Advertisement

Plant Responses to Salinity Through an Antioxidative Metabolism and Proteomic Point of View

  • J. A. HernándezEmail author
  • G. Barba-Espín
  • M. J. Clemente-Moreno
  • P. Díaz-Vivancos
Chapter

Abstract

Salt stress is one of the most damaging abiotic stresses because most crop plants are susceptible to salinity in different degrees. According to Food and Agriculture Organization of the United Nations (FAO), about 800 million Ha of land are affected by salinity around the world. In addition to the known components of osmotic stress and ion toxicity, salt stress is also manifested as an oxidative stress with all of these factors contributing to its deleterious effects. Although salinity-induced oxidative stress has been widely described, the effect of salinity on the antioxidative system and/or ROS generation in specific cell compartments has been less studied.

In recent years, high-throughput proteomic techniques have provided new ways to explore the complex network of plant salinity response in order to identify key elements for stress tolerance acquisition. However, from an overview of the available information about plant salinity responses it can be concluded that only a small number of the salt-inducible genes reported in the literature have been identified at the protein level. Most of the salt-responsive proteins identified in these studies correspond to the categories of amino acid metabolism, energy regulation, detoxification and redox regulation.

The overexpression of genes encoding for different antioxidant enzymes is a common strategy to induce salt tolerance in crop plants. In this sense, the overexpression of H2O2-scavenging enzymes (APX, CAT), SOD, ASC-recycling enzymes or GSH-related enzymes resulted in increased salt tolerance in different plant species. In addition, some authors have used the co-expression of two or three genes encoding antioxidants to achieve salt tolerance in plants.

