Investigation of The Roles of Hydrogen Peroxide and NADPH Oxidase in The Regulation of Polyamine Metabolism in Maize Plants under Drought Stress Conditions

Yıl 2022, Cilt Early View, Sayı , 40 - 40, 04.12.2022

Mehmet DEMİRALAY Aykut SAĞLAM Fuat YETİŞSİN Asım KADIOĞLU

https://doi.org/10.15832/ankutbd.861008

Öz

The relationship between hydrogen peroxide and polyamine metabolism and the role of NADPH oxidase (NOX) in this relationship under drought conditions has not yet been clarified. To reveal the relationship, expression levels of the genes in polyamine metabolism, such as arginine decarboxylase (ADC), agmatine aminohydrolase (AIH), spermidine synthase (SPDS), S-adenosyl methionine decarboxylase (SAMDC), diamine oxidase (DAO) and polyamine oxidase (PAO) were determined by RT PCR under drought stress combined with exogenous hydrogen peroxide (H2O2) and diphenyleneiodonium chloride (DPI) treatments in maize seedlings. Also, some basic stress parameters (leaf water potential, lipid peroxidation), polyamine levels (putrescine, spermidine, and spermine), and gene expression of NOX were measured under drought stress. Exogenous H2O2 induced polyamine contents by up-regulating polyamine-synthesizing genes and downregulating polyamine oxidizing genes. Moreover, when the NOX enzyme was inhibited by DPI, the polyamine metabolic pathway tended toward degradation rather than production. Exogenous H2O2 regulated polyamine metabolism to promote their synthesis, and NOX had a key role in this regulation.

Anahtar Kelimeler

Diphenyleneiodonium chloride, Drought stress, Hydrogen peroxide, NAPH oxidase, Polyamine metabolism

