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Nitric Oxide Treatment and Induced Genes Role Against Phytophthora infestans in Potato

Stickoxidbehandlung und die Rolle induzierter Gene gegen Phytophthora infestans bei Kartoffeln

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Abstract

Effects of sodium nitroprusside (SNP; nitric oxide donor) treatments on enhancement of secondary metabolites production, oxidative stress mediators (\(\mathrm{O}_{2}^{-}\)) accumulation and antioxidant defense enzymes of Potato Spunta Sp. suspension culture cells elicited by a fungal extract from phytophthora infestans mycelium. The obtained data confirmed the significant increase in various oxidative burst (super oxide anion, hydrogen peroxide and total glutathione) contents. The administration of various NO concentrations strongly decreased hydrogen peroxide concentration and superoxide anion levels. Moreover, the SNP treatments regulate elicitor-induced activation of phenylalanine ammonium-lyase and total soluble phenols accumulation. The highest concentrations of NO donor sodium nitroprusside potentiated elicitor-induced H2O2 production. On the other hand, the lowest H2O2 contents coincided with elicitation regulated various activities of enzymes superoxide-dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT) and Phenyl alanine ammonia lyase (PAL) activity, the decrease in H2O2 concentration was probably due to a direct reduction interaction of NO-H2O2. On the other hand, the addition of these previous NO treatments affects mRNA peroxidase gene expression using RT-PCR techniques. In general, the addition of lower concentrations of nitric oxide reduce the mRNA peroxidase activity on contrary, the higher concentrations induced the mRNA peroxidase activity, which induce the hypersensitive reactions against fungus infection.

Zusammenfassung

Auswirkungen von Behandlungen mit Natrium-Nitroprussid (SNP, Stickoxiddonor) auf die Steigerung der Produktion von Sekundärmetaboliten, die Anreicherung von Mediatoren oxidativen Stresses (\(\mathrm{O}_{2}^{-}\)) und antioxidative Abwehrenzyme in Suspensionskulturzellen der Kartoffelsorte Spunta Sp., hervorgerufen durch ein Pilzextrakt aus Myzel der Art Phytophthora infestans. Die erzielten Daten bestätigten die signifikante Steigerung verschiedener oxidativer Bursts (Superoxidanion, Wasserstoffperoxid und Gesamtgehalt Glutathion). Die Verabreichung unterschiedlicher NO-Konzentrationen senkte die Wasserstoffperoxidkonzentration und die Superoxidanionwerte stark. Außerdem regulieren die SNP-Behandlungen die Elicitor-induzierte Aktivierung von Phenylalanin-Ammoniak-Lyase sowie die Anreicherung der Gesamtmenge löslicher Phenole. Die höchsten Konzentrationen NO-Donor-Natriumnitroprussid potenzierten die Elicitor-induzierte H2O2-Produktion. Andererseits fallen die geringsten H2O2-Werte mit verschiedenen Elicitor-regulierten Aktivitäten der Enzyme Superoxiddismutase (SOD), Ascorbatperoxidase (APX), Katalase (CAT) und Phenylalanin-Ammoniak-Lyase (PAL) zusammen. Der Rückgang in der H2O2-Konzentration lag wahrscheinlich an der direkten Reduktionsinteraktion mit NO-H2O2. Die Hinzufügung dieser o. g. NO-Behandlungen wirkt sich allerdings auch auf die mRNA-Peroxidase-Genexpression mit RT-PCR-Techniken aus. Allgemein senkt die Hinzufügung geringerer Konzentrationen Stickoxid die mRNA-Peroxidaseaktivität. Die höheren Konzentrationen induzierten aber die mRNA-Peroxidaseaktivität, was wiederum Überempfindlichkeitsreaktionen gegen die Pilzinfektion induziert.

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References

  • Abramowski D, Arasimowicz-Jelonek M, Izbiańska K, Billert H, Floryszak-Wieczorek J (2015) Nitric oxide modulates redox-mediated defense in potato challenged with Phytophthora infestans. Eur J Plant Pathol 143:237–260

    Article  CAS  Google Scholar 

  • Aebi H (1983) Catalase. In: Bergmeyer H (ed) Methods of enzymatic analysis. Verlag Chemie, Weinheim, pp 273–277

    Google Scholar 

  • Afify AMR, El-Beltagi HS (2011a) Effect of the insecticide cyanophos on liver function in adult male rats. Fresen Environ Bull 20(4a):1084–1088

    CAS  Google Scholar 

  • Afify AMR, El-Beltagi HS, Fayed SA, Shalaby EA (2011b) Acaricidal activity of successive extracts from Syzygium cumini L. Skeels (Pomposia) against Tetranychus urticae Koch. Asian Pac J Trop Biomed 1(5):359–364

    Article  CAS  PubMed Central  Google Scholar 

  • Alguacil MM, Hernandez JA, Caravaca F, Portillo B, Roldan A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid soil. Physiol Plant 118:562–570

