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Physiological responses of plants and mites to salicylic acid improve the efficacy of spirodiclofen for controlling Tetranychus urticae (Acari: Tetranychidae) on greenhouse tomatoes

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Abstract

Salicylic acid (SA) is a signaling molecule that can induce plant resistance to certain herbivores. Although the role of jasmonic acid in mediating mite-tomato plant interactions has been well studied, the role of salicylic acid has not. This study examined how the application of exogenous SA, via its effects on tomato plant physiology, alters the activity of mite digestive enzymes, mite energy reserves, and mite susceptibility to spirodiclofen. Enzymatic activity—including superoxide dismutase, ascorbate peroxidase, guaiacol peroxidase, polyphenol oxidase, and phenylalanine ammonia-lyase—along with contents of total phenolic, hydrogen peroxide, and total chlorophyll significantly increased in plants 24 h after treatment with 2 mM of SA. In contrast, catalase activity significantly decreased in treated plants, and malondialdehyde content was unaffected. Mites fed on tomato plants treated with SA had significantly lower glutathione S-transferase, esterase, α-amylase, and aminopeptidase activities than those fed on control plants. Energy reserve analyses demonstrated a significant decrease in contents of lipid, protein, and glycogen in mites fed on SA-treated plants, whereas carbohydrate content significantly increased. The LC50 of spirodiclofen was decreased 1.8-fold for Tetranychus urticae fed on SA-treated tomato plants compared to controls. Treatment of adult mites with 2 mM SA on leaf discs did not cause any direct mortality after 24 h. Finally, a greenhouse bioassay confirmed that spider mite mortality following exposure to spirodiclofen was significantly higher on SA plants than on control plants. Mortality of mites exposed to half of the recommended rate of spirodiclofen was similar to those exposed to the recommended rate when they were held on treated plants. These results have valuable implications for T. urticae management programs in tomato production.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Google Scholar 

  • Acar O, Türkan I, Özdemir F (2001) Superoxide dismutase and peroxidase activities in drought sensitive and resistant barley (Hordeum vulgare L.) varieties. Acta Physiol Plant 23:351–356

    CAS  Google Scholar 

  • Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology. Academic Press, Cambridge, pp 121–126

    Google Scholar 

  • Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2:875–877

    CAS  Google Scholar 

  • Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Ahmad I (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121

    CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    CAS  Google Scholar 

  • Attia S, Grissa KL, Lognay G, Bitume E, Hance T, Mallieux AC (2013) A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides. J Pest Sci 86:361–386

    Google Scholar 

  • Barbehenn R, Cheek S, Gasperut A, Lister E, Maben R (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut fluids of Malacosoma disstria and Orgyia leucostigma caterpillars. J Chem Ecol 31:969–988

    CAS  Google Scholar 

  • Barbehenn R, Dukatz C, Holt C, Reese A, Martiskainen O, Salminen JP, Constabel CP (2010) Feeding on poplar leaves by caterpillars potentiates foliar peroxidase action in their guts and increases plant resistance. Oecologia 164:993–1004

    Google Scholar 

  • Bensoussan N, Zhurov V, Yamakawa S, O’Neil CH, Suzuki T, Grbic M, Grbic V (2018) The digestive system of the two-spotted spider mite, Tetranychus urticae (Koch), in the context of the mite-plant interaction. Fron Plant Sci 9:1–18

    Google Scholar 

  • Bi JL, Felton GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511–1530

    CAS  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116

    CAS  Google Scholar 

  • Carletto J, Martin T, Vanlerberghe-Masutti F, Brévault T (2010) Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Man Sci 66:301–307

    CAS  Google Scholar 

  • Croft H, Chen J (2017) Leaf pigment content. In: Liang S (ed) Comprehensive remote sensing. Elsevier, Amsterdam, pp 1–26

    Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    CAS  Google Scholar 

  • de Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Google Scholar 

  • Demaeght P, Dermauw W, Tsakireli D, Khajehali J, Nauen R, Tirry L, Vontas J, Lümmen P, Van Leeuwen T (2013) Molecular analysis of resistance to acaricidal spirocyclic tetronic acids in Tetranychus urticae: CYP392E10 metabolizes spirodiclofen, but not its corresponding enol. Ins Biochem Mol Biol 43:544–554

    CAS  Google Scholar 

  • Despres L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307

    Google Scholar 

  • Felton GW, Donato K, Broadway R, Duffey S (1992) Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exigua. J Ins Physiol 38:277–285

