Advertisement

Plant Abiotic Stress: Function of Nitric Oxide and Hydrogen Peroxide

  • Małgorzata JanickaEmail author
  • Małgorzata Reda
  • Natalia Napieraj
  • Katarzyna Kabała
Chapter

Abstract

The negative effect of various environmental stresses is partially due to the generation of reactive oxygen species (ROS). ROS were originally considered to be detrimental to cells. However, it is now recognized that hydrogen peroxide functions as a trigger for induction of many genes encoding enzymes involved in cellular protection under stress. In a number of abiotic responses, NO generation occurs in parallel with H2O2, and both molecules can act synergistically and/or independently. Studies have shown that NO and H2O2 function as stress signals in plants, mediating a range of resistance mechanisms. The main place of the signal perception of worsening environmental conditions is the plasma membrane. On the other hand, one of the major proteins of the plant cell membrane is the plasma membrane H+-ATPase (PM H+-ATPase), a key enzyme in adaptation of plants to abiotic stresses. In plants exposed to different abiotic stresses, e.g., salinity, heavy metals, and low or high temperature, an increase in permeability related to membrane damage is observed. Maintaining ionic balance and replenishing the loss of essential substances are important issues. Support of active transport of ions through the plasma membrane requires increased generation of an electrochemical proton gradient by PM H+-ATPase, which results in a proton-motive force used by active transporters for assimilation of various nutrients, as well as for releasing toxic ions from cells. NO and H2O2 are important elements for understanding the mechanisms of PM H+-ATPase modification at both genetic and posttranslational level. Nowadays the role of NO and H2O2 as well as the signal cascades by which signaling molecules participate in plant responses to changing environmental conditions is under intensive study.

Keywords

Abiotic stress NO H2O2 Plasma membrane H+-ATPase 

References

  1. Ahn SJ, Yang IJ, Chung GC, Cho BH (1999) Inducible expression of plasma membrane H+-ATPase in the roots of figleaf gourd plants under chilling root temperature. Physiol Plant 106:35–40CrossRefGoogle Scholar
  2. Alvarez I, Tomaro LM, Bernavides PM (2003) Changes in polyamines, proline and ethylene in sunflower calluses treated with NaCl. Plant Cell Tissue Organ Cult 74:51–59CrossRefGoogle Scholar
  3. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationship in green cells. Physiol Plant 100:224–233CrossRefGoogle Scholar
  4. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620PubMedCrossRefPubMedCentralGoogle Scholar
  5. Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radic Res 50:291–303PubMedCrossRefPubMedCentralGoogle Scholar
  6. Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 13:15193–15208PubMedPubMedCentralCrossRefGoogle Scholar
  7. Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533PubMedCrossRefPubMedCentralGoogle Scholar
  8. Astolfi S, Zuchi S, Chiani A, Passera C (2003) In vivo and in vitro effects of cadmium on H+-ATPase activity of plasma membrane vesicles from oat (Avena sativa L.) roots. J Plant Physiol 160:387–393PubMedCrossRefPubMedCentralGoogle Scholar
  9. Astolfi S, Zuchi S, Passera C (2005) Effect of cadmium on H+-ATPase activity of plasma memebrane vesicles isolated from roots of different S-supplied maize (Zea mays L.) plants. Plant Sci 169:361–368CrossRefGoogle Scholar
  10. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a tree component system. J Exp Bot 53:1367–1137PubMedPubMedCentralGoogle Scholar
  11. Breckle SW, Kahle H (1991) Effects of toxic heavy metals (Cd, Pb) on growth and mineral nutrition on beech (Fagus sylvatica L). Plant Ecol 101:43–53CrossRefGoogle Scholar