Keywords

Salt Stress Transgenic Tobacco Plant Salt Stress Condition Salt Stress Tolerance DHAR Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Acosta-Motos JR, Diaz-Vivancos P, Álvarez S, Fernández-García N, Sánchez-Blanco MJ, Hernández JA (2015a) NaCl-induced physiological and biochemical adaptative mechanisms in the ornamental Myrtus communis L. plants. J Plant Physiol 183:41–51PubMedCrossRefGoogle Scholar
  2. Acosta-Motos JR, Diaz-Vivancos P, Álvarez S, Fernández-García N, Sánchez-Blanco MJ, Hernández JA (2015b) Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L. plants for coping with NaCl stress and recovery. Planta 242:829–849PubMedCrossRefGoogle Scholar
  3. Aghaei K, Ehsanpour AA, Shah AH, Komatsu S (2009) Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 36:91–98PubMedCrossRefGoogle Scholar
  4. Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A (2007) A bacterial transgene for catalase protects translation of d1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol 145:258–265PubMedPubMedCentralCrossRefGoogle Scholar
  5. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  6. Ashraf M (2004) Some important physiological selection criteria for salt tolerance in plants. Flora 199:361–376CrossRefGoogle Scholar
  7. Azevedo-Neto AD, Pitsco JT, Eneas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and saltsensitive maize genotypes. Environ Exp Bot 56:87–94CrossRefGoogle Scholar
  8. Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004a) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121:231–238PubMedCrossRefGoogle Scholar
  9. Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004b) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928CrossRefGoogle Scholar
  10. Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X (2011) Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J Proteome Res 10:4349–4364PubMedCrossRefGoogle Scholar
  11. Bolu WH, Polle A (2004) Growth and stress reactions in roots and shoots of a salt-sensitive poplar species (Populus x canescens). Trop Ecol 45:161–171Google Scholar
  12. Chen J-H, Jiang H-W, Hsieh E-J, Chen H-Y, Chien C-T, Hsieh H-L, Lin T-P (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen Z, Pan YH, An LY, Yang WJ, Xu LG, Zhu C (2013) Heterologous expression of a halophilic archaeon manganese superoxide dismutase enhances salt tolerance in transgenic rice. Russ J Plant Physiol 60(3):359–366CrossRefGoogle Scholar
  14. Chitteti BR, Peng ZH (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6:1718–1727PubMedCrossRefGoogle Scholar
  15. Corpas FJ, Gomez M, Hernandez JA, del Rio LA (1993) Metabolism of activated oxygen in leaf peroxisomes from two Pisum sativun L. cultivars with different sensivity to sodium chloride. J Plant Physiol 141:160–165CrossRefGoogle Scholar
  16. Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2094PubMedPubMedCentralCrossRefGoogle Scholar
  17. Dani V, Simon WJ, Duranti M, Croy RR (2005) Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 5:737–745PubMedCrossRefGoogle Scholar
  18. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedCrossRefGoogle Scholar
  19. Diaz-Vivancos P, Barba-Espin G, Clemente-Moreno MJ, Hernández JA (2010) Characterization of the antioxidative system during the vegetative development of pea plants. Biol Plant 54:76–82Google Scholar
  20. Diaz-Vivancos P, Faize M, Barba-Espin G, Faize L, Petri C, Hernández JA, Burgos L (2013) Ectopic expression of cytosolic superoxide dismutase and ascorbate peroxidase leads to salt stress tolerance in transgenic plums. Plant Biotech J 11:976–985Google Scholar
  21. Ding S, Lu Q, Zhang Y, Yang Z, Wen X, Zhang L, Lu C (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol Biol 69:577–592PubMedCrossRefGoogle Scholar
  22. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in heath. Trends Plant Sci 5:193–198PubMedCrossRefGoogle Scholar
  23. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264PubMedCrossRefGoogle Scholar
  24. Eltelib HA, Fujikawa Y, Esaka M (2012) Overexpression of the acerola (Malpighia glabra) monodehydroascorbate reductase gene in transgenic tobacco plants results in increased ascorbate levels and enhanced tolerance to salt stress. S Afr J Bot 78:295–301CrossRefGoogle Scholar
  25. Faize M, Burgos L, Faize L, Piqueras A, Nicolás E, Barba-Espín G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernández JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought. J Exp Bot 62:2599–2613PubMedCrossRefGoogle Scholar
