Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-11T08:14:55.818Z Has data issue: false hasContentIssue false
  • English
  • Français

Exogenous salicylic acid improves resistance of aphid-susceptible wheat to the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae)

Published online by Cambridge University Press:  05 April 2021

Jian-Lu Feng ,
Jie Zhang ,
Jun Yang ,
Ling-Ping Zou ,
Ting-Ting Fang ,
Huan-Li Xu  and
Qing-Nian Cai Open the ORCID record for Qing-Nian Cai [Opens in a new window]
Jian-Lu Feng
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China
Jie Zhang
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China
Jun Yang
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China
Ling-Ping Zou
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China
Ting-Ting Fang
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China
Huan-Li Xu*
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China MOA Key Laboratory of Crop Pest Monitoring and Green Control, College of Plant Protection, China Agricultural University, Beijing 100193, China
Qing-Nian Cai*
Affiliation:
College of Plant Protection, China Agricultural University, Beijing 100193, China MOA Key Laboratory of Crop Pest Monitoring and Green Control, College of Plant Protection, China Agricultural University, Beijing 100193, China
*
Author for correspondence: Qing-Nian Cai, Email: caiqn@cau.edu.cn; Huan-Li Xu, Email: hanabati@cau.edu.cn
Author for correspondence: Qing-Nian Cai, Email: caiqn@cau.edu.cn; Huan-Li Xu, Email: hanabati@cau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Salicylic acid (SA), a phytohormone, has been considered to be a key regulator mediating plant defence against pathogens. It is still vague how SA activates plant defence against herbivores such as chewing and sucking pests. Here, we used an aphid-susceptible wheat variety to investigate Sitobion avenae response to SA-induced wheat plants, and the effects of exogenous SA on some defence enzymes and phenolics in the plant immune system. In SA-treated wheat seedlings, intrinsic rate of natural increase (rm), fecundity and apterous rate of S. avenae were 0.25, 31.4 nymphs/female and 64.4%, respectively, and significantly lower than that in the controls (P < 0.05). Moreover, the increased activities of phenylalanine-ammonia-lyase, polyphenol oxidase (PPO) and peroxidase in the SA-induced seedlings obviously depended on the sampling time, whereas activities of catalase and 4-coumarate:CoA ligase were suppressed significantly at 24, 48 and 72 h in comparison with the control. Dynamic levels of p-coumaric acid at 96 h, caffeic acid at 24 and 72 h and chlorogenic acid at 24, 48 and 96 h in wheat plants were significantly upregulated by exogenous SA application. Nevertheless, only caffeic acid content was positively correlated with PPO activity in SA-treated wheat seedlings (P = 0.031). These findings indicate that exogenous SA significantly enhanced the defence of aphid-susceptible wheat variety against aphids by regulating the plant immune system, and may prove a potential application of SA in aphid control.

Keywords

Defence-related enzymesphenolic acidsalicylic acidSitobion avenaeTriticum aestivum
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 544 - 552
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors equally contributed to this work.