Öz

Kaynakça

• Abass M S & Mohamed H I (2011). Alleviation of adverse effects of drought stress on common bean (Phaseolus vulgaris L.) by exogenous application of hydrogen peroxide. Bangladesh Journal of Botany 40: 75-83
• Aebi H E (1983). Catalase. In: Bergmeyer H U (Ed.), Methods of Enzymatic Analysis, Verlag Chemie, Germany, pp. 273-286
• Akyol T Y, Yılmaz O, Uzilday B, Özgür Uzilday R & Türkan I (2020). Plant response to salinity: an analysis of ROS formation, signaling, and antioxidant defense. Turkish Journal of Botany 44: 1-13
• Alcazar R, Cuevas J C, Patron M, Altabella T & Tiburcio A F (2006a). Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiologia Plantarum 128: 448-455
• Alcazar R, Marco F, Cuevas J C, Patron M, Ferrando A, Carrasco P, Tiburcio A F & Altabella T (2006b). Involvement of polyamines in plant response to abiotic stress. Biotechnology Letters 28: 1867-1876
• Alcazar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrian M, Tiburcio A F & Altabella T (2010a). Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants overexpressing the homologous Arginine decarboxylase 2 gene. Plant Physiology and Biochemistry 48: 547-552
• Alcazar R, Altabella T, Marco F, Bortolitto C, Reymond M, Koncz C, Carasso P & Tiburcio A F (2010b). Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta 231: 1237-1249
• Alcazar R, Bitrian M, Bartels D, Koncz C, Altabella T & Tiburcio A F (2011). Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signaling and Behavior 6: 243-250
• Andronis A E, Moschou P N, Toumi I & Roubelakis-Angelakis K A (2014). Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana. Frontiers in Plant Science 5: 132
• Angelini R, Cona A, Federico R, Fincato P, Tavladoraki P & Tisi A (2010). Plant amine oxidases “on the move”: an update. Plant Physiology and Biochemistry 48: 560-564
• Bailey-Serres J & Mittler R (2006). The roles of reactive oxygen species in plant cells. Plant Physiology 141: 311
• Beauchamp C & Fridovich I (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44: 276-287
• Bradford M M (1976). Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248–254
• Cakmak I & Marschner H (1988). Zinc-dependent changes in ESR signals, NADPH oxidase and plasma membrane permeability in cotton roots. Physiologi Plantarum 73: 182-186
• Capell T, Bassie L & Christou P (2004). Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences of the United States of America 101: 9909–9914
• Chaudiere J & Ferrari-Iliou R (1999). Intracellular antioxidants from chemical to biochemical mechanisms. Food and Chemical Toxicology 37: 949-962
• Cohen S S (1998). A Guide to The Polyamines. Oxford University Press, New York Cona A, Rea G, Angelini R, Federico R & Tavladoraki P (2006a). Functions of amine oxidases in plant development and defence. Trends in Plant Science 11: 80-88
• Cona A, Rea G, Botta M, Corelli F, Federico R & Angelini R (2006b). Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays. Journal of Experimental Botany 57: 2277–2289
• Cruz de Carvalho MH (2008). Drought stress and reactive oxygen species. Plant Signaling and Behavior 3: 156-165
• Das K & Roychoudhury A (2014). Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2: 53
• Do, P T, Drechsel O, Heyer A G, Hincha D K & Zuther E (2014). Changes in free polyamine levels, expression of polyamine biosynthesis genes and performance of rice cultivars under salt stress: A comparison with responses to drought. Frontiers in Plant Science 5: 182
• Dikalov S, Nazarewicz R, Panov A, Harrison D G & Dikalova A (2011). Crosstalk between mitochondrial ROS and NADPH oxidases in cardiovascular and degenerative diseases: Application of mitochondria-targeted antioxidants. Free Radical Biology and Medicine 51: 85-86
• Erdei L, Szegletes Z, Barabas K & Pestenacz A (1996). Responses in polyamine under osmotic and salt stress in sorghum and maize seedlings. Journal of Plant Physiology 147: 599-603
• Fincato P, Moschou P N, Spedaletti V, Tavazza R, Angelini R, Federico R, Roubelakis-Angelakis K A & Tavladoraki P (2011). Functional diversity inside the Arabidopsis polyamine oxidase gene family. Journal of Experimental Botany 62: 1155-1168
• Fincato P, Moschou P N, Ahou A, Angelini R, Roubelakis-Angelakis K A, Federico R & Tavladoraki P (2012). The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue and organ-specific expression pattern during seedling growth and flower development. Amino Acids 42: 831-841
• Galston A W, Kaur-Sawhney R, Altabella T & Tiburcio A F (1997). Plant polyamines in reproductive activity and response to abiotic stress. Botanica Acta 110: 197-207
• Gill S & Tuteja N (2010). Polyamines and abiotic stress tolerance in plants. Plant Signaling & Behavior 5: 26-33 Groppa M D & Benavides M P (2008). Polyamines and abiotic stress: Recent advances. Amino Acids 34: 35-45
• Guven F G (2013). Effect of alpha lipoic acid pre-treatment on drought tolerance in drought-sensitive and drought-resistant maize genotypes. Master thesis, Karadeniz Technical University, Turkey
• Hatmi S, Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Baillieul F, Eullaffroy P, Clément C, Ferchichi A & Aziz A (2015). Drought stress tolerance in grapevine involves activation of polyamine oxidation contributing to improved immune response and low susceptibility to Botrytis cinerea. Journal of Experimental Botany 66: 775-787
• He L, Gao Z & Li R (2009). Pretreatment of seed with H2O2 enhances drought tolerance of wheat (Triticum aestivum L.) seedlings. African Journal of Biotechnology 8: 6151-6157