  26. Fernández-García N, Hernández M, Casado-Vela J, Bru R, Elortza F, Hedden P, Olmos E (2011) Changes to the proteome and targeted metabolites of xylem sap in Brassica oleracea in response to salt stress. Plant Cell Environ 34:821–836PubMedCrossRefGoogle Scholar
  27. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388CrossRefGoogle Scholar
  28. Gallie DR (2013) L-ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica 2013:24. Article ID 795964Google Scholar
  29. Gill T, Sreenivasulu Y, Kumar S, Ahuja PS (2010) Over-expression of Potentilla superoxide dismutase improves salt stress tolerance during germination and growth in Arabidopsis thaliana. J Plant Genet Transgenics 1:1–10Google Scholar
  30. Gómez JM, Hernández JA, Jiménez A, Del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radic Res 31:S11–S18PubMedCrossRefGoogle Scholar
  31. Gómez JM, Jiménez A, Olmos E, Sevilla F (2004) Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. J Exp Bot 55:119–130PubMedCrossRefGoogle Scholar
  32. Gueta-Dahan Y, Yaniv Z, Zilinskas B, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in Citrus. Planta 203:460–469Google Scholar
  33. Guo Y, Song Y (2009) Differential proteomic analysis of apoplastic proteins during initial phase of salt stress in rice. Plant Signal Behav 4:121–122PubMedPubMedCentralCrossRefGoogle Scholar
  34. Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford UniversityPress, LondonGoogle Scholar
  35. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  36. Hernández JA, Corpas FJ, Gómez M, Del Río LA, Sevilla F (1993) Salt induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Plant Physiol 89:103–110CrossRefGoogle Scholar
  37. Hernández JA, Olmos E, Corpas FJ, Sevilla F, Del Río LA (1995) Salt-induced oxidative stress in chloroplast of pea plants. Plant Sci 105:151–167CrossRefGoogle Scholar
  38. Hernández JA, Campillo A, Jiménez A, Alarcon JJ, Sevilla F (1999) Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol 141:241–251CrossRefGoogle Scholar
  39. Hernández JA, Jiménez A, Mullineaux PM, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  40. Hernández JA, Ferrer MA, Jiménez A, Ros-Barceló A, Sevilla F (2001) Antioxidant systems and O2.-/H2O2 production in the apoplast of Pisum sativum L. leaves: its relation with NaCl-induced necrotic lesions in minor veins. Plant Physiol 127:817–831PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hernandez J, Nistal DB, Labrador E (2002) Cold and salt stress regulates the expression and activity of a chickpea cytosolic Cu/Zn superoxide dismutase. Plant Sci 163:507–514Google Scholar
  42. Hoque MA, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165:813–824PubMedCrossRefGoogle Scholar
  43. Hu Y, Guo S, Li X, Ren X (2013) Comparative analysis of salt-responsive phosphoproteins in maize leaves using Ti(4+)--IMAC enrichment and ESI-Q-TOF MS. Electrophoresis 34:485–492PubMedCrossRefGoogle Scholar
  44. Ikbal FE, Hernández JA, Barba-Espín G, Koussa T, Aziz A, Faize M, Diaz-Vivancos P (2014) Enhanced salt-induced antioxidative responses involve a contribution of polyamine biosynthesis in grapevine plants. J Plant Physiol 171:779–788PubMedCrossRefGoogle Scholar
  45. Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607PubMedCrossRefGoogle Scholar
  46. Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea (Pisum sativum L.) leaves. Plant Physiol 114:275–284PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kim YS, Kim IS, Shin SY, Park TH, Park HM, Kim YH, Lee GS, Kang HG, Lee SH, Yoon HS (2014) Overexpression of dehydroascorbate reductase confers enhanced tolerance to salt stress in rice plants (Oryza sativa L. japonica). J Agron Crop Sci 200:444–456CrossRefGoogle Scholar
  48. Koffler BE, Luschin-Ebengreuth N, Zechmann B (2015) Compartment specific changes of the antioxidative status in Arabidopsis thaliana during salt stress. J Plant Biol 58:8–16CrossRefGoogle Scholar
  49. Kosová K, Prášil IT, Vítámvás P (2013) Protein contribution to plant salinity response and tolerance acquisition. Int J Mol Sci 14:6757–6789PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160:347–353PubMedCrossRefGoogle Scholar
  51. Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673PubMedCrossRefGoogle Scholar
  52. Lee Y-P, Kim S-H, Bang J-W, Lee H-S, Kwak S-S, Kwon S-Y (2007) Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Rep 26:591–598PubMedCrossRefGoogle Scholar
  53. Li Y-J, Hai R-L, Du X-H, Jiang X-N, Lu H (2009) Over-expression of a Populus peroxisomal ascorbate peroxidase (PpAPX) gene in tobacco plants enhances stress tolerance. Plant Breed 128:404–410CrossRefGoogle Scholar
