Advertisement

Drought, Desiccation, and Oxidative Stress

  • Renate Scheibe
  • Erwin BeckEmail author
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 215)

Abstract

Reactive oxygen species (ROS) are noxious but inevitable by-products of aerobic metabolism. Singlet oxygen 1O2, the oxygen radical anion O 2 , the extremely toxic hydroxyl radical OH, and finally H2O2 originate in photosynthesis, but O 2 and H2O2 can also arise in the mitochondrial electron transport, and H2O2 is a normal intermediate in photorespiration and a product of several plasma membranes or apoplastic oxidases. All aerobic organisms, in particular plants, have a great variety of antioxidative and detoxifying compounds and enzymes to keep the level of ROS in all cellular compartments low. Under stress, the production of ROS is enhanced and organisms must counteract oxidative stress by enhancing their antioxidative potential. The elevated level of ROS, especially of H2O2, can be sensed and start MAP-kinase signaling cascades or can activate or inactivate signal transmitting elements such as protein kinases and phosphatases. Redox regulation of thiol–disulfide interchanges plays a major role in ROS signaling. Interaction of osmotic and ROS signals result in mutual modulations of the respective signaling networks. Such interactions are shown for drought-induced gene activation and for the regulation of stomata closure. Thus, ROS play a dual role in plants, as noxious reactants involved in uncontrolled or programmed cell death, but also as signals stimulating adaptation to abiotic stress, in particular from desiccation and drought. Representing one of the major challenges for plant life, tolerance of, or resistance to oxidative stress under drought is a promising aim for genetic engineering of crop plants.

Keywords

Reactive Oxygen Species Drought Stress Reactive Oxygen Species Production NADPH Oxidase Photosynthetic Electron Transport Chain 
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. Ahsan MK, Lekli I, Ray D, Yodoi J, Das DK (2009) Redox regulation of cell survival by the thioredoxin superfamily: an implication of redox gene therapy in the heart. Antioxid Redox Signal 11:2741–2758PubMedGoogle Scholar
  2. Akashi K, Miyake C, Yokota A (2001) Citrulline, a novel compatible solute in drought-tolerant wild watermelon leaves, is an efficient hydroxyl radical scavenger. FEBS Lett 508:438–442PubMedGoogle Scholar
  3. Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical-scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Biophys Res Commun 323:72–78PubMedGoogle Scholar
  4. Annamalai P, Yanagihara S (1999) Identification and characterization of a heat stress induced gene in cabbage encodes a Kunitz type protease inhibitor. J Plant Physiol 155:226–233Google Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedGoogle Scholar
  6. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedGoogle Scholar
  7. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287Google Scholar
  8. Atkin OK, Macharel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597PubMedGoogle Scholar
  9. Bailly C (2004) Acitve oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107Google Scholar
  10. Baroli CG, Simontacci M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50:375–383Google Scholar
  11. Bartels D (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance? Trends Plant Sci 6:284–286PubMedGoogle Scholar
  12. Bartoli CG, Gomez F, Gergoff G, Guiamét JJ, Puntarulo S (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J Exp Bot 56:1269–1276PubMedGoogle Scholar
  13. Bellinger Y, Larher F (1987) Proline accumulation in higher plants: a redox buffer? Plant Physiol 6:23–27Google Scholar
  14. Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiol 112:265–272PubMedGoogle Scholar
  15. Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462. doi: 10.1111/j.1399-3054.2009.01340.x PubMedGoogle Scholar
  16. Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5:241–246PubMedGoogle Scholar
  17. Bowler C, van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116Google Scholar
  18. Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54Google Scholar
  19. Broin M, Cuiné S, Peltier G, Rey P (2000) Involvement of CDSP 32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett 467:245–248PubMedGoogle Scholar
  20. Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220PubMedGoogle Scholar
  21. Chen KM, Gong HJ, Chen GC, Wang SM, Zhang CL (2004) Gradual drought under field conditions influences the glutathione metabolism, redox balance and energy supply in spring wheat. J Plant Growth Regul 23:20–28Google Scholar
  22. Chinnusamy V, Schumaker K, Zhu J-K (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236PubMedGoogle Scholar
  23. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and response to oxidative stress in plants. J Exp Bot 57:449–459PubMedGoogle Scholar
