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Signals induced by exogenous nitric oxide and their role in controlling brown rot disease caused by Monilinia fructicola in postharvest peach fruit

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Abstract

Recent evidence suggests that nitric oxide (NO) signaling plays an important role in plant–pathogen interactions and that aconitase is a major target of NO. In the present study on the signaling role of NO in the elicitation of defense responses in peach fruit against Monilinia fructicola and subsequent effect on brown rot disease, 15 μM NO solution induced disease resistance in harvested peaches. As a potentiated elicitor, NO induced high levels of endogenous NO and superoxide (O2 ), hydrogen peroxide (H2O2), and NADPH oxidase and Ca2+-ATPase activity in the fruit. Aconitase activity in peach fruit was inhibited by NO. Activity of partially purified aconitase was inhibited in vitro by sodium nitroprusside (SNP) and H2O2; however, the inhibition could be relieved by carboxy-2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (cPTIO) or catalase (CAT), indicating that the defense response and signals induced by NO transduction depend on aconitase and conditions leading to elevated levels of NO; otherwise, H2O2 would inactivate aconitase directly in fruit. Treatment with NO resulted in salicylic acid (SA) accumulating during storage. Higher levels of jasmonic acid (JA) were detected in NO-treated fruit 48 h after the treatment. But after NO was removed, the level of SA and JA were lower than in the control. The results suggest that exogenous NO enhances resistance of harvested peach fruit against the fungus by inducing signals such as endogenous NO, reactive oxygen species (ROS), SA and JA and by inhibiting aconitase activity.

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References

  • Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246

    Article  CAS  PubMed  Google Scholar 

  • Capaldi DJ, Taylor KE (1983) A new peroxidase color reaction: oxidative coupling of 3-methyl-2-benzothiazolinone hydrazone (MBTH) with its formaldehyde azine. Application to glucose and choline oxidases. Anal Biochem 129:329–336

    Article  CAS  PubMed  Google Scholar 

  • Carafoli E (1987) Intracellular calcium homeostasis. Annu Rev Biochem 56:395–433

    Article  CAS  PubMed  Google Scholar 

  • Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J 10:491–503

    Article  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dalbasti T, Kilinc E (2005) Microelectrode for in vivo real-time detection of NO. Methods Enzymol 396:584–592

    Article  CAS  PubMed  Google Scholar 

  • Dangl J (1998) Innate immunity: plants just say NO to pathogens. Nature 394:525–527

    Article  CAS  PubMed  Google Scholar 

  • del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    Article  PubMed  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    Article  CAS  PubMed  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • Dempsey DMA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575

    Article  CAS  Google Scholar 

  • Desikan R, Hancock JT, Coffey MJ, Neill SJ (1996) Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett 382:213–217

    Article  CAS  PubMed  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374

    Article  CAS  PubMed  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Fan B, Shen L, Liu K, Zhao D, Yu M, Sheng J (2008) Interaction between nitric oxide and hydrogen peroxide in postharvest tomato resistance response to Rhizopus nigricans. J Sci Food Agr 88:1238–1244

    Article  CAS  Google Scholar 

  • Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824

    Article  CAS  PubMed  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JFH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    Article  CAS  PubMed  Google Scholar 

  • Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113:269–279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta KG, Shah JK, Brotman Y, Jahnke K, Willmitze L, Kaiser WM, Bauwe H, Igamberdiev AU (2012) Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot 63:1773–1784

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218:938–946

    Article  CAS  PubMed  Google Scholar 

  • Hung KT, Kao CH (2004) Nitric oxide acts as an antioxidant and delays methyl jasmonate-induced senescence of rice leaves. J Plant Physiol 161:43–52

    Article  CAS  PubMed  Google Scholar 

  • Jiang T, Zheng X, Li J, Jing G, Cai L, Ying T (2011) Integrated application of nitric oxide and modified atmosphere packaging to improve quality retention of button mushroom (Agaricus bisporus). Food Chem 126:1693–1699

    Article  CAS  PubMed  Google Scholar 

  • Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10:255–266

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kennedy MC, Emptage MH, Dreyer J-L, Beinert H (1983) The role of iron in the activation-inactivation of aconitase. J Biol Chem 258:11098–11105

    CAS  PubMed  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526

    Article  CAS  PubMed  Google Scholar 

  • Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant Microbe Interact 13:347–351

    Article  CAS  PubMed  Google Scholar 

  • Lai T, Wang Y, Li B, Qin G, Tian S (2011) Defense responses of tomato fruit to exogenous nitric oxide during postharvest storage. Postharvest Biol Technol 62:127–132

    Article  CAS  Google Scholar 

  • Landgraf FA, Zehr EI (1982) Inoculum sources for Monilinia fructicola in South Carolina peach orchards. Phytopathology 72:185–190

    Article  Google Scholar 

  • Leshem YY, Wills RBH, Ku VV-V (1998) Evidence for the function of the free radical gas—nitric oxide (NO)—as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Bioch 36:825–833

