Abstract
Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) biotype B is a key pest of Solanum lycopersicum L. (Solanaceae) throughout the world. In this study, we examined the induction of resistance on tomato plants treated with SA, BABA, and Trichoderma either individually or in combination against B. tabaci biotype B through the assessment of some biological and behavioral aspects of this insect pest. Also, to understand the mode of action of these inducers, we correlated and analyzed the biochemical basis of plant resistance, by measuring levels of polyphenol oxidase (PPO), peroxidase (POD), phenylalanine ammonia lyase (PAL), and phenolic content in leaves of treated tomato plants. The longest development time of whitefly immature stages was recorded for plants treated with root β-aminobutyric acid application (RBABA) + root Trichoderma application (RT), root salicylic acid application (RSA) + RT, and RT. In a free-choice assay, B. tabaci adults showed a significantly lower preference for settling and oviposition in RBABA + RT, RSA + RT, and RT in comparison with control. In a no-choice assay, B. tabaci females laid significantly fewer eggs on treatments than those in control, with better results observed in RBABA + RT. Plants responded to different treatments and showed higher induction of PPO, POD, and PAL activities, besides the higher accumulation of phenols in RBABA + RT, RSA + RT, and RT treatments. These results suggest that RBABA + RT, RSA + RT, and RT could be utilized for the induction of effective plant defense against B. tabaci.
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Alkooranee JT, Aledan TR, Xiang J, Lu G, Li M (2015) Induced systemic resistance in two genotypes of B. napus and R. alboglabra (RRCC) by Trichoderma isolates against S. sclerotiorum. Am J Plant Sci 6:1662–1674
Alkooranee JT, Aledan TR, Ali AK, Lu G, Zhang X, Wu J, Fu C, Li M (2017) Detecting the hormonal pathways in oilseed rape behind induced systemic resistance by Trichoderma harzianum TH12 to Sclerotinia sclerotiorum. PLoS One 12:e0168850
Arimura GI, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923
Baccelli I, Mauch-Mani B (2016) Beta-aminobutyric acid priming of plant defense: the role of ABA and other hormones. Plant Mol Biol 91:703–711
Battaglia D, Bossi S, Cascone P, Digilio MC, Prieto JD, Fanti P, Guerrier E, Iodice L, Lingua G, Lorito M, Maffei ME, Massa N, Ruocco M, Sasso R, Trotta V (2013) Tomato below ground-above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Mol Plant-Microbe Interact 26:1249–1256
Beecher GR (1998) Nutrient content of tomatoes and tomato products. Proc Soc Exp Biol Med 218:98–100
Bosch M, Berger S, Schaller A, Stintzi A (2014) Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta. BMC Plant Biol 14:257
Bouagga S, Urbaneja A, Rambla JL, Flors V, Granell A, Jaques JA, Pérez-Hedo M (2018) Zoophytophagous mirids provide an integral control of pests by inducing direct defenses, antixenosis and attraction to parasitoids in sweet pepper plants. Pest Manag Sci 74:1286–1296
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, van Loon JJA, Dicke M (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot 60:2575–2587
Canto T, Aranda MA, Fereres A (2009) Climate change effects on physiology and population processes of hosts and vectors that influence the spread of hemipteran-borne plant viruses. Glob Chang Biol 15:1884–1894
Chen Y, Ni X, Cottrell TE, Wood BW, Buntin GD (2009) Changes of oxidase and hydrolase activities in pecan leaves elicited by black pecan aphid (Hemiptera: Aphididae) feeding. J Econ Entomol 102:1262–1269
Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47:289–297
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to Herbivory. Springer Science and Business Media B.V., Dordrecht, pp 253–269
Contreras-Cornejo HA, Macias-Rodriguez L, del-Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol Ecol 92:fiw036
D’cunha GB, Satyanarayan V, Nair PM (1996) Purification of phenylalanine ammonialyase from Rhodotorula glutinis. Phytochemistry 42:17–20
D’Evoli L, Lombardi-Boccia G, Lucarini M (2013) Influence of heat treatments on carotenoid content of cherry tomatoes. Foods 2:352–363
