Molecular Cell Biology: Are Reactive Oxygen Species Regulators of Leaf Senescence?

  • Ulrike Zentgraf
  • Vera Hemleben
Part of the Progress in Botany book series (BOTANY, volume 69)

Senescence processes can influence many important agricultural traits; however, our knowledge concerning regulatory mechanisms controlling senescence is still limited. Free radicals are thought to play an essential role in senescence, especially those derived from oxygen. In addition to their deleterious functions, they might serve as signalling molecules. The critical balance between production and scavenging of reactive oxygen species (ROS), which normally is very tightly regulated, appears to be specifically disrupted during the progression of senescence in different cellular compartments either by depletion of antioxidants or excess production of ROS. Hydrogen peroxide (H2O2) is very likely the most important ROS. In contrast to other ROS, it has a relatively long half-life and can also pass membranes; therefore, it can be assumed that it executes signalling functions. Hydrogen peroxide is produced in different cell compartments but can also be released into the cytosol or vice versa. The role of ROS originating from different cellular compartments like chloroplasts, peroxisomes or mitochandria is discussed here with respect to senescence.


Jasmonic Acid Leaf Senescence Alternative Oxidase Oxidative Stress Tolerance Molecular Cell Biology 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238.Google Scholar
  2. Arrigo AP (1999) Gene expression and the thiol redox state. Free Radical Biol Med 27: 936–944.Google Scholar
  3. Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570.Google Scholar
  4. Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol 134:1784–1792.PubMedGoogle Scholar
  5. Batt T, Woolhouse HW (1975) Changing activities during senescence and sites of synthesis of photosynthetic enzymes in leaves of labiate, Perilla frutenscens (L.). British J Exp Bot 26:569–579.Google Scholar
  6. Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344.Google Scholar
  7. Borghouts C, Werner A, Elthon T, Osiewacz HD (2001) Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserine. Mol Cell Biol 21:390–399.PubMedGoogle Scholar
  8. Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116.Google Scholar
  9. Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585.PubMedGoogle Scholar
  10. Casano LM, Martín M, Sabater B (1994) Sensitivity of superoxide dismutase transcript levels and activities to oxidative stress is lower in mature-senescent than in young barley leaves. Plant Physiol 106:1033–1039.PubMedGoogle Scholar
  11. Chia LS, Thompson JE, Dumbroff EB (1981) Simulation of the effects of leaf senescence on membranes by treatment with paraquat. Plant Physiol 67:415–420.PubMedGoogle Scholar
  12. Corpas FJ, Barroso JB, Río LA del (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150.PubMedGoogle Scholar
  13. Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733.PubMedGoogle Scholar
  14. Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006) Response to Zemojtel et al. Plant nitric oxide synthase: back to square one. Trends Plant Sci 11:526–527.Google Scholar
  15. Dalton DA, Langeberg L, Treneman NC (1993) Correlations between the ascorbate–glutathione pathway and effectiveness in legume root nodules. Physiol Plant 87:365–370.Google Scholar
  16. Dat JF, 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 57:779–795.PubMedGoogle Scholar
  17. Delaunay A, Pflieger D, Barrault MB, Vinh J, Toledano MB (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481.PubMedGoogle Scholar
  18. Dertinger U, Schaz U, Schulze ED (2003) Age-dependence of the antioxidative system in tobacco with enhanced glutathione reductase activity or senescence-induced production of cytokinins. Physiol Plant 119:19–29.Google Scholar
  19. Desikan, R, Mackerness AHS, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172.PubMedGoogle Scholar
  20. Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55: 205–212.PubMedGoogle Scholar
  21. Dhinsda RJ, Dhinsda PP, Thorpe TA (1981) Leaf senescence: correlation with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101.Google Scholar
  22. Diaz C, Purdy S, Christ A, Morot-Gaudry J-F, Wingler A, Masclaux-Daubresse C (2005) Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis thaliana: a metabolic profiling approach. Plant Physiol 138:898–908.PubMedGoogle Scholar
  23. Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, Nunes de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709.PubMedGoogle Scholar
  24. Djanaguiraman M, Devi DD, Shanker AK, Sheeba JA, Bangarusamy U (2005) Selenium–an antioxidative protectant in soybean during senescence. Plant Soil 272:77–86.Google Scholar