    CAS  Google Scholar 

  • Felton GW, Duffey SS (1991) Protective action of midgut catalase in lepidopteran larvae against oxidative plant defenses. J Chem Ecol 17:1715–1732

    CAS  Google Scholar 

  • Felton GW, Donato K, Del Vecchio RJ, Duffey SS (1989) Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J Chem Ecol 15:2667–2694

    CAS  Google Scholar 

  • Foray V, Pelisson PF, Bel-venner MC, Desouhant E, Venner S, Menu F, Giron D, Rey B (2012) A handbook for uncovering the complete energetic budget in insects: the van Handel’s method (1985) revisited. Physiol Entomol 37:295–302

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  Google Scholar 

  • GraphPad (2019) Graphpad Prism ver 8.2.0, GraphPad Software, La Jolla California USA. www.graphpad.com. Accessed 30 Sept 2020

  • Gunes A, Inal A, Alpaslanm M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736

    CAS  Google Scholar 

  • Hallik L, Kazantsev T, Kuusk A, Galmés J, Tomás M, Niinemets Ü (2017) Generality of relationships between leaf pigment contents and spectral vegetation indices in Mallorca (Spain). Reg Environ Change 17:2097–2109

    Google Scholar 

  • Heidel-Fischer HM, Vogel H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Cur Opin Insect Sci 8:8–14

    Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300

    Google Scholar 

  • Jafarbeigi F, Samih MA, Alaei H, Shirani H (2020) Induced tomato resistance against Bemisia tabaci triggered by salicylic acid, β-Aminobutyric Acid, and Trichoderma. Neotrop Entomol 49:456–467

    CAS  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

    CAS  Google Scholar 

  • Johnson KS, Felton GW (2001) Plant phenolics as dietary antioxidants for herbivorous insects: a test with genetically modified tobacco. J Chem Ecol 27:2579–2597

    CAS  Google Scholar 

  • Juntheikki MR, Julkunen-Tiitto R (2000) Inhibition of β-glucosidase and esterase by tannins from Betula, Salix, and Pinus species. J Chem Ecol 26:1151–1165

    CAS  Google Scholar 

  • Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Fron Plant Sci 6:1–17

    Google Scholar 

  • Kong W, Liu F, Zhang C, Zhang J, Feng H (2016) Non-destructive determination of Malondialdehyde (MDA) distribution in oilseed rape leaves by laboratory scale NIR hyperspectral imaging. Sci Rep 6:1–8

    Google Scholar 

  • Lagadic L, Caquet T, Ramade F (1994) The role of biomarkers in environmental assessment (5). Invertebrate populations and communities. Ecotoxicology 3:193–208

    CAS  Google Scholar 

  • Lee K (1991) Glutathione S-transferase activities in phytophagous insects: induction and inhibition by plant phototoxins and phenols. Insect Biochem 21:353–361

    CAS  Google Scholar 

  • Liang P, Cui JZ, Yang XQ, Gao XW (2007) Effects of host plants on insecticide susceptibility and carboxylesterase activity in Bemisia tabaci biotype B and greenhouse whitefly Trialeurodes vaporariorum. Pest Manage Sci 63:365–371

    CAS  Google Scholar 

  • Lindroth RL (1989) Differential esterase activity in Papilio glaucus subspecies: absence of cross-resistance between allelochemicals and insecticides. Pest Biochem Physiol 35:185–191

    CAS  Google Scholar 

  • Litskas VD, Migeon A, Navajas M, Tixier MS, Stavrinides MC (2019) Impacts of climate change on tomato, a notorious pest and its natural enemy: small scale agriculture at higher risk. Environ Res Lett 14:1–9

    Google Scholar 

  • Liu B, Coy M, Wang JJ, Stelinski LL (2015) The effect of host plant species on the detoxifying enzymes of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae). Fla Entomol 98:997–999

    CAS  Google Scholar 

  • Lukasik I, Golawska S (2007) Activity of Se-independant glutathione peroxidase and glutathione reductase within cereal aphid tissues. Biol Lett 4:31–39

    Google Scholar 

  • Lukasik I, Goławska S (2013) Effect of host plant on levels of reactive oxygen species and antioxidants in the cereal aphids Sitobion avenae and Rhopalosiphum padi. Biochem Syst Ecol 51:232–239

    CAS  Google Scholar 

  • Lukasik I, Golawska S, Wojcicka A (2009) Antioxidant defense mechanisms of cereal aphids based on ascorbate and ascorbate peroxidase. Biologia 64:994–998