Ferrigo D, Raiola A, Piccolo E, Scopel C, Causin R (2014) Trichoderma harzianum T22 induces in maize systemic resistance against Fusarium verticillioides. J Plant Pathol 96:133–142
Gerasimova NG, Pridvorova SM, Ozeretskovskaya OL (2005) Role of L-phenylalanine ammonia lyase in the induced resistance and susceptibility of potato plants. Appl Biochem Microbiol 41:103–105
Golizadeh A, Abedi Z, Borzoui E, Golikhajeh N, Jafary M (2016) Susceptibility of five sugar beet cultivars to the black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae). Neotrop Entomol 45:427–432
Guerrieri E, Lingua MC, Digilio Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756
Guo R, Shen W, Qian H, Zhang M, Liu L, Wang Q (2013) Jasmonic acid and glucose synergistically modulate the accumulation of glucosinolates in Arabidopsis thaliana. J Exp Bot 64:5707–5719
Guo TW, Liao CT, Chuang WP (2019) Defensive responses of rice cultivars resistant to Cnaphalocrocis medinalis (Lepidoptera: Crambidae). Arthropod Plant Interact 13:611–620
Hodge S, Pope TW, Holaschke M, Powell G (2006) The effect of beta-aminobutyric acid on the growth of herbivorous insects feeding on Brassicaceae. Ann Appl Biol 148:223–229
Iverson AL, Hammond RB, Iverson LR (2001) Induction of soybean resistance to the Mexican bean beetle (Coleoptera: Coccinellidae). J Kansas Entomol Soc 74:185–191
Khan IA, Wan FH (2015) Life history of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) biotype B on tomato and cotton host plants. J Entomol Zool Stud 3:117–121
Llorens E, García-Agustín P, Lapeña L (2017) Advances in induced resistance by natural compounds: towards new options for woody crop protection. Sci Agric 74:90–100
Lu H (2009) Dissection of salicylic acid-mediated defense signaling networks. Plant Signal Behav 4:713–720
Lu J, Li J, Ju H, Liu X, Erb M, Wang X, Lou Y (2014) Contrasting effects of ethylene biosynthesis on induced plant resistance against a chewing and a piercing-sucking herbivore in rice. Mol Plant 7:1670–1682
Mohan V, Gupta S, Thomas S, Mickey H, Charakana C, Chauhan VS, Sharma K, Kumar R, Tyagi K, Sarma S, Gupta SK, Kilambi HV, Nongmaithem S, Kumari A, Gupta P, Sreelakshmi Y, Sharma R (2016) Tomato fruits show wide phenomic diversity but fruit developmental genes show low genomic diversity. PLoS One 11:e0152907
Nouri-Ganbalani G, Borzoui E, Nouri A, Tajmiri P (2017) Effect of different potato cultivars on nutritional indices and activity of some digestive enzymes of Leptinotarsa decemlineata (Col.: Chrysomelidae). IJPPS 48:109–118
Nouri-Ganbalani G, Borzoui E, Shahnavazi M, Nouri A (2018) Induction of resistance against Plutella xylostella (L.) (Lep.: Plutellidae) by jasmonic acid and mealy cabbage aphid feeding in Brassica napus L. Front Physiol 9:859
Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723
Papadopoulou GV, van Dam NM (2017) Mechanisms and ecological implications of plant-mediated interactions between belowground and aboveground insect herbivores. Ecol Res 32:13–26
Pascual S, Nombela G, Avilés M, Muñiz M (2003) Induced resistance in tomato to whitefly Bemisia tabaci by bion. IOBC-WPRS Bull 26:61–64
Peñalver-Cruz A, Garzo E, Prieto-Ruiz I, Díaz-Garro M, Winters A, Moreno A, Fereres A (2019) Feeding behavior, life history and virus transmission ability of Bemisia tabaci (Gennadius) Mediterranean species (Hemiptera: Aleyrodidae) under elevated CO2. Insect Sci. https://doi.org/10.1111/1744-7917.12661
Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A (2015) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554
Pérez-Hedo M, Rambla JL, Granell A, Urbaneja A (2018) Biological activity and specificity of Miridae-induced plant volatiles. BioControl 63:203–213
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375
Pineda A, Soler R, Pozo MJ, Rasmann S, Turlings T (2015) Above-belowground interactions involving plants, microbes and insects. Front Plant Sci 6:1–3
Plewa MJ, Smith SR, Wagner ED (1991) Diethyldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutat Res 247:57–64
Rakha M, Hanson P, Ramasamy S (2017) Identification of resistance to Bemisia tabaci Genn. In closely related wild relatives of cultivated tomato based on trichome type analysis and choice and no-choice assays. Genet Resour Crop Evol 64:247–260