  54. Li Q, Li Y, Li C, Yu X (2012) Enhanced ascorbic acid accumulation through overexpression of dehydroascorbate reductase confers tolerance to methyl viologen and salt stresses in tomato. Czech J Genet Plant Breed 48:74–86Google Scholar
  55. Light GG, Mahan JR, Roxas VP, Allen RD (2005) Transgenic cotton (Gossypium hirsutum L.) seedlings expressing a tobacco glutathione S -transferase fail to provide improved stress tolerance. Planta 222:346–354PubMedCrossRefGoogle Scholar
  56. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184Google Scholar
  57. Lu ZQ, Liu D, Liu SK (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917PubMedCrossRefGoogle Scholar
  58. Luo X, Wu J, Li Y, Nan Z, Guo X et al (2013) Synergistic effects of GhSOD1 and GhCAT1 overexpression in cotton chloroplasts on enhancing tolerance to methyl viologen and salt stresses. PLoS One 8(1):e54002PubMedPubMedCentralCrossRefGoogle Scholar
  59. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  60. Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 174:420–431CrossRefGoogle Scholar
  61. Meneguzzo S, Sgherri CLM, Navari-Izzo F, Izzo R (1998) Stromal and thylakoid-bound ascorbate peroxidase in NaCl-treated wheat. Physiol Plant 104:735–740CrossRefGoogle Scholar
  62. Miller G, Suzuki N, Ciftci-Yilmaz S, Mitller R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedCrossRefGoogle Scholar
  63. Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400PubMedCrossRefGoogle Scholar
  64. Mittova V, Tal M, Volokita M, Guy M (2003a) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856PubMedCrossRefGoogle Scholar
  65. Mittova V, Theodoulou FL, Kiddle G, Gomez L, Volokita M, Tal M, Foyer CH, Guy M (2003b) Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 554:417–421PubMedCrossRefGoogle Scholar
  66. Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates teh antioxidative system in root mitocondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 399:1105–1113CrossRefGoogle Scholar
  67. Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1179PubMedPubMedCentralCrossRefGoogle Scholar
  68. Moriwaki T, Yamamoto Y, Aida T, Funahashi T, Shishido T, Asada M, Prodhan SH, Komamine A, Motohashi T (2008) Overexpression of the Escherichia coli catalase gene, katE, enhances tolerance to salinity stress in the transgenic indica rice cultivar, BR5. Plant Biotechnol Rep 2:41–46CrossRefGoogle Scholar
  69. Mutlu S, Atici Ö, Nalbantoglu B (2009) Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. Biol Plant 53:334–338CrossRefGoogle Scholar
  70. Nagamiya K, Motohashi T, Nakao K, Prodhan SH, Hattori E, Hirose S, Ozawa K, Ohkawa Y, Takabe T, Takabe T, Komamine A (2007) Enhancement of salt tolerance in transgenic rice expressing an Escherichia coli catalase gene, katE. Plant Biotechnol Rep 1:49–55CrossRefGoogle Scholar
  71. Nam MH, Huh SM, Kim KM, Park WJ, Seo JB, Cho K, Kim DY, Kim BG, Yoon IS (2012) Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteome Sci 10:25PubMedPubMedCentralCrossRefGoogle Scholar
  72. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279PubMedCrossRefGoogle Scholar
  73. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Phan Tran LS (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49PubMedCrossRefGoogle Scholar
  74. Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. Plant J 62:316–329PubMedCrossRefGoogle Scholar
  75. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  76. Parker R, Flowers TJ, Moore AL, Harpham NV (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57:1109–1118PubMedCrossRefGoogle Scholar
  77. Pennell R (1998) Cell walls: structures and signals. Curr Opin Plant Biol 1:504–510PubMedCrossRefGoogle Scholar
  78. Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res 17:281–291PubMedCrossRefGoogle Scholar
  79. Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of Arabidopsis. Russ J Plant Physiol 57:233–240CrossRefGoogle Scholar
  80. Qiu-Fang Z, Yuan-Yuan L, Cai-Hong P, Cong-Ming L, Bao-Shan W (2005) NaCl enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Sci 168:423–430CrossRefGoogle Scholar
  81. Ramanjulu S, Kaiser W, Dietz KJ (1999) Salt and drought stress differentially affect the accumulation of extracellular proteins in barley. Z Naturforsch 54:337–347Google Scholar
  82. Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234PubMedCrossRefGoogle Scholar
  83. Sgherri CLM, Maffei M, Navari-lzzo F (2000) Antioxidative enzymes in wheat subjected to increasing water deficit and rewatering. J Plant Physiol 157:273–279CrossRefGoogle Scholar