  24. Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species. Plant Signal Behav 3:156–165PubMedGoogle Scholar
  25. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen network of Arabidopsis. Plant Cell 17:268–281PubMedGoogle Scholar
  26. 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 57:779–795PubMedGoogle Scholar
  27. Desikan R, Cheung M-K, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212PubMedGoogle Scholar
  28. Devi SR, Chen X, Oliver DJ, Xiang C (2006) A novel high-throughput genetic screen for stress-responsive mutants of Arabidopsis thaliana reveals new loci involving stress responses. Plant J 47:652–663Google Scholar
  29. Dietz K-J (2005) Plant thiol enzymes and thiol homeostasis in relation to thiol-dependent redox regulation and oxidative stress. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, NJ, USA, pp 25–52Google Scholar
  30. Dóczi R, Brader G, Pettko-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279PubMedGoogle Scholar
  31. Downing WL, Mauxion F, Fauvarque MO, Reviron MP, de Vienne D, Vartanian N, Giraudat J (1992) A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water stress in leaves, not in seeds. Plant J 2:685–693PubMedGoogle Scholar
  32. Eckardt N (2001) Luc genetic screen illuminates stress-responsive gene regulation. Plant Cell 13:1969–1972PubMedGoogle Scholar
  33. Fischer BB, Eggen RIL, Trebst A, Krieger-Liszkay A (2006) The glutathione peroxidase homologous gene Gpxh in Chlamydomonas reinhardtii is upregulated by singlet oxygen produced in photosystem II. Planta 223:583–590PubMedGoogle Scholar
  34. Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RIL (2007) Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett 581:5555–5560PubMedGoogle Scholar
  35. Foyer CH, Noctor G (2005a) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in physiological context. Plant Cell Environ 28:1056–1071Google Scholar
  36. Foyer CH, Noctor G (2005b) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedGoogle Scholar
  37. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254PubMedGoogle Scholar
  38. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J 33:691–705PubMedGoogle Scholar
  39. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Naruasaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedGoogle Scholar
  40. Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IM, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445PubMedGoogle Scholar
  41. Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121PubMedGoogle Scholar
  42. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430PubMedGoogle Scholar
  43. George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confers drought tolerance on tobacco. J Plant Physiol 167:311–318PubMedGoogle Scholar
  44. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan Y-F, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of ALTERNATIVE OXIDASE1A in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610PubMedGoogle Scholar
  45. Gorman AA, Rodgers MA (1992) Current perspectives of singlet oxygen detection in biological environments. J Photochem Photobiol 14:159–176Google Scholar
  46. Guan LM, Zhao J, Scandalios JG (2000) Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95PubMedGoogle Scholar
  47. Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J Prot Res 6:1451–1460Google Scholar
  48. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedGoogle Scholar
  49. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150PubMedGoogle Scholar
  50. Halliwell B, Gutteridge JMC (1999) Free Radicals in Biology and Medicine. Oxford University Press, OxfordGoogle Scholar
  51. Hatz S, Lambert JDC, Ogilby PR (2007) Measuring the lifetime of singlet oxygen in a single cell: addressing the issue of cell viability. Photochem Photobiol Sci 6:1106–1116PubMedGoogle Scholar
  52. Hazen SP, Wu Y, Kreps JA (2003) Gene expression profiling of plant responses to abiotic stress. Funct Integr Genom 3:105–111Google Scholar
  53. Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066PubMedGoogle Scholar
  54. Holmberg N, Bülow L (1998) Improving stress tolerance in plants by gene transfer. Trends Plant Sci 3:61–66Google Scholar
  55. Hosein B, Palmer G (1983) The kinetics and mechanism of reaction of reduced ferredoxin by molecular oxygen and its reduced products. Biochem Biophys Acta 723:383–390Google Scholar
  56. Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or Paraquat. Plant Physiol 116:173–181Google Scholar
  57. Jahan MS, Ogawa K, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Deficient glutathione in guard cells facilitates abscisic acid-induced stomatal closure but does not affect light-induced stomatal opening. Biosci Biotechnol Biochem 72:2795–2798PubMedGoogle Scholar
  58. Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413. doi: 10.111/j1399-3054.2009.01321.x PubMedGoogle Scholar