References

Aksoy, M (2020) A new insight into purification of polyphenol oxidase and inhibition effect of curcumin and quercetin on potato polyphenol oxidase. Protein Expression and Purification 171, 105612.CrossRefGoogle ScholarPubMed
Alba, JM, Schimmel, BC, Glas, JJ, Ataide, LM, Pappas, ML, Villarroel, CA, Schuurink, RC, Sabelis, MW and Kant, MR (2015) Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytologist 205, 828–840.CrossRefGoogle ScholarPubMed
Alvarez, MA (2014) Plant secondary metabolism. In Alvarez, MA (ed), Plant Biotechnology for Health: From Secondary Metabolites to Molecular Farming. Switzerland: Springer International Publishing, pp. 15–31.CrossRefGoogle Scholar
Ananieva, EA, Christov, KN and Popova, LP (2004) Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. Journal of Plant Physiology 161, 319–328.CrossRefGoogle ScholarPubMed
Aziz, MA, Iftkhar, A and Hanif, M (2013) Life table studies on Trilocha virescence (Bombycidae: Lepidoptera) on Ficus nitida. Asian Journal of Agriculture and Biology 1, 2–7.Google Scholar
Ballaré, CL (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends in Plant Science 16, 249–257.CrossRefGoogle ScholarPubMed
Bastias, DA, Martinez-Ghersa, MA, Newman, JA, Card, SD, Mace, WJ and Gundel, PE (2018) The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell and Environment 41, 395–405.CrossRefGoogle ScholarPubMed
Bhattarai, KK, Xie, Q-G, Pourshalimi, D, Younglove, T and Kaloshian, I (2007) Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Molecular Plant-Microbe Interactions 20, 276–282.CrossRefGoogle Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Cai, QN, Zhang, QW and Cheo, M (2004) Contribution of indole alkaloids to Sitobion avenae resistance in wheat. Journal of European Entomology 128, 517–521.Google Scholar
Campos, ML, Kang, J-H and Howe, GA (2014) Jasmonate-triggered plant immunity. Journal of Chemical Ecology 40, 657–675.CrossRefGoogle ScholarPubMed
Cao, HH, Wang, SH and Liu, TX (2014) Jasmonate- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Science 21, 47–55.CrossRefGoogle Scholar
Chrzanowski, G, Ciepiela, AP, Sprawka, I, Sempruch, C, Sytykiewicz, H and Czerniewicz, P (2003) Activity of polyphenoloxidase in the ears of spring wheat and triticale infested by grain aphid (Sitobion avenae (F.)). Electronic Journal of Polish Agricultural Universities, Biology 6, art-04.Google Scholar
Chu, HY, Wegel, E and Osbourn, A (2011) From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants. The Plant Journal 66, 66–79.CrossRefGoogle ScholarPubMed
Dong, J, Wan, G and Liang, Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. Journal of Biotechnology 148, 99–104.CrossRefGoogle ScholarPubMed
Ehlting, J, Buttner, D, Wang, Q, Douglas, CJ, Somssich, IE and Kombrink, E (1999) Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. The Plant Journal 19, 9–20.CrossRefGoogle ScholarPubMed
Engelberth, J, Viswanathan, S and Engelberth, MJ (2011) Low concentrations of salicylic acid stimulate insect elicitor responses in Zea mays seedlings. Journal of Chemical Ecology 37, 263–266.CrossRefGoogle ScholarPubMed
Fry, SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytologist 161, 641–675.CrossRefGoogle ScholarPubMed
Glinwood, R, Liu, X-F, Hu, X-S, Keller, MA, Zhao, H-Y, Wu, Y-F and Liu, T-X (2014) Tripartite interactions of barley yellow dwarf virus, Sitobion avenae and wheat varieties. PLoS ONE 9, e106639.Google Scholar
Han, Y, Wang, Y, Bi, J-L, Yang, X-Q, Huang, Y, Zhao, X, Hu, Y and Cai, Q-N (2009) Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. Journal of Chemical Ecology 35, 176–182.CrossRefGoogle ScholarPubMed
Hatcher, PE, Moore, J, Taylor, JE, Tinney, GW and Paul, ND (2004) Phytohormones and plant-herbivore-pathogen interactions: integrating the molecular with the ecological. Ecology 85, 59–69.CrossRefGoogle Scholar
Horváth, E, Janda, T, Szalai, G and Páldi, E (2002) In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Science 163, 1129–1135.CrossRefGoogle Scholar
Hu, Y, Han, Y, Zhao, X, Yang, X, Huang, Y, Lou, P and Cai, Q (2008) Dynamics and effect evaluation of three phenolic compound contents in wheat varieties with different resistances to Sitobion avenae. Chinese Journal of Applied & Environmental Biology 14, 753–756.Google Scholar
Jonathan Gogbeu, S, Mathurin Okoma, K, Beranger N'Goran, KS and Odette Dogbo, D (2015) Salicylic acid, phosphorous acid and fungicide Sumi 8 effects on polyphenol oxidases activities and Cassava resistance to anthracnose. American Journal of Agriculture and Forestry 3, 109.CrossRefGoogle Scholar
Kim, JH and Jander, G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. The Plant Journal 49, 1008–1019.CrossRefGoogle ScholarPubMed
Knobloch, K-H and Hahlbrock, K (1977) 4-Coumarate:CoA ligase from cell suspension cultures of Petroselinum hortense Hoffm: partial perification, substrate specificity, and further properties. Archives of Biochemistry and Biophysics 184, 237–248.CrossRefGoogle ScholarPubMed
Kováčik, J and Klejdus, B (2012) Tissue and method specificities of phenylalanine ammonia-lyase assay. Journal of Plant Physiology 169, 1317–1320.CrossRefGoogle ScholarPubMed
Kováčik, J, Grúz, J, Bačkor, M, Strnad, M and Repčák, M (2009) Salicylic acid-induced changes to growth and phenolic metabolism in Matricaria chamomilla plants. Plant Cell Reports 28, 135–143.CrossRefGoogle ScholarPubMed