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Drzewiecka K, Chmielowska-Bąk J, Abramowski D, Izbiańska K (2014a) Aluminum induces cross-resistance of potato to Phytophthora infestans. Planta 239:679–694

    Article  CAS  PubMed  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Abramowski D, Izbiańska K (2014b) Nitric oxide and reactive nitrogen species. In: nitric oxide in plants: metabolism and role in stress physiology. Springer, pp 165–184

    Chapter  Google Scholar 

  • Aziz A, Heyraud A, Lambert B (2004) Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botyrtis cinerea. Planta 218:767–774

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Capaldi DJ, Taylor KE (1983) A new peroxidase colour 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 

  • Cheng F‑Y, Hsu S‑Y, Kao C‑H (2002) Nitric oxide counteracts the senescence of detached rice leaves induced by dehydration and polyethylene glycol but not by sorbitol. Plant Growth Regul 38:265–272

    Article  CAS  Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 14:1380–1384

    Article  Google Scholar 

  • Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000) NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24:667–677

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 4:195–200

    Article  Google Scholar 

  • Cárdenas ML, Ryan CA (2002) Nitric oxide modulates wound signaling in tomato plants. Plant Physiol 130:487–493

    Article  Google Scholar 

  • De-Pinto MC, Tommasi F, De-Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 2:698–708

    Article  Google Scholar 

  • Del-Rio LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 2:71–81

    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 

  • Delledonne M, Murgia I, Ederle D, Sbicego PF, Biondani A, Polverari A, Lamb C (2002) Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease-resistance response. Plant Physiol Biochem 40:605–610

    Article  CAS  Google Scholar 

  • Dubreuil-Maurizi C, Vitecek J, Marty L, Branciard L, Frettinger P, Wendehenne D et al (2011) Glutathione deficiency of the arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression and the hypersensitive response. Plant Physiol 157:2000–2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Assal SE, Le J, Basu D, Mallery EL, Szymanski DB (2004) Arabidopsis GNARLED Encodes a NAP125 homolog that positively regulates ARP2/3. Curr Biol 14:1405–1409

    Article  CAS  Google Scholar 

  • El-Beltagi HS, Mohamed HI (2013) Reactive oxygen species, lipid peroxidation and antioxidative defense mechanism. Not Bot Hort Agrobot Cluj 41(1):44–57

    CAS  Google Scholar 

  • El-Beltagi HS, Kesba HH, Abdel-Alim AI, Al-Sayed AA (2011) Effect of root-knot nematode and two species of crown on antioxidant activity of grape leaves. Afr J Biotechnol 10(57):12202–12210

    CAS  Google Scholar 

  • El-Beltagi HS, Farahat AA, Alsayed AA, Mahfoud NA (2012) Response of antioxidant substances and enzymes activities as a defense mechanism against root-knot nematode infection. Not Bot Hort Agrobot Cluj 40(1):132–142

    CAS  Google Scholar 

  • El-Beltagi HS, Ahmed OK, Hegazy AE (2015) Molecular role of nitric oxide in secondary products production in Ginkgo biloba cell suspension culture. Not Bot Hort Agrobo Cluj 43(1):12–18

    Article  CAS  Google Scholar 

  • El-Beltagi HS, Ahmed OK, Hegazy AE (2016) Protective effect of nitric oxide on high temperature induced oxidative stress in wheat (Triticum aestivum) callus culture. Not Sci Biol 8(2):192–198

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Farkas GL, Kiraly Z (1962) Role of phenolic compounds in the physiology of plant diseases and disease resistance. J Phytopathol 44:105–150

    Article  CAS  Google Scholar 

  • Ferrer MA, Ros-Barcelo A (1999) Differential effects of nitric oxide on peroxidase and H2O2 production by the xylem of Zinnia elegans. Plant Cell Environ 22:891–897

    Article  CAS  Google Scholar 

  • Goodman RN, Kiraly E, Zaitlin M (1967) The biochemistry and physiology of infections in plant diseases. Van Nostrand Company, WC, Princeton-New Yersey

    Google Scholar 

  • Guo P, Cao Y, Li Z, Zhao B (2004) Role of an endogenous nitric oxide burst in the resistance of wheat to stripe rust. Plant Cell Environ 27:473–477

    Article  CAS  Google Scholar 

  • Hückelhoven R, Dechert C, Kogel KH (2003) Over expression of barley BAX inhibitor 1induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. PNAS 100:5555–5560

    Article  PubMed  PubMed Central  Google Scholar 

  • Huie RE, Padmaja S (1993) Reaction of NO with. Free Radic Res Commun 18:195–199

    Article  CAS  PubMed  Google Scholar 

  • Hung K‑T, Chang C‑J, Kao C‑H (2002) Paraquat toxicity is reduced by nitric oxide in rice leaves. J Plant Physiol 159:159–166