  25. Dufour E, Larsson NG (2004) Understanding aging: revealing order out of chaos. Biochim Biophys Acta 1658:122–132.PubMedGoogle Scholar
  26. Dufour E, Boulay J, Rincheval V, Sainsard-Chanet A (2000) A causal link betweeen respiration and senescence in Podospora anserina. Proc Natl Acad Sci USA 97:4138–4143.PubMedGoogle Scholar
  27. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574.PubMedGoogle Scholar
  28. Evans PJ, Gallesi D, Mathieu C, Hernandez MJ, Felip M de, Halliwell B, Puppo A (1999) Oxidative stress occurs during soybean nodule senescence. Planta 208:73–79.Google Scholar
  29. Fajkus J, Zentgraf U (2002) Structure and maintenance of chromosome ends. In: Krupp G, Parwaresch R (eds) Telomeres and telomerases: cancer and biology. Bioscience/Gen-Expression, available at:
  30. Ferri KF, Kroemer G (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3:E255–E263.PubMedGoogle Scholar
  31. Foyer CH (1996) Oxygen processing in photosynthesis. Biochem Soc Trans 24:427–433.PubMedGoogle Scholar
  32. Foyer CH (2004) The role of ascorbic acid in defense networks and signaling in plants. In: Asard H, May JM, Smirnoff S (eds) Vitamin C. Functions and biochemistry in animals and plants. Bios, Oxford, pp 65–82.Google Scholar
  33. Foyer CH, Trebstm A, Noctor G (2005) Protective and signalling functions of ascorbate, glutathione and tocopherol in chloroplasts. In: Demmig-Adams B, Adams WW (eds) Advances in photosynthesis and respiration: photoprotection, photoinhibition, gene regulation, and environment, vol 19. Kluwer, Dordrecht, pp 241–268.Google Scholar
  34. Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988.PubMedGoogle Scholar
  35. Gan S, Amasino RM (1997) Making sense of senescence: molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113:313–319.PubMedGoogle Scholar
  36. Gasch A, Spellman P, Kao C, Harel O, Eisen M, Storz G, Botstein D, Brown P (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257.PubMedGoogle Scholar
  37. Grbic V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602.Google Scholar
  38. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312.PubMedGoogle Scholar
  39. Groten K Vanacke, H, Dutilleul C, Bastian F, Bernhard S, Carzaniga R, Foyer CH (2005) The roles of redox processes in pea nodule development and senescence. Plant Cell Environ 28:1293–1304.Google Scholar
  40. Guo FQ (2006) Response to Zemojtel et al. Plant nitric oxide synthase: AtNOS1 is just the beginning. Trends Plant Sci 11:527–528.Google Scholar
  41. Guo FQ, Crawford NM (2005) Arabidopsis Nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450.PubMedGoogle Scholar
  42. Haghdoost S, Sjolander L, Czene S, Hanns-Ringdahl M (2006) The nucleotide pool is a significant target for oxidative stress. Free Radical Biol Med 41:620–626.Google Scholar
  43. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Oxford University Press, Oxford.Google Scholar
  44. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Geront 11:298–300.PubMedGoogle Scholar
  45. Harman D (1998) Extending functional life span. Exp Geront 33:95–112.Google Scholar
  46. He Y, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiol 126:707–716.PubMedGoogle Scholar
  47. He Y, Fukushige H, Hildebrande DF, Gan S (2002) Evidence supporting a role for jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884.PubMedGoogle Scholar
  48. Hensel LL, Grbić V, Baumgarten D, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5:553–564.PubMedGoogle Scholar
  49. Himelblau E, Mira H, Lin SJ, Culotta VC, Penarrubia L, Amasino RM (1998) Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol 117:1227–1234.PubMedGoogle Scholar
  50. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213:469–473.PubMedGoogle Scholar
  51. Hiser C, McIntosh L (1990) Alternative oxidase of potato is an integral membrane protein synthesized de novo during aging of tuber slices. Plant Physiol 93:312–318.PubMedGoogle Scholar
  52. Hollander-Czytko H, Grabowski J, Sandorf I, Weckermann K, Weiler EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cystine lyase in Arabidopsis under stress conditions. J Plant Physiol 162: 767–770.PubMedGoogle Scholar
  53. Jiménez A, Hernández JA, Río LA del, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea (Pisum sativum L.) leaves. Plant Physiol 114:275–284.PubMedGoogle Scholar
  54. Jiménez A, Hernandez JA, Pastori G, Rio LA del, Sevilla F(1998) Role of the ascorbate–glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335.PubMedGoogle Scholar
  55. John I, Drake R, Farrell A, Cooper W, Lee P, Horton P, Grierson D (1995) Delayed leaf senescence in ethylene-deficient ACC-oxidase antisense tomato plants: molecular and physiological analysis. Plant J 7:483–490.Google Scholar
