WangM, WuM, LiX, LiuH, NiuN, LiS, ChenL. Volatile organic compounds (VOCs) from plants: From release to detection. Trends Anal Chem, 2023, 158

[65] LiuG, WangQ, ChenH, WangY, ZhouX, BaoD, WangN, SunJ, HuangF, YangM, ZhangH, YanP, LiX, ShiJ, FuJ. Plant-derived monoterpene S-linalool and β-ocimene generated by CsLIS and CsOCS-SCZ are key chemical cues for attracting parasitoid wasps for suppressing Ectropis obliqua infestation in Camellia sinensis L. Plant Cell Environ, 2024, 47: 913-927

[66] MaedaT, KishimotoH, WrightLC, JamesDG. Mixture of Synthetic Herbivore-induced Plant Volatiles Attracts More Stethorus punctum picipes (Casey) (Coleoptera: Coccinellidae) than a Single Volatile. J Insect Behav, 2015, 28: 126-137

[67] Malook S ul, Xu Y, Qi J, Li J, Wang L, Wu J. Mythimna separata herbivory primes maize resistance in systemic leaves. J Exp Bot. 2021;72:3792–805.

[68] MandlikR, ThakralV, RaturiG, ShindeS, NikolićM, TripathiDK, SonahH, DeshmukhR. Significance of silicon uptake, transport, and deposition in plants. J Exp Bot, 2020, 71: 6703-6718

[69] MaselouDA, AnastasakiE, MilonasPG. The Role of Host Plants, Alternative Food Resources and Herbivore Induced Volatiles in Choice Behavior of an Omnivorous Predator. Front Ecol Evol, 2019

[70] MasseyFP, HartleySE. Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol, 2009, 78: 281-291

[71] MeldauS, ErbM, BaldwinIT. Defence on demand: mechanisms behind optimal defence patterns. Ann Bot, 2012, 110: 1503-1514

[72] MohammedK, AgarwalM, DuXB, NewmanJ, RenY. Behavioural responses of the parasitoid Aphytis melinus to volatiles organic compounds (VOCs) from Aonidiella aurantii on its host fruit Tahitian lime fruit Citrus latifolia. Biol Control, 2019, 133: 103-109

[73] MonsonRK, TrowbridgeAM, LindrothRL, LerdauMT. Coordinated resource allocation to plant growth–defense tradeoffs. New Phytol, 2022, 233: 1051-1066

[74] MosblechA, KönigS, StenzelI, GrzeganekP, FeussnerI, HeilmannI. Phosphoinositide and Inositolpolyphosphate Signalling in Defense Responses of Arabidopsis thaliana Challenged by Mechanical Wounding. Mol Plant, 2008, 1: 249-261

[75] MosblechA, ThurowC, GatzC, FeussnerI, HeilmannI. Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J, 2011, 65: 949-957

[76] MunawarA, ZhangY, ZhongJ, GeY, Abou El-ElaAS, MaoZ, NtiriES, MaoL-J, ZhuZ, ZhouW. Heat stress affects potato’s volatile emissions that mediate agronomically important trophic interactions. Plant Cell Environ, 2022, 45: 3036-3051

[77] MundimFM, BrunaEM, Vieira-NetoEHM, VasconcelosHL. Attack frequency and the tolerance to herbivory of Neotropical savanna trees. Oecologia, 2012, 168: 405-414

[78] NawazM, SunJ, ShabbirS, KhattakWA, RenG, NieX, BoY, JavedQ, DuD, SonneC. A review of plants strategies to resist biotic and abiotic environmental stressors. Sci Total Environ, 2023, 900

[79] NguyenTH, GoossensA, LacchiniE. Jasmonate: A hormone of primary importance for plant metabolism. Curr Opin Plant Biol, 2022, 67

[80] Ortiz-CarreonFR, RojasJC, CisnerosJ, MaloEA. Herbivore-Induced Volatiles from Maize Plants Attract Chelonus insularis, an Egg-Larval Parasitoid of the Fall Armyworm. J Chem Ecol, 2019, 45: 326-337

[81] PandeyBK, VermaL, PrustyA, SinghAP, BennettMJ, TyagiAK, GiriJ, MehraP. OsJAZ11 regulates phosphate starvation responses in rice. Planta, 2021, 254: 8

