Abstract
Head blight caused by Fusarium graminearum (F. graminearum) is one of the major threats to wheat and barley around the world. The importance of this disease is due to a reduction in both grain yield and quality in infected plants. Currently, there is limited knowledge about the physiological mechanisms involved in plant resistance against this pathogen. To reveal the physiological mechanisms underlying the resistance to F. graminearum, spikes of resistant (Sumai3) and susceptible (Falat) wheat cultivars were analyzed 4 days after inoculation, as the first symptoms of pathogen infection appeared. F. graminearum inoculation resulted in a greater induction level and activity of salicylic acid (SA), callose, phenolic compounds, peroxidase, phenylalanine ammonia lyase (PAL), and polyphenol oxidase in resistant versus susceptible cultivars. Soil drench application to spikes of SA, 24 h before inoculation with F. graminearum alleviated Fusarium head blight symptoms in both resistant and susceptible cultivars. SA treated plants showed a significant increment in hydrogen peroxide (H2O2) production, lipid peroxidation, SA, and callose content. SA-induced H2O2 level seems to be related to increased superoxide dismutase and decreased catalase activities. In addition, real-time quantitative PCR analysis showed that SA pretreatment induced expression of PAL genes in both infected and non-infected head tissues of the susceptible and resistant cultivars. Our data showed that soil drench application of SA activates antioxidant defense responses and may subsequently induce systemic acquired resistance, which may contribute to the resistance against F. graminearum. These results provide novel insights about the physiological and molecular role of SA in plant resistance against hemi-biotrophic pathogen infection.
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References
Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiol 95(1):269–273
Aebi H, Catalase BH (1974) Methods of enzymatic analysis. Academic Press, New York
Agrios G (2005) Plant pathology, 5th edn. Academic Press, New York
Ali MB, Hahn EJ, Paek KY (2007) Methyl jasmonate and salicylic acid induced oxidative stress and accumulation of phenolics in Panax ginseng bioreactor root suspension cultures. Molecules 12(3):607–621
Bai G, Shaner G (2004) Management and resistance in wheat and barley to Fusarium head blight 1. Annu Rev Phytopathol 42:135–161
Benner JP (1993) Pesticidal compounds from higher plants. Pestic Sci 39:95–102
Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. New Phytol 127:617–633
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
Castro MS, Fontes W (2005) Plant defense and antimicrobial peptides. Protein Pept Lett 12:11–16
Chao Y-Y, Chen C-Y, Huang W-D, Kao CH (2010) Salicylic acid-mediated hydrogen peroxide accumulation and protection against Cd toxicity in rice leaves. Plant Soil 329:327–337
Chen C, Belanger RR, Benhamou N, Paulitz TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Induced plant resistance to herbivory. Springer, pp 253–270
Devi PUM, Reddy PS, Rani NU, Reddy K, Reddy MN, Reddanna P (2000) Lipoxygenase metabolites of α-linolenic acid in the development of resistance in Pigeonpea, Cajanus cajan (L.) Millsp, seedlings against Fusarium udum infection. Eur J Plant Pathol 106:857–865
Donofrio NM, Delaney TP (2001) Abnormal callose response phenotype and hypersusceptibility to Peronospora parasitica in defense-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Mol Plant-Microbe Interact 14:439–450
Ebrahim S, Usha K, Singh B (2011) Pathogenesis related (PR) proteins in plant defense mechanism. Sci Against Microb Pathog 2:1043–1054
Garcίa-Limones C, Hervás A, Navas-Cortés JA, Jiménez-Dίaz RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris. Physiol Mol Plant Pathol 61:325–337
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314
Goy PA, Felix G, Metraux J, Meins F Jr (1992) Resistance to disease in the hybrid Nicotiana glutinosa Nicotiana debneyi is associated with high constitutive levels of β-1,3-glucanase, chitinase, peroxidase and polyphenoloxidase. Physiol Mol Plant Pathol 41:11–21
Grossman S, Zakut R (1979) Determination of the activity of lipoxygenase (lipoxidase). Methods Biochem Anal 25:303–329
Gunnaiah R, Kushalappa AC, Duggavathi R, Fox S, Somers DJ (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PloS One 7:e40695
Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40:347–369
Harfouche AL, Rugini E, Mencarelli F, Botondi R, Muleo R (2008) Salicylic acid induces H2O2 production and endochitinase gene expression but not ethylene biosynthesis in Castanea sativa in vitro model system. J Plant Physiol 165:734–744
Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68:14–25
He C, Wolyn D (2005) Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. sp. asparagi. Plant Pathol 54:227–232
Heath MC (2000) Hypersensitive response-related death. In: Programmed cell death in higher plants. Springer, Berlin, pp 77–90
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Helepciuc FE, Mitoi ME, Manole-Paunescu A, Aldea F, Brezeanu A, Cornea CP (2014) Induction of plant antioxidant system by interaction with beneficial and/or pathogenic microorganisms. Rom Biotech Lett 19:9366–9375
Hemm MR, Rider SD, Ogas J, Murry DJ, Chapple C (2004) Light induces phenylpropanoid metabolism in Arabidopsis roots. Plant J 38:765–778
Kang G, Wang C, Sun G, Wang Z (2003) Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ Exp Bot 50:9–15
Köhle H, Jeblick W, Poten F, Blaschek W, Kauss H (1985) Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process. Plant Physiol 77:544–551
Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165:920–931
Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159(1):75–85
Leon J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678
Li L, Steffens JC (2002) Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta 215:239–247