  12. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145:1714–1725PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chinnusamy V, Jagendorf A, Zhu J (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448CrossRefGoogle Scholar
  14. Chinnusamy V, Zhu J, Zhu J (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–56CrossRefGoogle Scholar
  15. Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insight into cadmium sensing. Front Plant Sci 5:245PubMedPubMedCentralGoogle Scholar
  16. Clarke D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1380–1384CrossRefGoogle Scholar
  17. Corpas FJ, Leterrier M, Valderrema R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611PubMedCrossRefPubMedCentralGoogle Scholar
  18. Corpas FJ, Palma JM, del Rio LA, Barroso JB (2009) Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14PubMedCrossRefPubMedCentralGoogle Scholar
  19. del Rio LA, Corpas FJ, Sandalio LM (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81PubMedCrossRefPubMedCentralGoogle Scholar
  20. Demidchik V, Sokolik A, Yurin V (1997) The effect of Cu2+ ion transport systems of the plant cell plasmalemma. Plant Physiol 114:1313–1325PubMedPubMedCentralCrossRefGoogle Scholar
  21. Devi S, Prasad M (1999) Membrane lipid alterations in heavy metal exposed plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. From molecules to ecosystems. Springer, Berlin, pp 99–116CrossRefGoogle Scholar
  22. Domingos P, Pardo AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520PubMedCrossRefGoogle Scholar
  23. Egbichi I, Keyster M, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. South Afr J Bot 90:131–136CrossRefGoogle Scholar
  24. Eick M, Stöhr C (2012) Denitrification by plant roots? New aspects of plant plasma membrane-bound nitrate reductase. Protoplasma 249:909–918PubMedCrossRefPubMedCentralGoogle Scholar
  25. Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA (2016) When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front Plant Sci 7:471PubMedPubMedCentralCrossRefGoogle Scholar
  26. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  27. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–890PubMedCrossRefPubMedCentralGoogle Scholar
  28. Fuglsang A, Tulinius G, Ciu N, Palmgren M (2006) Protein phosphatases 2A scaffolding subunit A interacts with plasma membrane H+-ATPase C-terminus in the same region as 14-3-3 protein. Physiol Plant 128:334–340CrossRefGoogle Scholar
  29. Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261PubMedCrossRefPubMedCentralGoogle Scholar
  30. Gong M, Li YJ, Chen SZ (2002) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496CrossRefGoogle Scholar
  31. Groβ F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419Google Scholar
  32. Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11:537–543PubMedCrossRefGoogle Scholar
  33. Guy C (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223CrossRefGoogle Scholar
  34. Hancock JT (2012) NO synthase? Generation of nitric oxide in plants. Period Biol 114:19–24Google Scholar
  35. Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:37Google Scholar
  36. Howlett NG, Avery SV (1997) Relationship between cadmium sensitivity and degree of plasma membrane fatty acid unsaturation in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 48:539–545PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hu X, Zhang A, Zhang J, Jiang M (2006) Abscisic acid is a key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495PubMedCrossRefPubMedCentralGoogle Scholar
  39. Jakubowska D, Janicka-Russak M, Kabała K, Migocka M, Reda M (2015) Modification of plasma membrane NADPH oxidase activity in cucumber seedling roots in response to cadmium stress. Plant Sci 234:50–59PubMedCrossRefPubMedCentralGoogle Scholar
  40. Janicka M, Reda M, Czyżewska K, Kabała K (2018) Involvement of signalling molecules NO, H2O2 and H2S in modification of plasma membrane proton pump in cucumber roots subjected to salt or low temperature stress. Funct Plant Biol 45:428–439CrossRefGoogle Scholar