    CAS  Google Scholar 

  • Lukasik I, Golawska S, Sytykiewicz H, Leszczynski B (2015) Antioxidant defence based on glutathione in grain aphid Sitobion avenae (F.) and the bird cherry-oat aphid Rhopalosiphum padi: responses to the host plant alteration. Allelopathy J 35:273–284

    Google Scholar 

  • Ma X, Deng D, Chen W (2017) Inhibitors and activators of SOD, GSH-Px, and CAT. In: Senturk M (ed) Enzyme inhibitors and activators. IntechOpen, London, pp 207–258

    Google Scholar 

  • Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiol Plant 117:550–557

    CAS  Google Scholar 

  • Miles PW, Oertli JJ (1993) The significance of antioxidants in the aphid-plant interaction: the redox hypothesis. Entomol Exp Appl 67:275–283

    CAS  Google Scholar 

  • Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    Google Scholar 

  • Muniz-Huerta RF, Guevera-Gonzalez RG, Contreras-Medina LM, Torres-Pacheco I, Prado-Olivarez J, Ocampo-Velazquez RV (2013) A review of methods for sensing the nitrogen status in plants: advantages, disadvantages, and recent advances. Sensors 13:10823–10843

    Google Scholar 

  • Neoliya N, Singh D, Sangawan RS (2005) Azadirachtin influences total head protein content of Helicoverpa armigera Hub. larvae. Curr Sci 88:1889–1890

    CAS  Google Scholar 

  • Nicastro RL, Sato ME, Da Silva MZ (2010) Milbemectin resistance in Tetranychus urticae (Acari: Tetranychidae): selection, stability and cross-resistance to abamectin. Exp Appl Acarol 50:231–241

    CAS  Google Scholar 

  • Ogel ZB, Yuzugullu Y, Mete S, Bakir U, Kaptan Y, Sutay D, Demir AS (2006) Production, properties and application to biocatalysis of a novel extracellular alkaline phenol oxidase from the thermophilic fungus Scytalidium thermophilum. Appl Microbiol Biotechnol 71:853–862

    CAS  Google Scholar 

  • Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front Plant Sci 8:1–13

    Google Scholar 

  • Peng J, Deng X, Jia S, Huang J, Miao X, Huang Y (2004) Role of salicylic acid in tomato defense against cotton bollworm, Helicoverpa armigera Hubner. Zeits Naturfor 59:856–862

    CAS  Google Scholar 

  • Robertson JL, Jones MM, Olguin E, Alberts B (2017) Bioassays with arthropods. CRC Press, Boca Raton

    Google Scholar 

  • Santamaria ME, González-Cabrera J, Martínez M, Grbic V, Castañera P, Ortego F (2015) Digestive proteases in bodies and faeces of the two-spotted spider mite, Tetranychus urticae. J Inst Physiol 78:69–77

    CAS  Google Scholar 

  • Schmid-Siegert E, Stepushenko O, Glauser G, Farmer EE (2016) Membranes as structural antioxidants recycling of malondialdehyde to its source in oxidation-sensitive chloroplast fatty acids. J Biol Chem 291:13005–13013

    CAS  Google Scholar 

  • Schneider S, Ullrich W (1994) Differential induction of resistance and enhanced enzyme activities in cucumber and tobacco caused by treatment with various abiotic and biotic inducers. Physiol Mol Plant Pathol 45:291–304

    CAS  Google Scholar 

  • Sethi A, McAuslane HJ, Rathinasabapathi B, Nuessly GS, Nagata RT (2009) Enzyme induction as a possible mechanism for latex-mediated insect resistance in romaine lettuce. J Chem Ecol 35:190–200

    CAS  Google Scholar 

  • Shah S, Houborg R, McCabe M (2017) Response of chlorophyll, carotenoid and SPAD-502 measurement to salinity and nutrient stress in wheat (Triticum aestivum L.). Agronomy 7:61

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037

    Google Scholar 

  • Sinclair BJ (2015) Linking energetics and overwintering in temperate insects. J Therm Biol 54:5–11

    Google Scholar 

  • Singh D, Kesavan AK, Sohal SK (2019) Exploration of anti-insect potential of trypsin inhibitor purified from seeds of Sapindus mukorossi against Bactrocera cucurbitae. Sci Rep 9:1–14

    Google Scholar 

  • Sintim HO, Tashiro T, Motoyama N (2012) Effect of sesame leaf diet on detoxification activities of insects with different feeding behavior. Arch Insect Biochem Physiol 81:148–159

    CAS  Google Scholar 

  • Snyder MJ, Champagne DE, Cohen MB, Howard JJ (1998) Effects of plant diet on detoxification enzyme activities of two grasshoppers, Melanoplus differentialis and Taeniopoda eques. J Chem Ecol 24:2151–2165