Lajara, MM, López-Orenes, A, Ferrer, MA and Calderón, AA (2015) Long-term exposure treatments revert the initial SA-induced alterations of phenolic metabolism in grapevine cell cultures. Plant Cell, Tissue and Organ Culture (PCTOC 122, 665–673.CrossRefGoogle Scholar
Lazebnik, J, Frago, E, Dicke, M and van Loon, JJA (2014) Phytohormone mediation of interactions between herbivores and plant pathogens. Journal of Chemical Ecology 40, 730–741.CrossRefGoogle ScholarPubMed
Le Bourvellec, C, Le Quéré, J-M, Sanoner, P, Drilleau, J-F and Guyot, S (2004) Inhibition of apple polyphenol oxidase activity by procyanidins and polyphenol oxidation products. Journal of Agricultural and Food Chemistry 52, 122–130.CrossRefGoogle ScholarPubMed
Li, Y, Kim, JI, Pysh, L and Chapple, C (2015) Four isoforms of Arabidopsis thaliana 4-coumarate:CoA ligase (4CL) have overlapping yet distinct roles in phenylpropanoid metabolism. Plant Physiology 169, 2409–2421.Google ScholarPubMed
Mohase, L and van der Westhuizen, AJ (2002) Salicylic acid is involved in resistance responses in the Russian wheat aphid-wheat interaction. Journal of Plant Physiology 159, 585–590.CrossRefGoogle Scholar
Park, SW, Kaimoyo, E, Kumar, D, Mosher, S and Klessig, DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science (New York, N.Y.) 318, 113–116.CrossRefGoogle ScholarPubMed
Pieterse, CMJ, Van der Does, D, Zamioudis, C, Leon-Reyes, A and Van Wees, SCM (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489–521.CrossRefGoogle ScholarPubMed
Pyati, P, Bandani, AR, Fitches, E and Gatehouse, JA (2011) Protein digestion in cereal aphids (Sitobion avenae) as a target for plant defence by endogenous proteinase inhibitors. Journal of Insect Physiology 57, 881–891.CrossRefGoogle ScholarPubMed
Radwan, DEM (2012) Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays L.) leaves. Pesticide Biochemistry and Physiology 102, 182–188.CrossRefGoogle Scholar
Razmjou, J, Ramazani, S, Naseri, B, Ganbalani, GN and Dastjerdi, HR (2011) Resistance and susceptibility of various wheat varieties to Sitobion avenae (Hemiptera: Aphididae) in Iran. Applied Entomology and Zoology 46, 455–461.CrossRefGoogle Scholar
Reymond, P and Farmer, EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology 1, 404–411.CrossRefGoogle ScholarPubMed
Robert-Seilaniantz, A, Grant, M and Jones, JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology 49, 317–343.CrossRefGoogle ScholarPubMed
Ruelas, C, Tiznado-Hernandez, ME, Sanchez-Estrada, A, Robles-Burgueno, MR and Troncoso-Rojas, R (2006) Changes in phenolic acid content during Alternaria alternata infection in tomato fruit. Journal of Phytopathology 154, 236–244.CrossRefGoogle Scholar
Saballos, A, Sattler, SE, Sanchez, E, Foster, TP, Xin, Z, Kang, C, Pedersen, JF and Vermerris, W (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). The Plant Journal 70, 818–830.CrossRefGoogle Scholar
Smith, CM and Boyko, EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 1–16.CrossRefGoogle Scholar
Smith, JL, De Moraes, CM and Mescher, MC (2009) Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Management Science 65, 497–503.CrossRefGoogle ScholarPubMed
Tasgin, E, Atici, O, Nalbantoglu, B and Popova, L (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67, 710–715.CrossRefGoogle ScholarPubMed
Thaler, JS and Bostock, RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85, 48–58.CrossRefGoogle Scholar
Thaler, JS, Agrawal, AA and Halitschke, R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91, 1075–1082.CrossRefGoogle ScholarPubMed
Thaler, JS, Humphrey, PT and Whiteman, NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260–270.CrossRefGoogle ScholarPubMed
Urbanek Krajnc, A and Kristl, J and Ivancic, A (2011) Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus. Forest Ecology and Management 261, 416–426.CrossRefGoogle Scholar
Valiñas, MA, Lanteri, ML, ten Have, A and Andreu, AB (2017) Chlorogenic acid, anthocyanin and flavan-3-ol biosynthesis in flesh and skin of Andean potato tubers (Solanum tuberosum subsp. andigena). Food Chemistry 229, 837–846.CrossRefGoogle Scholar
Valverde, JM, Giménez, MJ, Guillén, F, Valero, D, Martínez-Romero, D and Serrano, M (2015) Methyl salicylate treatments of sweet cherry trees increase antioxidant systems in fruit at harvest and during storage. Postharvest Biology and Technology 109, 106–113.CrossRefGoogle Scholar
Vogt, T (2010) Phenylpropanoid biosynthesis. Molecular Plant 3, 2–20.CrossRefGoogle ScholarPubMed
Wang, J and Constabel, CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220, 87–96.CrossRefGoogle Scholar
Wang, M, Yuan, G, Chen, J, Lei, Z and Wu, Z (2006) Occurrence and damage characteristics of wheat aphids and identification of wheat resistance to aphids. Journal of Henan Agricultural Sciences 7, 58–60, (In Chinese).Google Scholar
Wen, P-F, Chen, J-Y, Kong, W-F, Pan, Q-H, Wan, S-B and Huang, W-D (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Science 169, 928–934.CrossRefGoogle Scholar
Zhang, Z, Meng, Z, Yao, Y and Zhou, L (2010) Change of ferulic acid content in wheat seedling. Chinese Food Science 31, 271–274.Google Scholar
Zhang, P-J, Li, W-D, Huang, F, Zhang, J-M, Xu, F-C and Lu, Y-B (2013) Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting salicylic acid signaling. Journal of Chemical Ecology 39, 612–619.CrossRefGoogle ScholarPubMed