  59. Jiang M, Zhang J (2002a) Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215:1022–1030PubMedGoogle Scholar
  60. Jiang M, Zhang J (2002b) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410PubMedGoogle Scholar
  61. Kaiser WM (1976) The effect of hydrogen peroxide on CO2-fixation of isolated chloroplasts. Biochim Biophys Acta 440:476–482PubMedGoogle Scholar
  62. Kaiser WM (1979) Reversible inhibition of the Calvin Cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377–382Google Scholar
  63. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291PubMedGoogle Scholar
  64. Khanna-Chopra R, Selote DS (2007) Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than – susceptible wheat cultivar under field conditions. Environ Exp Bot 60:276–283Google Scholar
  65. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshida H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080PubMedGoogle Scholar
  66. 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 167:77–80PubMedGoogle Scholar
  67. Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revivval of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24PubMedGoogle Scholar
  68. Kranner I, Birtić S (2005) A modulating role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740PubMedGoogle Scholar
  69. Kranner I, Grill D (1996) Significance of thiol-disulfide exchange in resting stages of plant development. Bot Acta 109:8–14Google Scholar
  70. Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedGoogle Scholar
  71. Kwak JM, Mäser P, Schroeder JI (2010) The clickable guard cell, Version II: Interactive model of guard cell signal transduction mechanisms and pathways. http://www-biology.ucsd.edu/labs/schroeder/index.html
  72. Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106:21419–21424PubMedGoogle Scholar
  73. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedGoogle Scholar
  74. Lopez-Huertas E, Charlton WL, Johnson B, Graham IA, Baker A (2000) Stress induces peroxisome biogenesis genes. EMBO J 19:6770–6777PubMedGoogle Scholar
  75. Lukosz M, Jakob S, Büchner N, Zschauer T-C, Altschmied J, Haendeler J (2010) Nuclear redox signaling. Antioxid Redox Signal 12:713–742PubMedGoogle Scholar
  76. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscsic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  77. Meinhard M, Rodriguez PL, Grill E (2002) The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214:775–782PubMedGoogle Scholar
  78. Miao Y, Lv D, Wang P, Wang X-C, Chen J, Miao C, Song C-P (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766PubMedGoogle Scholar
  79. Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288PubMedGoogle Scholar
  80. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489PubMedGoogle Scholar
  81. Mitsuhara I, Malik KA, Miura M, Ohashi Y (1999) Animal cell-death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants. Curr Biol 9:775–778PubMedGoogle Scholar
  82. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedGoogle Scholar
  83. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedGoogle Scholar
  84. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedGoogle Scholar
  85. Miyake C, Asada K (1996) Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate; hydrogen peroxide decomposes Compound I of ascorbate peroxidase. Plant Cell Physiol 37:423–430Google Scholar
  86. Moon H, Lee B, Choi G, Shin D, Prasad DT, Lee O, Kwak S-S, Kim DH, Nam J, Bahk J, Hong JC, Lee SY, Cho MJ, Lim CO, Yun D-J (2003) NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 100:358–363PubMedGoogle Scholar
  87. Moore JP, Westall KL, Ravenscroft N, Farrant JM, Lindsey GG, Brandt WF (2005) The predominant polyphenol in the leaves of the resurrection plant Myrothamnus flabellifolius, 3, 4, 5 tri-O-galloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochem J 385:301–308PubMedGoogle Scholar
  88. Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM (2009) Towards a systems-based understanding of plant desiccation tolerance. Trends Plant Sci 14:110–117PubMedGoogle Scholar
  89. Morabito D, Guerrier G (2000) The free oxygen radical scavenging enzymes and redox status in roots and leaves of Populus x euramericana in response to osmotic stress, desiccation and rehydration. J Plant Physiol 157:74–80Google Scholar
  90. Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants – where do we stand? Physiol Plant 138:372–383PubMedGoogle Scholar
  91. Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215:716–726PubMedGoogle Scholar
  92. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591PubMedGoogle Scholar
  93. Mubarakshina M, Khorobrykh S, Ivanov B (2006) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane. Biochim Biophys Acta 1757:1496–1503PubMedGoogle Scholar
  94. Munné-Bosch S, Peñuelas J (2004) Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions. Plant Sci 166:1105–1110Google Scholar
  95. Murata Y, Pei Z-M, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523PubMedGoogle Scholar