[82] PaulilloLCMS, LopesAR, CristofolettiPT, ParraJRP, TerraWR, Silva-FilhoMC. Changes in Midgut Endopeptidase Activity of Spodoptera frugiperda (Lepidoptera: Noctuidae) are Responsible for Adaptation to Soybean Proteinase Inhibitors. J Econ Entomol, 2000, 93: 892-896

[83] PeñaflorMFGV, ErbM, MirandaLA, WerneburgAG, BentoJMS. Herbivore-Induced Plant Volatiles Can Serve as Host Location Cues for a Generalist and a Specialist Egg Parasitoid. J Chem Ecol, 2011, 37: 1304-1313

[84] PicherskyE, NoelJP, DudarevaN. Biosynthesis of Plant Volatiles: Nature’s Diversity and Ingenuity. Science, 2006, 311: 808-811

[85] PrudicKL, OliverJC, BowersMD. Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia, 2005, 143: 578-587

[86] QianJ, ZhuC, LiJ, YangY, GuD, LiaoY, ZengL, YangZ. The Circadian Clock Gene PHYTOCLOCK1 Mediates the Diurnal Emission of the Anti-Insect Volatile Benzyl Nitrile from Damaged Tea (Camellia sinensis) Plants. J Agr Food Chem, 2024, 72: 13284-13296

[87] QinZ, GeY, JiaW, ZhangL, FengM, HuangX, FuZ, ShiW. Nitrogen fertilization enhances growth and development of Cacopsylla chinensis by modifying production of ferulic acid and amino acids in pears. J Pest Sci, 2023, 97: 1417-1431

[88] QuilisJ, López-GarcíaB, MeynardD, GuiderdoniE, SanSB. Inducible expression of a fusion gene encoding two proteinase inhibitors leads to insect and pathogen resistance in transgenic rice. Plant Biotechnol J, 2014, 12: 367-377

[89] RashidMM, JahanM, IslamKS. Impact of Nitrogen, Phosphorus and Potassium on Brown Planthopper and Tolerance of Its Host Rice Plants. Rice Sci, 2016, 23: 119-131

[90] RenL-L, HardyG, LiuZ-D, WeiW, DaiH-G. Corn Defense Responses to Nitrogen Availability and Subsequent Performance and Feeding Preferences of Beet Armyworm (Lepidoptera: Noctuidae). J Econ Entomol, 2013, 106: 1240-1249

[91] ReynoldsOL, PadulaMP, ZengR, GurrGM. Silicon: Potential to Promote Direct and Indirect Effects on Plant Defense Against Arthropod Pests in Agriculture. Front Plant Sci, 2016, 7: 744

[92] Sarwar M. Effects of potassium fertilization on population build up of rice stem borers (lepidopteron pests) and rice (Oryza sativa L.) yield. Journal of Cereals and Oilseeds. 2012;3:6–9.

[93] SchweizerF, Fernández-CalvoP, ZanderM, Diez-DiazM, FonsecaS, GlauserG, LewseyMG, EckerJR, SolanoR, ReymondP. Arabidopsis Basic Helix-Loop-Helix Transcription Factors MYC2, MYC3, and MYC4 Regulate Glucosinolate Biosynthesis, Insect Performance, and Feeding Behavior. Plant Cell, 2013, 25: 3117-3132

[94] SheardLB, TanX, MaoH, WithersJ, Ben-NissanG, HindsTR, KobayashiY, HsuF-F, SharonM, BrowseJ, HeSY, RizoJ, HoweGA, ZhengN. Jasmonate perception by inositol-phosphate-potentiated COI1–JAZ co-receptor. Nature, 2010, 468: 400-405

[95] SinghV, SoodAK. Plant Nutrition: A tool for the management of hemipteran insect-pests-A review. Agric Rev, 2017, 38: 260-270

[96] SinghA, KumarA, HartleyS, SinghIK. Silicon: its ameliorative effect on plant defense against herbivory. J Exp Bot, 2020, 71: 6730-6743

[97] SoléR. Using information theory to decode network coevolution. Science, 2020, 368: 1315-1316

[98] SunQ, LiuX, YangJ, LiuW, DuQ, WangH, FuC, LiW-X. MicroRNA528 Affects Lodging Resistance of Maize by Regulating Lignin Biosynthesis under Nitrogen-Luxury Conditions. Mol Plant, 2018, 11: 806-814