  56. Jones A (2000) Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci 5:225–230.PubMedGoogle Scholar
  57. Jongebloed U, Szederkényi J, Hartig K, Schobert C, Komor E (2004) Sequence of morphological and physiological events during natural ageing of a castor bean leaf: sieve tube occlusions and carbohydrate back-up precede chlorophyll degradation. Physiol Plant 120:338–346.PubMedGoogle Scholar
  58. Kar M, Feierabend J (1984) Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence. Planta 160:385–391.Google Scholar
  59. Keskitalo J, Bergquist G, Gardestrom P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139:1635–1648.PubMedGoogle Scholar
  60. Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci USA 92:9555–9559.PubMedGoogle Scholar
  61. Knox JP, Dodge AD (1985) Singlet oxygen and plants. Phytochemistry 24:889–896.Google Scholar
  62. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinases cascade in plants. Proc Natl Acad Sci USA 97:2940–2945.PubMedGoogle Scholar
  63. Krupinska K, Falk J, Humbeck K (2003) Genetic, metabolic and environmental factors associated with ageing in plants. In: Osiewacz HD (ed) Aging of organisms. Kluwer, Dordrecht, pp 55–78.Google Scholar
  64. Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764.PubMedGoogle Scholar
  65. Landolt R, Matile P (1990) Glyoxysome-like microbodies in senescent spinach leaves. Plant Sci 72:159–163.Google Scholar
  66. Lee H, Lee JS, Bae EK, Choi YI, Noh EW (2005) Differential expression of a poplar copper chaperone gene in response to various abiotic stresses. Tree Physiol 25:395–401.PubMedGoogle Scholar
  67. Li W, Ruf S, Bock R (2006) Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol Genet Genomics 275:185–192.PubMedGoogle Scholar
  68. Lopez-Huertas E, Charlton WL, Johnson B, Graham IA, Baker A (2000) Stress induces peroxisome biogenesis genes. EMBO J 19:6770–6777.PubMedGoogle Scholar
  69. Martin GM, Austad SN, Johnson TE (1996) Genetic analysis of aging: role of oxidative damage and environmental stresses. Nat Genet 13:25–34.PubMedGoogle Scholar
  70. Martin-Tryon EL, Kreps JA, Harmer SL (2006) GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol 143:473–486.PubMedGoogle Scholar
  71. Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518.PubMedGoogle Scholar
  72. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235.Google Scholar
  73. Matile P, Hörtensteiner S, Thomas H, Kräutler B (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol 112:1403–1409.PubMedGoogle Scholar
  74. Maxwell DP, Nickels R, McIntosh L (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J 29:269–279.PubMedGoogle Scholar
  75. May JM, Qu ZC, Mendiratta S (1998) Protection and recycling of alpha-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349:281–289.PubMedGoogle Scholar
  76. McIntosh L (1994) Molecular biology of the alternative oxidase. Plant Physiol 105:781–786.PubMedGoogle Scholar
  77. McRae DG, Thompson JE (1983) Senescence dependent changes in superoxide anion production by illuminated chloroplast from bean leaves. Planta 158:185–193.Google Scholar
  78. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867.PubMedGoogle Scholar
  79. Miao Y, Laun T, Smykowski A, Zentgraf U (2007) Arabidopsis MEKK1 can take a short cut: it can directly interact with the senescence-related WRKY53 transcription factor on the protein level and it can bind to its promoter. Plant Mol Biol, DOI 10.1007/s11103–007-9198-z.Google Scholar
  80. Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5:2–15.Google Scholar
  81. Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence. Plant Physiol 120:1015–1023.PubMedGoogle Scholar
  82. Mira H, Martinez N, Penarrubia L (2002) Expression of a vegetative-storage-protein gene from Arabidopsis is regulated by copper, senescence and ozone. Planta 214:939–946.PubMedGoogle Scholar
  83. Mishina TE, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ 30:39–52.PubMedGoogle Scholar
  84. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498.PubMedGoogle Scholar
  85. Moore AL, Albury MS, Crichton PG, Affourtit C (2002) Function of the alternative oxidase: is it still a scavenger? Trends Plant Sci 7:478–481.PubMedGoogle Scholar
  86. Munne-Bosch S, Alegre L (2002) Plant aging increases oxidative stress in chloroplasts. Planta 214:608–615.PubMedGoogle Scholar
  87. Munne-Bosch S, Falk J (2004) New insights into the function of tocopherols in plants. Planta 218:323–326.PubMedGoogle Scholar
  88. Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signalling through direct MAPK interaction. J Biol Chem 279:26959–26966.PubMedGoogle Scholar