  96. Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665PubMedGoogle Scholar
  97. Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71Google Scholar
  98. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148PubMedGoogle Scholar
  99. Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot J-P, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379PubMedGoogle Scholar
  100. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176PubMedGoogle Scholar
  101. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850PubMedGoogle Scholar
  102. Nuhse TS, Bottrill AR, Jones AM, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940PubMedGoogle Scholar
  103. Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892PubMedGoogle Scholar
  104. Ogawa K, Kanematsu S, Takabe K, Asada K (1995) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PS I) in spinach chloroplasts: detection by immunogold labeling after rapid freezing and substitution method. Plant Cell Physiol 36:565–573Google Scholar
  105. Ogawa K, Kanematsu S, Asada K (1996) Intra- and extra-cellular localization of “cytosolic” CuZn-superoxide dismutase in spinach leaf and hypocotyls. Plant Cell Physiol 37:790–799Google Scholar
  106. Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Iida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. Plant J 34:868–887PubMedGoogle Scholar
  107. Pammenter NW, Berjak P (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Sci Res 9:13–37Google Scholar
  108. Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-f F, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez D, McCourt R, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits Type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedGoogle Scholar
  109. Pastore D, Trono D, Laus MN, Di Fonzo N, Flagella Z (2007) Possible plant mitochondria involvement in cell adaptation to drought stress. A case study: Durum wheat mitochondria. J Exp Bot 58:195–210PubMedGoogle Scholar
  110. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734PubMedGoogle Scholar
  111. Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology – a charging concept. Plant Physiol BiochemPubMedGoogle Scholar
  112. Pukacka S, Ratajczak E (2006) Antioxidative response of ascorbate-glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. J Plant Physiol 163:1259–1266PubMedGoogle Scholar
  113. Rabbani MA, Maruyama K, Abe H, Khan A, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767PubMedGoogle Scholar
  114. Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202Google Scholar
  115. Rey P, Pruvot G, Besuwe N, Eymery F, Rumeau D, Peltier G (1998) A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J 13:97–107PubMedGoogle Scholar
  116. Rey P, Cuiné S, Eymery F, Garin J, Court M, Jacquot J-P, Rouhier N, Broin M (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41:31–42PubMedGoogle Scholar
  117. Robinson JM, Bunce JA (2000) Influence of drought-induced water stress on soybean an spinach leaf ascorbate-dehydroascorbate level and redox status. Int J Plant Sci 161:271–279PubMedGoogle Scholar
  118. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110PubMedGoogle Scholar
  119. Rodriguez Milla MA, Maurer A, Rodriguez Huete A, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615PubMedGoogle Scholar
  120. Rodriguez Milla MA, Townsend J, Chang I-F, Cushman JC (2006) The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant Mol Biol 61:13–30Google Scholar
  121. Romano PGN, Horton P, Gray JE (2004) The Arabidopsis cyclophilin gene family. Plant Physiol 134:1268–1282PubMedGoogle Scholar
  122. Saibo NJM, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623PubMedGoogle Scholar
  123. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedGoogle Scholar
  124. Santiago J, Dupeux F, Round A, Antoni R, Park S-Y, Jamin M, Cutler SR, Rodriguez PL, Márquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462:665–668PubMedGoogle Scholar
  125. Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26PubMedGoogle Scholar
  126. Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostsis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489PubMedGoogle Scholar
  127. Schmidt K, Fufezan C, Kieger-Liszkay A, Satoh H, Paulsen H (2003) Recombinant water-soluble chlorophyll protein from Brassica oleracea var botrys binds various chlorophyll derivatives. Biochemistry 42:7427–7433PubMedGoogle Scholar
  128. Seki M, Satou M, Sakurai T, Akiyama K, Iida K, Ishida J, Nakajima M, Enju A, Narusaka M, Fujita M, Oono Y, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2004) RIKEN Arabidopsis full-length (RAFL) cDNA and its applications for expression profiling under abiotic stress condition. J Exp Bot 55:213–223PubMedGoogle Scholar
  129. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227Google Scholar
  130. Skovsen E, Snyder JW, Lambert JDC, Ogilby PR (2005) Lifetime and diffusion of singlet oxygen in a cell. J Phys Chem B 109:8570–8573PubMedGoogle Scholar