  41. Janicka-Russak M (2011) Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. In: Shanker A, Venkateswarlu B (eds) Abiotic stress response in plants- physiological, biochemical and genetic perspectives. InTech, Rijeka, pp 197–218Google Scholar
  42. Janicka-Russak M, Kabała K, Burzyński M, Kłobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728PubMedPubMedCentralCrossRefGoogle Scholar
  43. Janicka-Russak M, Kabała K (2012) Abscisic acid and hydrogen peroxide induce modification of plasma membrane H+-ATPase from Cucumis sativus L. roots under heat shock. J Plant Physiol 1969:1607–1614CrossRefGoogle Scholar
  44. Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2012a) Response of plasma membrane H+-ATPase to low temperature in cucumber roots. J Plant Res 125:291–300PubMedCrossRefGoogle Scholar
  45. Janicka-Russak M, Kabała K, Burzyński M (2012b) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142PubMedPubMedCentralCrossRefGoogle Scholar
  46. Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2013) Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress. J Plant Physiol 170:915–922PubMedCrossRefPubMedCentralGoogle Scholar
  47. Janicka-Russak M, Kłobus G (2007) Modification of plasma membrane and vacuolar H+-ATPase in response to NaCl and ABA. J Plant Physiol 164:295–302PubMedCrossRefPubMedCentralGoogle Scholar
  48. Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255PubMedPubMedCentralCrossRefGoogle Scholar
  49. Jiang M, Zhang J (2002) Involvement of plasma membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215:1022–1030PubMedCrossRefPubMedCentralGoogle Scholar
  50. Johnston MK, Jacob NP, Brodl MR (2007) Heat shock-induced changes in lipid and protein metabolism in the endoplasmic reticulum of barley aleurone layers. Plant Cell Physiol 48:31–41PubMedCrossRefGoogle Scholar
  51. Jones HG, Jones MB (1989) Introduction: some terminology and common mechanisms. In: Jones HG, Flowers TJ, Jones MB (eds) Plants under stress. Cambridge University Press, Cambridge, pp 1–10CrossRefGoogle Scholar
  52. Kabała K, Janicka-Russak M (2012) Na+/H+ antiport activity in plasma membrane and tonoplast vesicles isolated from NaCl treated cucumber roots. Biol Plant 56:377–382CrossRefGoogle Scholar
  53. Kabała K, Janicka-Russak M, Burzyński M, Kłobus G (2008) Comparison of heavy metal effect on the proton pumps of plasma membrane and tonoplast in cucumber root cells. J Plant Physiol 165:278–288PubMedCrossRefPubMedCentralGoogle Scholar
  54. Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud J, Boutry M (2005) Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins convert a dimer into a hexamer. Proc Natl Acad Sci U S A 102:11675–11680PubMedPubMedCentralCrossRefGoogle Scholar
  55. Kasamo K (2003) Regulation of plasma membrane H+-ATPase activity by the membrane environment. J Plant Res 116:517–523PubMedCrossRefPubMedCentralGoogle Scholar
  56. Kłobus G, Janicka-Russak M (2004) Modulation by cytosolic components of proton pump activities in plasma membrane and tonoplast from Cucumis sativus roots during salt stress. Physiol Plant 121:84–92PubMedCrossRefPubMedCentralGoogle Scholar
  57. Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kolbert Z, Ortega L, Erdei L (2010) Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots. J Plant Physiol 167:77–80PubMedCrossRefPubMedCentralGoogle Scholar
  59. Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signaling during chilling and cold acclimation in plants. Physiol Plant 113:158–164PubMedCrossRefPubMedCentralGoogle Scholar
  60. Königshofer H, Tromballa HW, Löppert HG (2008) Early events in signaling high temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ 31:1771–1780PubMedCrossRefPubMedCentralGoogle Scholar