  89. Navabpour S, Morris K, Allen R, Harrison E, Mackerness SAH, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292.PubMedGoogle Scholar
  90. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247.PubMedGoogle Scholar
  91. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279.PubMedGoogle Scholar
  92. Noctor G, Veljovic-Jovanovic S, Driscol S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in wheat leaves: a predominant role for photorespiration? Ann Bot 89:841–850.PubMedGoogle Scholar
  93. Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753.Google Scholar
  94. Orendi G, Zimmermann P, Baar C, Zentgraf U (2001) Loss of stress-induced expression of catalase3 during leaf senescence in Arabidopsis thaliana is restricted to oxidative stress. Plant Sci 161:301–314.PubMedGoogle Scholar
  95. Opresko PL, Fan JH, Danzy S, Wilson DM, Bohr VA (2005) Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2. Nucleic Acid Res 33:1230–1239.PubMedGoogle Scholar
  96. Orr WC, Sohal RS (1994) Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263:1128–1130.PubMedGoogle Scholar
  97. Panavas T, Rubinstein B (1998) Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Sci 133:125–138.Google Scholar
  98. Parthier B (1988) Gerontoplasts–the yellow end in the ontogenesis of chloroplasts. Endocytobiosis Cell Res 5:163–190.Google Scholar
  99. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265.PubMedGoogle Scholar
  100. Pastori GM, Rio LA del (1994) An activated-oxygen-mediated role for peroxisomes in the mechanism of senescence of Pisum sativum L. leaves. Planta 193:385–391.Google Scholar
  101. Pastori GM, Río LA del (1997) Natural senescence of pea leaves: an activated oxygen-mediated function for peroxisomes. Plant Physiol 113:411–418.PubMedGoogle Scholar
  102. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovi, S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951.PubMedGoogle Scholar
  103. Pauls KP, Thompson JE (1984) Evidence for the accumulation of peroxidized lipids in membranes of senescing cotyledons. Plant Physiol 75:1152–1157.PubMedGoogle Scholar
  104. Pérez-Ruiz JM, Spínola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18:356–2368 - FNI.Google Scholar
  105. Pich MM, Raule N, Catani L, Fagioli ME, Faenza I, CoccoL, Lenaz G (2004) Increased transcription of mitochondrial genes for complex I in human platelets during ageing. FEBS Lett 558:19–22.Google Scholar
  106. Pistelli L, Nieri B, Smith SM, Alpi A, De Bellis L (1996) Glyoxylate cycle enzyme activities are induced in senescent pumpkin fruits. Plant Sci 119:23–29.Google Scholar
  107. Polle A (2001) Dissecting the superoxide dismutase–ascorbate–glutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462.PubMedGoogle Scholar
  108. Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487.PubMedGoogle Scholar
  109. Pourtau N, Marès M, Purdy S, Quentin N, Ruël A, Wingler A (2004) Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219:765–772.PubMedGoogle Scholar
  110. Pourtau N, Jennings R, Pelze, E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568.PubMedGoogle Scholar
  111. Prakash JS, Baig MA, Mohanty P (2001) Senescence induced structural reorganization of thylakoid membranes in Cucumis sativus cotyledons; LHC II involvement in reorganization of thylakoid membranes. Photosynth Res 68:153–161.PubMedGoogle Scholar
  112. Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, Felipe MR de, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701.PubMedGoogle Scholar
  113. Quirino BF, Reiter WD, Amasino RM (2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol Biol 46:447–457.PubMedGoogle Scholar
  114. Richter C, Schweizer M (1997) Oxidative stress in mitochondria. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defences. Cold Spring Harbor Laboratory Press, New York, pp 169–200.Google Scholar
  115. Río LA del, Pastori, GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200.PubMedGoogle Scholar
  116. Río LA del, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272.PubMedGoogle Scholar
  117. Rio LA del, Sandalio LM, Altomare DA, Zilinskas BA (2003) Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54:923–933.PubMedGoogle Scholar
  118. Rio LA del, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335.PubMedGoogle Scholar
  119. Scandalios JG (2002) Oxidative stress responses–what have genome-scale studies taught us? Genome Biol 3:R1019.1–R1019.6.Google Scholar
  120. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319.PubMedGoogle Scholar
  121. Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448.Google Scholar
  122. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63.PubMedGoogle Scholar