Ramiro DA, Guerreiro-Filho O, Mazzafera P (2006) Phenol contents, oxidase activities, and the resistance of coffee to the leaf miner Leucoptera coffeella. J Chem Ecol 32:1977–1988
Rashid MH, Chung YR (2017) Induction of systemic resistance against insect herbivores in plants by beneficial soil microbes. Front Plant Sci 8:1816
SAS (2011) SAS® software version 9.3, user’s manual. SAS Institute, Cary, NC
Sedaghatbaf R, Samih MA, Zohdi H, Zarabi M (2018) Vermicomposts of different origins protect tomato plants against the sweetpotato whitefly. J Econ Entomol 111:146–153
Stout MJ, Fidantsef AL, Duffey SS, Bostock RM (1999) Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato Lycopersicon esculentum. Physiol Mol Plant P 54:115–130
Takahashi KM, Berti Filho E, Lourenção AL (2008) Biology of Bemisia tabaci (GENN.) B-biotype and parasitism by Encarsia formosa (Gahan) on collard, soybean and tomato plants. Sci Agric 65:639–642
Tan CW, Chiang SY, Ravuiwasa KT, Yadav J, Hwang SY (2012) Jasmonate-induced defenses in tomato against Helicoverpa armigera depend in part on nutrient availability, but artificial induction via methyl jasmonate does not. Arthropod Plant Interact 6:531–541
Ton J, van der Ent S, van Hulten M, Pozo M, van Oosten V, van Loon LC, Mauch-Mani B, Turlings TCJ, Pieterse CMJ (2009) Priming as a mechanism behind induced resistance against pathogens, insects and abiotic stress. IOBC/WPRS Bull 44:3–13
Tytgat TO, Verhoeven KJ, Jansen JJ, Raaijmakers CE, Bakx-Schotman T, McIntyre LM, van der Putten WH, Biere A, van Dam NM (2013) Plants know where it hurts: root and shoot jasmonic acid induction elicit differential responses in Brassica oleracea. PLoS One 8:e65502
Verkerk RHJ (2004) Manipulation of tritrophic interactions for IPM. In: Koul O, Dhaliwal GS, Cuperus GW (eds) Intregrated Pest management: potential, Constraints and Challenges. CABI, Oxfordshire, UK, pp 55–71
Vicent MRS, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338
Vicuna D (2005) The role of peroxidases in the development of plants and their responses to abiotic stresses. Doctoral thesis. Dublin Institute of Technology. Doi:https://doi.org/10.21427/D7CW2B
Vogt T (2010) Phenylpropanoid biosyntesis. Mol Plant 3:2–20
Wang JH, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96
War AR, Sharma HC (2014) Effect of jasmonic acid and salicylic acid induced resistance in groundnut on Helicoverpa armigera. Physiol Entomol 39:136–142
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012a) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320
War AR, Paulraj MG, War MY, Ignacimuthu S (2012b) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792
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
Yip EC, Sowers RP, Helms AM, Mescher MC, De Moraes CM, Tooker JF (2019) Trade-offs between defenses against herbivores in goldenrod (Solidago altissima). Arthropod Plant Interact 13:279–287
Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA, Gols R, Dicke M (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197:1291–1299
Zhong Y, Wang B, Yan J, Cheng L, Yao L, Xiao L, Wu T (2014) DL-β-Aminobutyric acid-induced resistance in soybean against Aphis glycines Matsumura (Hemiptera: Aphididae). PLoS One 9:e85142
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The authors thank the Vali–e–Asr University of Rafsanjan (Rafsanjan, Iran) for supporting this experiment.
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FT, MAS, HA, and HS conceived and designed the experimental work and analysis; FT executed experimental work; FT and HA performed experimental data analyses; FT and HA wrote the manuscript; MAS and HS checked the English text and revised the manuscript.
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Jafarbeigi, F., Samih, M.A., Alaei, H. et al. Induced Tomato Resistance Against Bemisia tabaci Triggered by Salicylic Acid, β-Aminobutyric Acid, and Trichoderma. Neotrop Entomol 49, 456–467 (2020). https://doi.org/10.1007/s13744-020-00771-0
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DOI: https://doi.org/10.1007/s13744-020-00771-0