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant-Microbe Interact 24:183–193
Makandar R, Essig JS, Schapaugh MA, Trick HN, Shah J (2006) Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol Plant-Microbe Interact 19:123–129
Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J (2010) Involvement of salicylate and jasmonate signaling pathways in Arabidopsis interaction with Fusarium graminearum. Mol Plant-Microbe Interact 23:861–870
Makandar R, Nalam VJ, Lee H, Trick HN, Dong Y, Shah J (2012) Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Mol Plant-Microbe Interact 25:431–439
Mandal S, Mallick N, Mitra A (2009) Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol Biochem 47:642–649
Mauch-Mani B, Métraux J-P (1998) Salicylic acid and systemic acquired resistance to pathogen attack. Ann Bot 82:535–540
Mayer AM, Harel E (1979) Polyphenol oxidases in plants. Phytochemistry 18:193–215
Mhaske SD, Mahatma MK, Jha S, Singh P, Ahmad T (2013) Polyamine metabolism and lipoxygenase activity during Fusarium oxysporum f. sp. ricini-castor interaction. Physiol Mol Biol Plants 19:323–331
Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Sci 162:491–498
Mohan R, Vijayan P, Kolattukudy PE (1993) Developmental and tissue-specific expression of a tomato anionic peroxidase (tap1) gene by a minimal promoter, with wound and pathogen induction by an additional 5′-flanking region. Plant Mol Biol 22:475–490
Nalam VJ (2012) 9-Lipoxygenase oxylipin pathway in plant response to biotic stress. Denton, Texas. UNT digital library. http://digital.library.unt.edu/ark:/67531/metadc115127/
Nishimura MT, Stein M, Hou B-H, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Ochoa-Alejo N, Gómez-Peralta JE (1993) Activity of enzymes involved in capsaicin biosynthesis in callus tissue and fruits of chili pepper (Capsicum annuum L.). J Plant Physiol 141:147–152
Parry D, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grain cereals- a review. Plant Pathol 44:207–238
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316
Proctor RH, Hohn TM, McCormick SP, Desjardins AE (1995) Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl Environ Microbiol 61:1923–1930
Raju S, Jayalakshmi S, Sreeramulu K (2008) Comparative study on the induction of defense related enzymes in two different cultivars of chickpea (Cicer arietinum L) genotypes by salicylic acid, spermine and Fusarium oxysporum f. sp. ciceri. Aust J Crop Sci 2:121–140
Ramamoorthy V, Raguchander T, Samiyappan R (2002) Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 239:55–68
Raymond J, Rakariyatham N, Azanza J (1993) Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochemistry 34:927–931
Reimers PJ, Guo A, Leach JE (1992) Increased activity of a cationic peroxidase associated with an incompatible interaction between Xanthomonas oryzae pv oryzae and rice (Oryza sativa). Plant Physiol 99:1044–1050
Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28:293–305
Sekhar B, Reddy G (1982) Amino acid profiles in some scented rice varieties. Theor Appl Genet 62:35–37
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 2012:1–26
Shimada K, Fujikawa K, Yahara K, Nakamura T (1992) Antioxidative properties of xanthan on the autoxidation of soybean oil in cyclodextrin emulsion. J Agric Food Chem 40:945–948
Shin KH, Kamal AHM, Cho K, Choi JS, Yu J, Nam-Chon P, Lee YW, Lee JK, Park J-C, Kim H-T (2011) Defense proteins are induced in wheat spikes exposed to Fusarium graminearum. Plant Omics 4:270
Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–270
Silva CF, Batista LR, Schwan RF (2008) Incidence and distribution of filamentous fungi during fermentation, drying and storage of coffee (Coffea arabica L.) beans. Braz J Microbiol 39:521–526
Sood N, Sohal B, Lore J (2013) Foliar application of benzothiadiazole and salicylic acid to combat sheath blight disease of rice. Rice Sci 20:349–355
Ton J, Mauch-Mani B (2004) β-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130
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
Wang Y, Liu J-H (2012) Exogenous treatment with salicylic acid attenuates occurrence of citrus canker in susceptible navel orange (Citrus sinensis Osbeck). J Plant Physiol 169:1143–1149
Wen D, Li C, Di H, Liao Y, Liu H (2005) A universal HPLC method for the determination of phenolic acids in compound herbal medicines. J Agric Food Chem 53:6624–6629
Wertheim B (2012) Beyond the gene list: exploring transcriptomics data in search for gene function, trait mechanisms and genetic architecture. In: Functional genomics. Intech Open Access Publisher
Xu J, Duan X, Yang J, Beeching JR, Zhang P (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol 161:1517–1528
Xue RF, Wu J, Wang LF, Blair MW, Wang XM, De Ge W, Zhu ZD, Wang SM (2014) Salicylic acid enhances resistance to Fusarium oxysporum f. sp. phaseoli in Common Beans (Phaseolus vulgaris L.). J Plant Growth Regul 33:470–476
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421
Zhang J, Cui S, Li J, Wei J, Kirkham M (1995) Protoplasmic factors, antioxidant responses, and chilling resistance in maize. Plant Physiol Biochem 33:567–575
Zimmerli L, Jakab G, Métraux J-P, Mauch-Mani B (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. P Natl Acad Sci 97:12920–12925
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Our high gratitude goes to Prof. Jyoti Shah of the Department of Biological Science, University of North Texas, USA, for his constructive advice. We also thank the editor and two anonymous reviewers for constructive comments on an earlier version of this paper.
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Sorahinobar, M., Niknam, V., Ebrahimzadeh, H. et al. Central Role of Salicylic Acid in Resistance of Wheat Against Fusarium graminearum . J Plant Growth Regul 35, 477–491 (2016). https://doi.org/10.1007/s00344-015-9554-1
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DOI: https://doi.org/10.1007/s00344-015-9554-1