  61. Krishna P, Sacco M, Cherutti JF, Hill S (1995) Cold-induced accumulation of hsp-90 transcripts in Brassica napus. Plant Physiol 107:915–923PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kubiś J (2003) Polyamines and “scavenging system”: influence of exogenous spermidine on catalase and guaiacol peroxidase activities, and free polyamines level in barley leaves under water deficit. Acta Physiol Plant 25:337–343CrossRefGoogle Scholar
  63. Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328PubMedCrossRefPubMedCentralGoogle Scholar
  64. Larkindale J, Huang B (2004) Changes of lipid composition and saturation level in leaves and roots for heat-stress and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environ Exp Bot 51:57–67CrossRefGoogle Scholar
  65. Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene and salicylic acid. Plant Physiol 128:682–695PubMedPubMedCentralCrossRefGoogle Scholar
  66. Li W, Wei Z, Qiao Z, Wu Z, Cheng L, Wang Y (2013) Proteomics analysis of alfalfa response to heat stress. PLoS One 8:82725CrossRefGoogle Scholar
  67. Liu A, Fan J, Gitau MM, Chen L, Fu J (2016) Nitric oxide involvement in Bermuda grass response to salt stress. J Amer Soc Hort Sci 141:425–443CrossRefGoogle Scholar
  68. Lopez-Pérez L, Martínez Ballesta M, Maurel C, Carvajal M (2009) Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry 70:492–500PubMedCrossRefPubMedCentralGoogle Scholar
  69. Mahajan S, Tuteja N (2005) Cold, salinity and drought stress: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefPubMedCentralGoogle Scholar
  70. Martz F, Sutinen M, Kiviniemi S, Palta J (2006) Changes in freezing tolerance, plasma membrane H+-ATPase activity and fatty acid composition in Pinus resinosa needles during cold acclimation and de-acclimation. Tree Physiol 26:783–790PubMedCrossRefPubMedCentralGoogle Scholar
  71. Mata-Pérez C, Begara-Morales JC, Chaki M, Sánchez-Calvo B, Valderrama R, Padilla MN, Corpas FJ, Barroso JB (2016) Protein tyrosine nitration during development and abiotic stress response in plants. Front Plant Sci 7:1699PubMedPubMedCentralCrossRefGoogle Scholar
  72. Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants. Ann Bot 98:279–288PubMedPubMedCentralCrossRefGoogle Scholar
  73. Moschou PN, Paschalidis AK, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724PubMedPubMedCentralCrossRefGoogle Scholar
  74. Murphy A, Taiz L (1997) Correlation between potassium efflux and copper sensitivity in 10 Arabidopsis ecotypes. New Phytol 136:211–222CrossRefGoogle Scholar
  75. Murphy A, Eisinger WR, Shaff JE, Kochian LV, Taiz L (1999) Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiol 121:1375–1382PubMedPubMedCentralCrossRefGoogle Scholar
  76. Neil S, Barros R, Bright J, Desikan R, Hancock J, Harrison J et al (2008) Nitroc oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176CrossRefGoogle Scholar
  77. Neill SJ, Desikan D, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1242PubMedCrossRefGoogle Scholar
  78. Niu X, Narasimhan M, Salzman R (1993) NaCl regulation of plasma membrane H+-ATPase gene expression in Glycophyte and Halophyte. Plant Physiol 103:712–718CrossRefGoogle Scholar
  79. Oufattole M, Arango M, Boutry M (2000) Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma membrane H+-ATPase, and one which is induced by mechanical stress. Planta 210:715–722PubMedCrossRefPubMedCentralGoogle Scholar
  80. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefPubMedCentralGoogle Scholar
  81. Pál M, Horwáth E, Janda T, Páldi E, Szalai G (2005) Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physiol Plant 125:356–364CrossRefGoogle Scholar
  82. Paschalidis AK, Toumi I, Moschou NP, Kalliopi A, Roubelakis-Angelakis A (2010) ABA-dependent amine oxidases-derived H2O2 affects stomata conductance. Plant Signal Behav 5:1153–1156CrossRefGoogle Scholar
  83. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 17:731–734CrossRefGoogle Scholar