    Article  CAS  Google Scholar 

  • Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D (1997) Elicitor-stimulated ion sfluxes and from oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 94:4800–4805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keshavarz-Tohid V, Taheri P, Taghavi SM, Tarighi S (2016) The role of nitric oxide in basal and induced resistance in relation with hydrogen peroxide and antioxidant enzymes. J Plant Physiol 199:29–38

    Article  CAS  PubMed  Google Scholar 

  • Kobeasy MI, El-Beltagi HS, El-Shazly MA, Khattab EAH (2011) Induction of resistance in Arachis hypogaea L. against Peanut Mottle Virus by nitric oxide and salicylic acid. Physiol Mol Plant Pathol 76:112–118

    Article  CAS  Google Scholar 

  • Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiol 155:780–790

    Article  CAS  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: The versatility of an extensive signal molecule. Annu Rev Plant Physiol 54:109–136

    CAS  Google Scholar 

  • Mackernessa SAH, John CF, Jordan B, Tomas B (2001) Early signaling components in ultraviolet-B responses: Distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489:237–242

    Article  Google Scholar 

  • Małolepsza U, Rózalska S (2005) Nitric oxide and hydrogen peroxide in tomato resistance. Plant Physiol Biochem 43:623–635

    Article  PubMed  Google Scholar 

  • Murphy LD, Herzog CE, Rudick JB (1990) Use of the polymerase chain reaction in the quantitation of mdr-1 gene expression. Biochemistry 29:10351–10356

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Ng T, Gao W, Li L, Niu SM, Zhao L, Liu J, Shi LS, Fu M, Liu F (2005) NRC Canada Rose (Rosa rugosa)-flower extract increases the activities of antioxidant enzymes and their gene expression and reduces lipid peroxidation. Biochem Cell Biol 83:78–85

    Article  CAS  PubMed  Google Scholar 

  • Ochoa-Alejo N, Gomez-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

    Article  CAS  Google Scholar 

  • Orozco ML, Cárdenas CAR (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol 130:487–493

    Article  Google Scholar 

  • Palavan-Unsal N, Arisan D (2009) Nitric oxide signaling in plants. Bot Rev 75:203–229

    Article  Google Scholar 

  • Qiao W, Fan L (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50(10):1238–1246

    Article  CAS  PubMed  Google Scholar 

  • Sambrook JM, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathol 97:523–531

    Article  CAS  Google Scholar 

  • Shehab GG, Kansowa OA, El-Beltagi HS (2010) Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.). Not Bot Hort Agrobot Cluj 38(1):139–148

    CAS  Google Scholar 

  • Silber R, Farber M, Papopoulos E, Nervla D, Liebes L, Bruch M, Bron R (1992) Glutathione depletion in chronic lymphocytic leukemia b‑lymphocytes. Blood 80:2038–2040

    CAS  PubMed  Google Scholar 

  • Song F, Goodman RM (2001) Activity of nitric oxide is dependent on, but is partially required for function of salicylic acid in the signaling pathway in tobacco systemic acquired resistance. Mol Plant Microbe Interact 14:1458–1462

    Article  CAS  PubMed  Google Scholar 

  • Tamir S, Lewis RS, De-Rojas WT, Deen WM, Wishnok JS, Tannenbaum SR (1993) The influence of delivery rate on the chemistry and biological effects of nitric oxide. Chem Res Toxicol 6:895–899

    Article  CAS  PubMed  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Luo Z, Du R (2015) Nitric oxide delays chlorophyll degradation and enhances antioxidant activity in banana fruits after cold storage. Acta Physiol Plant 37:74

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB (1993) Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA 90:9813–9817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu LJ, Lan WZ, Qin WM, Xu HB (2001) Effects of salicylic acid on fungal elicitor-induced membrane-lipid peroxidation and taxol production in cell suspension cultures of Taxus chinensis. Process Biochem 37:477–482

    Article  Google Scholar 

  • Zhang C, Czymmek KJ, Shapiro AD (2003) Nitric oxide does not trigger early programmed cell death events but may contribute to cell-to-cell signaling governing progression of the Arabidopsis hypersensitive response. Mol Plant Microbe Interact 16:962–972

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, He J, Wang X, Zhang L (2008) Nitric oxide protects against polyethylene glycol induced oxidative damage in two ecotypes of reed suspension cultures. J Plant Physiol 165:182–191

    Article  CAS  PubMed  Google Scholar 

  • Zieslin N, Ben-Zaken R (1993) Peroxidase activity and presence of phenolic substances in peduncles of rose flowers. Plant Physiol Biochem 31:333–339

    CAS  Google Scholar 

Download references

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Correspondence to Hossam S. El-Beltagi.

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H.S. El-Beltagi, O.K. Ahmed and G.M.G. Shehab declare that they have no competing interests.

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El-Beltagi, H.S., Ahmed, O.K. & Shehab, G.M.G. Nitric Oxide Treatment and Induced Genes Role Against Phytophthora infestans in Potato. Gesunde Pflanzen 69, 171–183 (2017). https://doi.org/10.1007/s10343-017-0402-z

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