  131. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58Google Scholar
  132. Smirnoff N, Cumbes Q (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1957–1960Google Scholar
  133. Steiger HM, Beck E, Beck R (1977) Oxygen concentration in isolated chloroplasts during photosynthesis. Plant Physiol 60:903–906PubMedGoogle Scholar
  134. Steiger HM, Beck E (1981) Formation of hydrogen peroxide and oxygen dependence of photosynthetic CO2 assimilation by intact chloroplasts. Plant Cell Physiol 22:561–576Google Scholar
  135. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040PubMedGoogle Scholar
  136. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedGoogle Scholar
  137. Tabaei-Aghdaei SR, Harrison P, Pearce RS (2000) Expression of dehydration-stress-related genes in the crowns of wheatgrass species [Lophopyrum elongatum (Host) A. Love and Agropyron desertorum (Fisch. ex Link.) Schult.] having constrating acclimation to salt, cold and drought. Plant Cell Environ 23:561–571Google Scholar
  138. Takahashi S, Katagiri T, Yamaguchi-Shinozaki K, Shinozaki K (2000) An Arabidopsis gene encoding a Ca2+-binding protein is induced by abscisic acid during dehydration. Plant Cell Physiol 41:898–903PubMedGoogle Scholar
  139. Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55PubMedGoogle Scholar
  140. Tanaka T, Nakamura H, Nishiyama A, Hosoi F, Masutani H, Wada H, Yodoi J (2000) Redox regulation by thioredoxin superfamily; protection against oxidative stress and aging. Free Radical Res 33:851–855Google Scholar
  141. Tolbert NE (1994) Role of photosynthesis and photorespiration in regulating atmospheric CO2 and O2. In: Tolbert NE, Preiss J (eds) Regulation of atmospheric CO2 and O2 by photosynthetic carbon metabolism. Oxford University Press, New York, Oxford, pp 8–33Google Scholar
  142. Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754PubMedGoogle Scholar
  143. Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984PubMedGoogle Scholar
  144. Vasquez-Robinet C, Mane SP, Ulanov AV, Watkinson JI, Stromberg VK, De Koeyer D, Schafleitner R, Willmot DB, Bonierbale M, Bohnert HJ, Grene R (2008) Physiological and molecular adaptation to drought in Andean potato genotypes. J Exp Bot 59:2109–2123PubMedGoogle Scholar
  145. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539PubMedGoogle Scholar
  146. Vieira Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:329–334PubMedGoogle Scholar
  147. Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertsdotter U, Sederoff RR, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133:1702–1716PubMedGoogle Scholar
  148. Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816PubMedGoogle Scholar
  149. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631PubMedGoogle Scholar
  150. Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139PubMedGoogle Scholar
  151. Yamaguchi-Shinozaki K, Shinozaki K (2004) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94Google Scholar
  152. Yang S-L, Lan S-S, Gong M (2009) Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol 166:1694–1699PubMedGoogle Scholar
  153. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318PubMedGoogle Scholar
  154. Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48:606–614PubMedGoogle Scholar
  155. Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in responses to oxidative stresses. Plant Physiol 123:223–233PubMedGoogle Scholar
  156. Yu C-W, Murphy TM, Lin C-H (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963Google Scholar
  157. Zagdańska B, Wiśniewski K (1996) Change in the thiol/disulfide redox potential in wheat leaves upon water deficit. J Plant Physiol 149:462–465Google Scholar
  158. Zhang X, Wang H, Takemiya A, Song CP, Kinoshita T, Shimazaki K (2004) Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts. Plant Physiol 136:4150–4158PubMedGoogle Scholar
  159. Zhang J, Addepalli B, Yun K-Y, Hunt AG, Xu R, Rao S, Li QQ, Falcone DL (2008) A polyadenylation factor subunit implicated in regulating oxidative signaling in Arabidopsis thaliana. PLoS ONE 3:e2410PubMedGoogle Scholar
  160. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377PubMedGoogle Scholar
  161. Zhao Z, Chen G, Zhang C (2001) Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Aust J Plant Physiol 28:1055–1061Google Scholar
  162. Zheng J, Zhao J, Tao Y, Wang J, Liu Y, Fu J, Jin Y, Gao P, Zhang J, Bai Y, Wang G (2004) Isolation and analysis of water stress induced genes in maize seedlings by subtractive PCR and cDNA macroarray. Plant Mol Biol 55:807–823PubMedGoogle Scholar
  163. Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Mol Cell Biol Lett 10:515–534Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Plant PhysiologyUniversity of OsnabrueckOsnabrueckGermany
  2. 2.Department of Plant PhysiologyUniversity of BayreuthBayreuthGermany

Personalised recommendations