  84. Pérez de Juan J, Irigoyen J, Sánchez-Díaz M (1997) Chilling of drought-hardened and non-hardened plants of different chilling-sensitive maize lines changes in water relations and ABA contents. Plant Sci 122:71–79CrossRefGoogle Scholar
  85. Perez-Prat E, Narasimhan M, Niu X, Botella M, Bressan R, Valupesta V, Hasegawa PM, Binzel ML (1994) Growth cycle stage dependent NaCl induction of plasma membrane H+-ATPase mRNA accumulation in de-adapted tobacco cells. Plant Cell Environ 17:327–333CrossRefGoogle Scholar
  86. Piotrovskii MS, Shevyreva TA, Zhestkova IM, Trofimova MS (2011) Activation of plasmalemmal NADPH oxidase in etiolated maize seedlings exposed to chilling temperatures. Russ J Plant Physiol 58:234–242CrossRefGoogle Scholar
  87. Polisensky DH, Braam J (1996) Cold shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol 111:1271–1279PubMedPubMedCentralCrossRefGoogle Scholar
  88. Qiao W, Faan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246PubMedCrossRefPubMedCentralGoogle Scholar
  89. Qiao W, Li C, Fan LM (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93CrossRefGoogle Scholar
  90. Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–18PubMedCrossRefGoogle Scholar
  91. Queval G, Hager J, Gakière B, Noctor G (2008) Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in quantitative assays of leaf extracts. J Exp Bot 59:135–146PubMedCrossRefPubMedCentralGoogle Scholar
  92. Reda M, Golicka A, Kabała K, Janicka M (2018) Involvement of NR and PM-NR in NO biosynthesis in cucumber plants subjected to salt stress. Plant Sci 267:55–64PubMedCrossRefPubMedCentralGoogle Scholar
  93. Robertson AJ, Ishikawa M, Gusta LV, MacKenzie SL (1994) Abscisic acid induced heat tolerance in Bromus inermis lees cell suspension cultures. Plant Physiol 105:181–190PubMedPubMedCentralCrossRefGoogle Scholar
  94. Romero-Puertas MC, Rodríguez-Serrano M, Sandalio ML (2013) Protein S-nitrosylation in plants under abiotic stress: an overview. Front Plant Sci 4:373PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340PubMedPubMedCentralCrossRefGoogle Scholar
  96. Sahay S, Gupta M (2017) An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67:39–52PubMedCrossRefGoogle Scholar
  97. Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127:1–9CrossRefGoogle Scholar
  98. Sahu BB, Shaw BP (2009) Salt-inducible isoform of plasma membrane H+-ATPase gene in rice remains constitutively expressed in natural halophyte, Suaeda maritima. J Plant Physiol 166:1077–1089PubMedCrossRefPubMedCentralGoogle Scholar
  99. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668PubMedCrossRefPubMedCentralGoogle Scholar
  100. Sami F, Faizan M, Faraz A, Siddiqui F, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38PubMedCrossRefPubMedCentralGoogle Scholar
  101. Santolini J, André F, Jeandroz S, Wendehenne D (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38PubMedCrossRefGoogle Scholar
  102. Serrano R (1989) Structure and function of plasma membrane ATPase. Annu Rev Plant Physiol Plant Mol Biol 40:61–94CrossRefGoogle Scholar
  103. Shapiro AD (2005) Nitric oxide signaling in plants. Vitam Horm 72:339–398PubMedCrossRefPubMedCentralGoogle Scholar
  104. Siddiqui MH, Al-Whaibi MH, Basalah MO (2010) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455PubMedCrossRefPubMedCentralGoogle Scholar
  105. Silva P, Geros H (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signal Behav 4:718–726PubMedPubMedCentralCrossRefGoogle Scholar
  106. Stöhr C, Stremlau S (2006) Formation and possible roles of nitric oxide in plant roots. J Exp Bot 57:463–470PubMedCrossRefPubMedCentralGoogle Scholar
  107. Stöhr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293–2303PubMedCrossRefPubMedCentralGoogle Scholar
  108. Sun C, Lu L, Liu L, Liu W, Yu Y, Liu X, Hu Y, Jin C, Lin X (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250PubMedCrossRefPubMedCentralGoogle Scholar
  109. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 26:45–51CrossRefGoogle Scholar