    Article  CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Ma W, Smigel A, Walker RK, Moeder W, Yoshioka K, Berkowitz GA (2010) Leaf senescence signaling: the Ca2+-conducting Arabidopsis cyclic nucleotide gated channel2 acts through nitric oxide to repress senescence programming. Plant Physiol 154:733–743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Manjunatha G, Raj SN, Shetty NP, Shetty HS (2008) Nitric oxide donor seed priming enhances defense responses and induces resistance against pearl millet downy mildew disease. Pestic Biochem Physiol 91:1–11

    Article  CAS  Google Scholar 

  • Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:671–681

    Google Scholar 

  • Meuwly P, Métraux J-P (1993) Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal Biochem 214:500–505

    Article  CAS  PubMed  Google Scholar 

  • Moeder W, Del Pozo O, Navarre DA, Martin GB, Klessig DF (2007) Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol Biol 63:273–287

    Article  CAS  PubMed  Google Scholar 

  • Morré DJ, Morré DM (2000) Applications of aqueous two-phase partition to isolation of membranes from plants: a periodic NADH oxidase activity as a marker for right side-out plasma membrane vesicles. J Chromatog B 743:369–376

    Article  Google Scholar 

  • Mueller MJ, Brodschelm W, Spannagl E, Zenk MH (1993) Signaling in the elicitation process is mediated through the octadecanoid pathway leading to jasmonic acid. Proc Natl Acad Sci USA 90:7490–7494

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant Microbe Interact 23:846–860

    Article  CAS  PubMed  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16:1094–1105

    Article  CAS  PubMed  Google Scholar 

  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pristijono P, Wills RBH, Golding JB (2006) Inhibition of browning on the surface of apple slices by short term exposure to nitric oxide (NO) gas. Postharvest Biol Technol 42:256–259

    Article  CAS  Google Scholar 

  • Rega AF, Garrahan PJ (eds) (1986) The Ca2+ pump of plasma membranes. CRC Press, Boca Raton

    Google Scholar 

  • Robbins KM, Bhuvarahamurthy N, Pliska-Matyshak G, Murthy PP (1999) The isolation and characterization of right-side-out plasma membrane vesicles from barley aleurone cells. Lipids 34:75–82

    Article  CAS  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santiago-García J, Delgado-Coello BA, Maas-Oliva J (2000) Thermal analysis of the plasma membrane Ca2+-ATPase. Mol Cell Biochem 209:105–112

    Article  PubMed  Google Scholar 

  • Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Li J, Zhu S, Zhou J (2011) Browning inhibition on fresh-cut chestnut kernel by exogenous nitric oxide. Int J Food Sci Technol 46:944–950

    Article  CAS  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455

    Article  CAS  PubMed  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461

    Article  CAS  PubMed  Google Scholar 

  • Van Camp W, Van Montagu M, Inzé D (1998) H2O2 and NO: redox signals in disease resistance. Trends Plant Sci 3:330–334

    Article  Google Scholar 

  • Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 276:643–648

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonate-induced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol 46:923–930

    Article  CAS  PubMed  Google Scholar 

  • Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signalling and defence responses. Curr Opin Plant Biol 7:449–455

    Article  CAS  PubMed  Google Scholar 

  • Wills RBH, Ku VV-V, Leshem YY (2000) Fumigation with nitric oxide to extend the postharvest life of strawberries. Postharvest Biol Technol 18:75–79

    Article  CAS  Google Scholar 

  • Xing T, Higgins VJ, Blumwald E (1997) Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell 9:249–259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512

    Article  CAS  PubMed  Google Scholar 

  • Zemlyanukhin AA, Eprintsev AT, Zemlyanukhin LA, Igamberdiev AU (1984) Subcellular localization of aconitate hydratase isoforms in higher plants. Soviet Plant Physiol 31:270–275

    Google Scholar 

  • Zhang LL, Zhu SH, Chen CB, Zhou J (2011) Metabolism of endogenous nitric oxide during growth and development of apple fruit. Sci Hortic Amst 127:500–506

    Article  CAS  Google Scholar 

  • Zhao R, Sheng J, Lv S, Zheng Y, Zhang J, Yu M, Shen L (2011) Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biol Technol 62:121–126

    Article  CAS  Google Scholar 

  • Zheng Y, Shen L, Yu M, Fan B, Zhao D, Liu L, Sheng J (2011) Nitric oxide synthase as a postharvest response in pathogen resistance of tomato fruit. Postharvest Biol Technol 60:38–46

    Article  CAS  Google Scholar 

  • Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ (2012) Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem 60:141–149

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann S, Nürnberger T, Frachisse J-M, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94:2751–2755

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The research work was supported by the Project of National Natural Science Foundation of China (31101371), Shandong Natural Science Foundation (ZR2010CQ039) and China Postdoctoral Science Foundation (201104605).

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Correspondence to Jing Ying Shi or Qing Guo Wang.

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Shi, J.Y., Liu, N., Gu, R.X. et al. Signals induced by exogenous nitric oxide and their role in controlling brown rot disease caused by Monilinia fructicola in postharvest peach fruit. J Gen Plant Pathol 81, 68–76 (2015). https://doi.org/10.1007/s10327-014-0562-y

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