  123. Stacy RAP, Nordeng TW, Culiáñez-Macià FA, Aelen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19:1–8.PubMedGoogle Scholar
  124. Stessman D, Miller A, Spalding M, Rodermel S (2002) Regulation of photosynthesis during Arabidopsis leaf development in continuous light. Photosynth Res 72:27–37.PubMedGoogle Scholar
  125. Svensson AS, Rasmusson AG (2001) Light-dependent gene expression for proteins in the respiratory chain of potato leaves. Plant J 28:73–82.PubMedGoogle Scholar
  126. Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Physiol 31:83–111.Google Scholar
  127. Thomas H, Ougham H, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54:1127–1132.PubMedGoogle Scholar
  128. Thomas JC, Perron M, LaRosa PC, Smigocki AC (2005) Cytokinin and the regulation of a tobacco metallothionein-like gene during copper stress. Physiol Plant 123:262–271.Google Scholar
  129. Thompson JE, Ledg RL, Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105:317–344.Google Scholar
  130. Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139:1806–1820.PubMedGoogle Scholar
  131. Van Doorn WG (2004) Is petal senescence due to sugar starvation? Plant Physiol 134:35–42.PubMedGoogle Scholar
  132. Van Staden J, Cook EL, Noodén LD (1988) Cytokinins and senescence. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic, San Diego, pp 282–328.Google Scholar
  133. Vanacker H, Sandalio L, Jimenez A, Palma JM, Corpas FJ, Meseguer V, Gomez M, Sevilla F, Leterrier M, Foyer CH, Rio LA del (2006) Roles for redox regulation in leaf senescence of pea plants grown on different sources of nitrogen nutrition. J Exp Bot 57:1735–1745.PubMedGoogle Scholar
  134. Vandenabeele S, Van der Kelen K, Dat J, Gadjev I, Bonefaes T, Morsa S, Rottiers P, Sloten L, Van Montagu M, Zabeau M, Inzé D, Van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expresión in tobacco. Proc Natl Acad Sci USA 100:16113–16118.PubMedGoogle Scholar
  135. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005). Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821.PubMedGoogle Scholar
  136. Von Zglincki T (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27:339–344.Google Scholar
  137. Watanabe K, Yamada N, Takeuchi Y (2006) Oxidative DNA damage in cucumber cotyledons irradiated with ultraviolet light. J Plant Res 119:239–246.PubMedGoogle Scholar
  138. 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 16:4806–4816.PubMedGoogle Scholar
  139. Wingler A, Schaewen A von, Leegood RC, Lea PJ, Quick WP (1998) Regulation of leaf senescence by cytokinin, sugars, and light effects on NADH-dependent hydroxypyruvate reductase. Plant Physiol 116:329–335.Google Scholar
  140. Wingler A, Marès M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytol 161:781–789.Google Scholar
  141. Woo HR, Kim JH, Nam HG, Lim PO (2004) The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. Plant Cell Physiol 45:923–932.PubMedGoogle Scholar
  142. Ye ZZ, Rodriguez R, Tran A, Hoang H, Santos D de los, Brown S, Vellanoweth RL (2000) The developmental transition to flowering represses ascorbate peroxidase activity and induces enzymatic lipid peroxidation in leaf tissue in Arabidopsis thaliana. Plant Sci 158:115–127.PubMedGoogle Scholar
  143. Zapater JM, Guera A, Esteban-Carrasco A, Martin M, Sabater B (2005) Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Diff 12:1277–1284.Google Scholar
  144. Zavaleta-Mancera HA, Franklin KA, Ougham HJ, Thomas H, Schott IM (1999a) Regreening of senescent Nicotiana leaves. I. Reappearance of NADPH-protophyllide oxidoreductase and light harvesting chlorophyll a/b-binding protein. J Exp Bot 50:1677–1682.Google Scholar
  145. Zavaleta-Mancera HA, Thomas BJ, Thomas H, Scott IM (1999b) Regreening of Nicotiana leaves. II. Redifferentiation of plastids. J Exp Bot 50:1683–1689.Google Scholar
  146. Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102:13699–13704.PubMedGoogle Scholar
  147. Zemojtel T, Frohlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P, Durner J (2006) Plant nitric oxide synthase: a never-ending story? Trends Plant Sci 11:524–525.PubMedGoogle Scholar
  148. Zentgraf U, Hinderhofer K, Kolb D (2000) Specific association of a small protein with the telomeric DNA-protein complex during the onset of leaf senescence in Arabidopsis thaliana. Plant Mol Biol 42:429–438.PubMedGoogle Scholar
  149. Zimmermann P, Heinlein C, Orendi G, Zentgraf U (2006) Senescence specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ 29:1049–1060.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Ulrike Zentgraf
    • 1
  • Vera Hemleben
    • 1
  1. 1.ZMBP, General GeneticsUniversity of TübingenTübingenGermany

Personalised recommendations