  110. Svennelid F, Olsson A, Piotrowski M, Rosenquist M, Ottman C, Larsson C, Oecking C, Sommarin M (1999) Phosphorylation of Thr-948 at the C-terminus of the plasma membrane H+-ATPase creates a binding site for regulatory 14-3-3 protein. Plant Cell 11:2379–2391PubMedPubMedCentralGoogle Scholar
  111. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–805PubMedCrossRefPubMedCentralGoogle Scholar
  112. Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteom 71:391–411CrossRefGoogle Scholar
  113. Tischner R, Planchet E, Kaiser WM (2004) Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett 576:151–155PubMedCrossRefPubMedCentralGoogle Scholar
  114. Toumi I, Moschou PN, Paschalidis KA, Bouamama B, Ben Salem-Fnayou A, Ghorbel AW, Mliki A, Roubelakis-Angelakis KA (2010) Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol 167:519–525PubMedCrossRefPubMedCentralGoogle Scholar
  115. Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523CrossRefGoogle Scholar
  116. Van Gestelen P, Asard H, Caubergs RJ (1997) Solubilization and separation of a plant plasma membrane NADPH-superoxide (O. 2 )-synthase from other NAD(P)H-oxidoreductases. Plant Physiol 115:543–550PubMedPubMedCentralCrossRefGoogle Scholar
  117. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, van Montagu M, Zabeau M, Inze D, van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci U S A 100:16113–16118PubMedPubMedCentralCrossRefGoogle Scholar
  118. Vera-Estrella R, Barkla B, Higgins V, Blumwald E (1994) Plant defense response to fungal pathogens (activation of host-plasma membrane H+-ATPase by elicitor-induced enzyme dephosphorylation). Plant Physiol 104:209–215PubMedPubMedCentralCrossRefGoogle Scholar
  119. Volkov RA, Panchuk II, Mullineaux PM, Schoffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746PubMedCrossRefPubMedCentralGoogle Scholar
  120. Waie B, Rajam M (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734CrossRefGoogle Scholar
  121. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trend Plant Sci 9:244–253CrossRefGoogle Scholar
  122. Wang X, Ma Y, Huang C, Li J, Wan Q, Bi Y (2008) Involvement of glucose-6-phosphate dehydrogenase in reduced glutathione maintenance and hydrogen peroxide signal under salt stress. Plant Signal Behav 3:394–395PubMedPubMedCentralCrossRefGoogle Scholar
  123. Weidert ER, Schoenborn SO, Cantu-Medellin N, Choughule KV, Jones JP, Kelly EE (2014) Inhibition of xanthine oxidase by the aldehyde oxidase inhibitor raloxifene; implications for identifying molybdenum nitrite reductases. Nitric Oxide 37:41–45PubMedPubMedCentralCrossRefGoogle Scholar
  124. Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765PubMedCrossRefPubMedCentralGoogle Scholar
  125. Xiong L, Zhu J (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166PubMedCrossRefPubMedCentralGoogle Scholar
  126. Yang Y, Xu S, An L, Chen N (2007) NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J Plant Physiol 164:1429–1435PubMedCrossRefPubMedCentralGoogle Scholar
  127. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156PubMedCrossRefGoogle Scholar
  128. Yun BW, Feechan A, Yin M, Saidi NB, le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268PubMedCrossRefGoogle Scholar
  129. Zhang JZ, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton pump and Na+/H+ antiport in tonoplast. Planta 224:545–555PubMedCrossRefPubMedCentralGoogle Scholar
  130. Zhang F, Wang Y, Yang Y, Wu H, Wang D, Liu J (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785PubMedCrossRefPubMedCentralGoogle Scholar
  131. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:1–5CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Małgorzata Janicka
    • 1
    Email author
  • Małgorzata Reda
    • 1
  • Natalia Napieraj
    • 1
  • Katarzyna Kabała
    • 1
  1. 1.Department of Plant Molecular Physiology, Institute of Experimental BiologyUniversity of WrocławWrocławPoland

Personalised recommendations