  84. Shabala S, Munns R (2012) Salinity stress: physiological constraints and adaptative mechanisms. In: Shabala S (ed) Plant stress physiology. CAB International, London, pp 59–93. ISBN 9781845939953CrossRefGoogle Scholar
  85. Shafi A, Gill T, Sreenivasulu Y, Kumar S, Ahuja PS, Singh AK (2015) Improved callus induction, shoot regeneration, and salt stress tolerance in Arabidopsis overexpressing superoxide dismutase from Potentilla atrosanguinea. Protoplasma 252:41–51PubMedCrossRefGoogle Scholar
  86. Sierla M, Rahikainen M, Salojärvi J, Kangasjärvi J, Kangasjärvi S (2013) Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Signal 18:2220–2239PubMedCrossRefGoogle Scholar
  87. Sies H (1991) Oxidative stress II. Oxidants and antioxidants. Academic, LondonGoogle Scholar
  88. Song Y, Zhang C, Ge W, Zhang Y, Burlingame AL, Guoa Y (2011) Identification of NaCl stress-responsive apoplastic proteins in rice shoot stems by 2D-DIGE. J Proteomics 74:1045–1067PubMedPubMedCentralCrossRefGoogle Scholar
  89. Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sultana S, Khew CY, Morshed MM, Namasivayam P, Napis S, Ho CL (2012) Overexpression of monodehydroascorbate reductase from a mangrove plant (AeMDHAR) confers salt tolerance on rice. J Plant Physiol 169:311–318PubMedCrossRefGoogle Scholar
  91. Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates, SunderlandGoogle Scholar
  92. 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 60:795–804PubMedCrossRefGoogle Scholar
  93. Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599PubMedCrossRefGoogle Scholar
  94. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K et al (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152PubMedCrossRefGoogle Scholar
  95. Tseng MJ, Liu C-W, Yiu J-C (2007) Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. Plant Physiol Biochem 45:822–833PubMedCrossRefGoogle Scholar
  96. Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184PubMedCrossRefGoogle Scholar
  97. Valderrama R, Corpas FJ, Carreras A, Ferna’ndez-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461PubMedCrossRefGoogle Scholar
  98. Wang Y, Ying Y, Chen J, Wang XC (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677CrossRefGoogle Scholar
  99. Wang Y, Wisniewski M, Meilan R, Cui M, Webb R, Fuchigami L (2005) Overexpression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. J Am Soc Hortic Sci 130:167–173Google Scholar
  100. Wang Y, Wisniewski M, Meilan R, Uratsu SL, Cui MG, Dandekar A, Fuchigami L (2007) Ectopic expression of Mn-SOD in Lycopersicon esculentum leads to enhanced tolerance to salt and oxidative stress. J Appl Hortic 9:3–8Google Scholar
  101. Wang R, Chen S, Zhou X, Shen X, Deng L, Zhu H, Shao J, Shi Y, Dai S, Fritz E, Hüttermann A, Polle A (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 28:947–957PubMedCrossRefGoogle Scholar
  102. Wang YC, Qu GZ, Li HY, Wu YJ, Wang C, Liu GF, Yang CP (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124PubMedCrossRefGoogle Scholar
  103. Wang H, Zhou L, Fu Y, Cheung MY, Wong FL, Phang TH, Sun Z, Lam HM (2012) Expression of an apoplast-localized BURP-domain protein from soybean (GmRD22) enhances tolerance towards abiotic stress. Plant Cell Environ 35:1932–1947PubMedCrossRefGoogle Scholar
  104. Witzel K, Weidner A, Surabhi GK, Börner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 60:3545–3557Google Scholar
  105. Xu E, Brosché M (2014) Salicylic acid signaling inhibits apoplastic reactive oxygen species signaling. BMC Plant Biol 14:155PubMedPubMedCentralCrossRefGoogle Scholar
  106. Xu W-F, Shi W-M, Ueda A, Takabe T (2008) Mechanisms of salt tolerance in transgenic Arabidopsis thaliana carrying a peroxisomal ascorbate peroxidase gene from barley. Pedosphere 18:486–495CrossRefGoogle Scholar
  107. Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244PubMedCrossRefGoogle Scholar
  108. Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H, Shigeoka S (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J 37:21–33PubMedCrossRefGoogle Scholar
  109. Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zhao F, Zhang H (2006) Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice. Plant Cell Tissue Organ Cult 86:349–358CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • J. A. Hernández
    • 1
    Email author
  • G. Barba-Espín
    • 1
    • 2
  • M. J. Clemente-Moreno
    • 1
  • P. Díaz-Vivancos
    • 1
  1. 1.Fruit Tree Biotechnology Group, Department of Plant BreedingCEBAS-CSIC, Campus Universitario de EspinardoMurciaSpain
  2. 2.Department of Plant and Environmental SciencesUniversity of CopenhagenCopenhagenDenmark

Personalised recommendations