[99] SunX, SiemannE, LiuZ, WangQ, WangD, HuangW, ZhangC, DingJ. Root-feeding larvae increase their performance by inducing leaf volatiles that attract above-ground conspecific adults. J Ecol, 2019, 107: 2713-2723

[100] SunY, WangM, MurLAJ, ShenQ, GuoS. Unravelling the Roles of Nitrogen Nutrition in Plant Disease Defences. Int J Mol Sci, 2020, 21: 572

[101] SunJ, XiaoS, XueC. The tug-of-war on iron between plant and pathogen. Phytopathology Research, 2023, 5: 61

[102] TakemotoH, TakabayashiJ. Parasitic Wasps Aphidius ervi are More Attracted to a Blend of Host-Induced Plant Volatiles than to the Independent Compounds. J Chem Ecol, 2015, 41: 801-807

[103] ThinesB, KatsirL, MelottoM, NiuY, MandaokarA, LiuG, NomuraK, HeSY, HoweGA, BrowseJ. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature, 2007, 448: 661-665

[104] ValimH, DaltonH, JooY, McGaleE, HalitschkeR, GaquerelE, BaldwinIT, SchumanMC. TOC1 in Nicotiana attenuata regulates efficient allocation of nitrogen to defense metabolites under herbivory stress. New Phytol, 2020, 228: 1227-1242

[105] VeyratN, RobertCAM, TurlingsTCJ, ErbM. Herbivore intoxication as a potential primary function of an inducible volatile plant signal. J Ecol, 2016, 104(2): 591-600

[106] VirlaEG, AlbarracínEBL, DíazC, Van NieuwenhoveGA, FernándezFD, AráozMVC, MelchertNA, ConciLR, PecciMPG. Bottom-up effect of nitrogen fertilization on the density of the corn leafhopper and its impact on both disease incidence and natural parasitism. J Pest Sci, 2023, 96: 93-104

[107] WaldbauerGP, CohenRW, FriedmanS. Self-Selection of an Optimal Nutrient Mix from Defined Diets by Larvae of the Corn Earworm, Heliothis zea (Boddie). Physiol Zool, 1984, 57: 590-597

[108] WangH, ChenH, WangZ, LiuJ, ZhangX, LiC, ZengX. Molecular Identification, Expression, and Functional Analysis of a General Odorant-Binding Protein 1 of Asian Citrus Psyllid. Environ Entomol, 2019, 48: 245-252

[109] WangB, DongW, LiH, D’OnofrioC, BaiP, ChenR, YangL, WuJ, WangX, WangB, AiD, KnollW, PelosiP, WangG. Molecular basis of (E)-β-farnesene-mediated aphid location in the predator Eupeodes corollae. Curr Biol, 2022, 32: 951-962.e7

[110] WangW, WangX, LiaoH, FengY, GuoY, ShuY, WangJ. Effects of Nitrogen Supply on Induced Defense in Maize (Zea mays) against Fall Armyworm (Spodoptera frugiperda). Int J Mol Sci, 2022, 23: 10457

[111] WangJ, WeiJ, YiT, LiY-Y, XuT, ChenL, XuH. A green leaf volatile, (Z)-3-hexenyl-acetate, mediates differential oviposition by Spodoptera frugiperda on maize and rice. BMC Biol, 2023, 21: 140

[112] WebsterB, BruceT, DufourS, BirkemeyerC, BirkettM, HardieJ, PickettJ. Identification of Volatile Compounds Used in Host Location by the Black Bean Aphid. Aphis Fabae J Chem Ecol, 2008, 34: 1153-1161

[113] WetzelWC, KharoubaHM, RobinsonM, HolyoakM, KarbanR. Variability in plant nutrients reduces insect herbivore performance. Nature, 2016, 539: 425-427

[114] WuH, LiR-T, DongJ-F, JiangN-J, HuangL-Q, WangC-Z. An odorant receptor and glomerulus responding to farnesene in Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochem Mol Biol, 2019, 115

[115] WuS, HuC, ZhuC, FanY, ZhouJ, XiaX, ShiK, ZhouY, FoyerCH, YuJ. The MYC2-PUB22-JAZ4 module plays a crucial role in jasmonate signaling in tomato. Mol Plant, 2024, 17: 598-613

[116] XiaoY, WangQ, ErbM, TurlingsTCJ, GeL, HuL, LiJ, HanX, ZhangT, LuJ, ZhangG, LouY. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett, 2012, 15: 1130-1139

[117] XieH, DurieuxD, FanJ, LiuY, BragardC, HaubrugeE, SunJ, FrancisF, ChenJ. Effect of wheat plant volatiles on aphids and associated predator behavior: selection of efficient infochemicals for field study. Chinese Bulletin of Entomology, 2014, 51: 1470-1478

[118] Xu P, Zhu F, Buss G, Leal W. 1-Octen-3-ol – the attractant that repels. F1000 Research. 2015;4.