• Heath R L & Packer L (1968). Photoperoxidation in isolated chloroplasts. I. kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125: 189-198
• Kusano T, Yamaguchi K, Berberich T & Takahashi Y (2007). The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signaling and Behavior 2: 251-252
• Kusano T, Berberich T, Tateda C & Takahashi Y (2008). Polyamines: Essential factors for growth and survival. Planta 228: 367-381 Kwak J M, Mori I C, Pei Z M, Leonhardt N, Torres M A, Dangl J L, Bloom R E, Bodde S, Jones J D G & Schroeder J I (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22: 2623-2633
• Li Z Y & Chen S Y (2000). Differential accumulation of the S-adenosylmethionine decarboxylase transcript in rice seedlings in response to salt and drought stresses. Theoretical and Applied Genetics 100: 782-788
• Liu Z J, Guo Y K & Bai J G (2010). Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. Journal of Plant Growth Regulation 29: 171-183
• Liu C, Atanasov K E, Tiburcio A F & Alcázar R (2019). The polyamine putrescine contributes to H2O2 and RbohD/F-dependent positive feedback loop in Arabidopsis PAMP-Triggered Immunity. Frontiers in Plant Science 10: 894
• Moschou P N, Delis I D, Paschalidis K A & Roubelakis-Angelakis K A (2008a). Transgenic tobacco plants overexpressing polyamine oxidase are not able to cope with oxidative burst generated by abiotic factors. Physiologia Plantarum 133: 140-156
• Moschou P N, Paschalidis K A & Roubelakis-Angelakis K A (2008b). Plant polyamine catabolism: The state of the art. Plant Signaling and Behavior 3: 1061-1066
• Munne-Bosch S, Jubany-Mari T & Alegre L (2001). Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant Cell and Environment 24: 1319-1327
• Papadakis A K & Roubelakis-Angelakis K A (2005). Polyamines inhibit NADPH oxidase-Mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase-generated hydrogen peroxide. Planta 220: 826-837
• Parida A K & Das A B (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60: 324-349
• Pitzschke A, Forzani C & Hirt H (2006). Reactive oxygen species signaling in plants. Antioxidants and Redox Signaling 8: 1757-1764
• Potocký M, Jones M A, Bezvoda R, Smirnoff N & Žárský V (2007). Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytologist 174: 742–51
• Rodríguez-Rojas A, Kim J J, Johnston P R, Makarova O, Eravci M, Weise C, Hengge R & Rolff J (2020). Non-lethal exposure to H2O2 boosts bacterial survival and evolvability against oxidative stress. PLoS Genetics, 16(3): e1008649
• Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann J W & Fluhr R (2004). Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16: 616-628
• Saglam A, Saruhan N, Terzi R & Kadioğlu A (2011). The relations between antioxidant enzymes and chlorophyll fluorescence parameters in common bean cultivars differing in sensitivity to drought stress. Russian Journal of Plant Physiology 58: 60-68
• Seo S Y, Kim Y J & Park K Y (2019). Increasing polyamine contents enhances the stress tolerance via reinforcement of antioxidative properties. Frontiers in Plant Science 10: 1331
• Sequera-Mutiozabal M, Antoniou C, Tiburcio A F, Alcázar R & Fotopoulos V (2017). Polyamines: Emerging hubs promoting drought and salt stress tolerance in plants. Current Molecular Biology Reports 3: 28–36
• Sharma P & Dubey R S (2005). Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regulation 46: 209–221
• Shaw B, Thomas T H & Cooke D T (2002). Responses of sugar beet (Beta vulgaris) to drought and nutrient deficiency stress. Plant Growth Regulation 37: 77-83
• Siddique M R B, Hamid A & Islam M S (2000). Drought stress effects on water relations of wheat. Botanical Bulletin of Academia Sinica 41: 35-39
• Suzuki N, Miller G, Salazar C, Mondal H A, Shulaev E, Cortes D F, Shuman J L, Luo X, Shah J, Schlauch K, Shulaev V & Mittler R (2013). Temporal-spatial interaction between reactive oxygen species and Abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25: 3553-3569
• Terzi R, Kadioglu A, Kalaycioglu E & Saglam A (2014). Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves. Journal of Plant Interactions 9: 559-565
• Torres M A, Jones J D G & Dangl J L (2005). Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 37: 1130-1134
• Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K & Shinozaki K (2004). Arabidopsis stress-inducible gene for Arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochemical and Biophysical Research Communications 313: 369-375
• Urbanek H, Kuzniak-Gebarowska E & Herka K (1991). Elicitation of defense responses in bean leaves by Botrytis cinerea polygalacturanase, Acta Physiologiae Plantarum 13: 43-50
• Velikova V, Yordanov I & Edreva A (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective roles of exogenous polyamines. Plant Science 151: 59-66
• Waszczak C, Carmody M & Kangasjärvi J (2018). Reactive oxygen species in plant signaling. Annual Review of Plant Biology 29: 209-236
• Wu J, Shang Z, Jiang X, Moschou P N, Sun W, Roubelakis-Angelakis K A & Zhang S (2010). Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca+2-permeable channels and pollen tube growth. Plant Journal 63: 1042-1053
• Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A & Kusano T (2006). The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Letters 580: 6783-6788 Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi, T, Michael, A J & Kusano T (2007). A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochemical and Biophysical Research Communications 352: 486-490