    CAS  Google Scholar 

  • Spormann S, Soares C, Fidalgo F (2019) Salicylic acid alleviates glyphosate-induced oxidative stress in Hordeum vulgare L. J Environ Manage 241:226–234

    CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    CAS  Google Scholar 

  • Tirello P, Pozzebon A, Cassanelli S, Van Leeuwen T, Duso C (2012) Resistance to acaricides in Italian strains of Tetranychus urticae: toxicological and enzymatic assays. Exp Appl Acarol 57:53–64

    CAS  Google Scholar 

  • Van der Horst DJ, Vroemen SF, Van Marrewijk WJ (1997) Metabolism of stored reserves in insect fat body: hormonal signal transduction implicated in glycogen mobilization and biosynthesis of the lipophorin system. Comp Biochem Physiol B 117:463–474

    Google Scholar 

  • Van Leeuwen T, Van Pottelberge S, Tirry L (2005) Comparative acaricide susceptibility and detoxifying enzyme activities in field-collected resistant and susceptible strains of Tetranychus urticae. Pest Manage Sci 61:499–507

    Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Khajehali J, Tirry L (2009) Genetic and biochemical analysis of a laboratory-selected spirodiclofen-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Manage Sci 65:358–366

    Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66

    CAS  Google Scholar 

  • Villarroel M, Sancho E, Andreu-Moliner E, Ferrando M (2009) Biochemical stress response in tetradifon exposed Daphnia magna and its relationship to individual growth and reproduction. Sci Total Environ 407:5537–5542

    CAS  Google Scholar 

  • Wang KY, Liu TX, Yu CH, Jiang XY, Yi MQ (2002) Resistance of Aphis gossypii (Homoptera: Aphididae) to fenvalerate and imidacloprid and activities of detoxification enzymes on cotton and cucumber. J Econ Entomol 95:407–413

    CAS  Google Scholar 

  • Wang JW, Zheng LP, Wu JY, Tan RX (2006) Involvement of nitric oxide in oxidative burst, phenylalanine ammonia-lyase activation and Taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15:351–358

    CAS  Google Scholar 

  • Wani AB, Chadar H, Wani AH, Singh S, Upadhyay N (2017) Salicylic acid to decrease plant stress. Environ Chem Lett 15:101–123

    CAS  Google Scholar 

  • War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792

    CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Google Scholar 

  • War AR, Paulraj MG, Ignacimuthu S, Sharma HC (2013) Defensive responses in groundnut against chewing and sap-sucking insects. J Plant Growth Reg 32:259–272

    CAS  Google Scholar 

  • Wei H, Zhikuan J, Qingfang H (2007) Effects of herbivore stress by Aphis medicaginis Koch on the malondialdehyde contents and the activities of protective enzymes in different alfalfa varieties. Acta Ecol Sin 27:2177–2183

    Google Scholar 

  • Xie W, Wang S, Wu Q, Feng Y, Pan H, Jiao X, Zhou L, Yang X, Fu W, Teng H (2011) Induction effects of host plants on insecticide susceptibility and detoxification enzymes of Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manage Sci 67:87–93

    CAS  Google Scholar 

  • Ximénez-Embún MG, Castañera P, Ortego F (2017) Drought stress in tomato increases the performance of adapted and non-adapted strains of Tetranychus urticae. J Insect Physiol 96:73–81

    Google Scholar 

  • Ximénez-Embún MG, Ortego F, Castañera P (2016) Drought-stressed tomato plants trigger bottom–up effects on the invasive Tetranychus evansi. PLoS ONE 11:1–19

    Google Scholar 

  • Yang X, Margolies DC, Zhu KY, Buschman LL (2001) Host plant-induced changes in detoxification enzymes and susceptibility to pesticides in the twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 94:381–387

    CAS  Google Scholar 

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Acknowledgements

This research was supported by the research and technology deputy of the University of Tehran.

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KT and HA conceived and designed the study in consultation with ET. MH and PM conducted the experiments. MH and JPM analyzed the data and wrote the paper. All authors read and approved the manuscript.

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Correspondence to J. P. Michaud.

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Homayoonzadeh, M., Moeini, P., Talebi, K. et al. Physiological responses of plants and mites to salicylic acid improve the efficacy of spirodiclofen for controlling Tetranychus urticae (Acari: Tetranychidae) on greenhouse tomatoes. Exp Appl Acarol 82, 319–333 (2020). https://doi.org/10.1007/s10493-020-00559-2

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