[119] XuH, XieH, WuS, WangZ, HeK. Effects of Elevated CO2 and Increased N Fertilization on Plant Secondary Metabolites and Chewing Insect Fitness. Front Plant Sci, 2019

[120] XuS, LiL, XueB, GuoM, RenQ. Effect of potassium application and aphid feeding-induced salicylic acid on insect resistance in potato. Acta Entomol Sin, 2019, 62: 343-350

[121] YangL, HanY, LiP, WenL, HouM. Silicon amendment to rice plants impairs sucking behaviors and population growth in the phloem feeder Nilaparvata lugens (Hemiptera: Delphacidae). Sci Rep, 2017, 7: 1101

[122] YeM, SongY, LongJ, WangR, BaersonSR, PanZ, Zhu-SalzmanK, XieJ, CaiK, LuoS, ZengR. Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci U S A, 2013, 110: E3631-E3639

[123] YeM, GlauserG, LouY, ErbM, HuL. Molecular Dissection of Early Defense Signaling Underlying Volatile-Mediated Defense Regulation and Herbivore Resistance in Rice. Plant Cell, 2019, 31: 687-698

[124] YuH, ZhangY, WuK, GaoXW, GuoYY. Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environ Entomol, 2008, 37: 1410-1415

[125] YuH, ZhangY, LiY, LuZ, LiX. Herbivore- and MeJA-induced volatile emissions from the redroot pigweed Amaranthus retroflexus Linnaeus: their roles in attracting Microplitis mediator (Haliday) parasitoids. Arthropod-Plant Interactions, 2018, 12: 575-589

[126] ZengG, ZhiJ, YeM, YueW, SongJ. Inductive effects of exogenous calcium on the defense of kidney bean plants against Frankliniella occidentalis (Thysanoptera: Thripidae). Arthropod-Plant Interactions, 2020, 14: 473-480

[127] ZhangW, WuL, DingY, YaoX, WuX, WengF, LiG, LiuZ, TangS, DingC, WangS. Nitrogen fertilizer application affects lodging resistance by altering secondary cell wall synthesis in japonica rice (Oryza sativa). J Plant Res, 2017, 130: 859-871

[128] ZhangP-J, WeiJ-N, ZhaoC, ZhangY-F, LiC-Y, LiuS-S, DickeM, YuX-P, TurlingsTCJ. Airborne host–plant manipulation by whiteflies via an inducible blend of plant volatiles. Proc Natl Acad Sci U S A, 2019, 116: 7387-7396

[129] ZhangY, RenY, WangX, LiuY, WangN. Responses to Host Plant Volatiles and Identification of Odorant Binding Protein and Chemosensory Protein Genes in Bradysia odoriphaga. ACS Omega, 2019, 4: 3800-3811

[130] ZhangJ, HeN, LiuC, XuL, ChenZ, LiY, WangR, YuG, SunW, XiaoC, ChenHYH, ReichPB. Variation and evolution of C: N ratio among different organs enable plants to adapt to N-limited environments. Glob Chang Biol, 2020, 26: 2534-2543

[131] ZhengY, ZhangX, LiuX, QinN, XuK, ZengR, LiuJ, SongY. Nitrogen Supply Alters Rice Defense Against the Striped Stem Borer Chilo suppressalis. Front Plant Sci, 2021, 12

[132] ZhengY, LiuQ, ShiS, ZhuX, ChenY, LinS, TianH, HuangL, WeiH. Nitrogen Deficiency Enhances Eggplant Defense against Western Flower Thrips via the Induction of the Jasmonate Pathway. Plants, 2024, 13: 273

[133] Zhu-SalzmanK, ZengR. Insect Response to Plant Defensive Protease Inhibitors. Annu Rev Entomol, 2015, 60: 233-252

Funding

National Natural Science Foundation of China(32202468)

Basic and Applied Basic Research Foundation of Guangdong Province(2021A1515110126)

Basic and Applied Basic Research Foundation of Guangdong Province(2023A1515012213)