Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: Similar but different

Plant Physiology

Volumn 171, Issue 3, 2016, Pages 1560-1568

  Rogers, Hilary ^a   Munné Bosch, Sergi ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE;

CELL AGING; CYTOLOGY; FLOWER; METABOLISM; OXIDATION REDUCTION REACTION; PLANT CELL; PLANT LEAF; SIGNAL TRANSDUCTION;

CELL AGING; FLOWERS; OXIDATION-REDUCTION; PLANT CELLS; PLANT LEAVES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84977525417     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00163     Document Type: Article

References (92)

1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399
2. Aros D, Gonzalez V, Allemann RK, Müller CT, Rosati C, Rogers HJ (2012) Volatile emissions of scented Alstroemeria genotypes are dominated by terpenes, and a myrcene synthase gene is highly expressed in scented Alstroemeria flowers. J Exp Bot 63: 2739-2752
3. Arrom L, Munné-Bosch S (2010) Tocopherol composition in flower organs of Lilium and its variations during natural and artificial senescence. Plant Sci 179: 289-295
4. Arrom L, Munné-Bosch S (2012) Hormonal changes during flower development in floral tissues of Lilium. Planta 236: 343-354
5. 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
6. Bieker S, Riester L, Stahl M, Franzaring J, Zentgraf U (2012) Senescencespecific alteration of hydrogen peroxide levels in Arabidopsis thaliana and oilseed rape spring variety Brassica napus L. cv. Mozart. J Integr Plant Biol 54: 540-554
7. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23: 873-894
8. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48: 181-199
9. Caliandro R, Nagel KA, Kastenholz B, Bassi R, Li Z, Niyogi KK, Pogson BJ, Schurr U, Matsubara S (2013) Effects of altered α-and β-branch carotenoid biosynthesis on photoprotection and whole-plant acclimation of Arabidopsis to photo-oxidative stress. Plant Cell Environ 36: 438-453
10. Cavaiuolo M, Cocetta G, Ferrante A (2013) The antioxidants changes in ornamental flowers during development and senescence. Antioxidants (Basel) 2: 132-155
11. Chakrabarty D, Chatterjee J, Datta SK (2007) Oxidative stress and antioxidant activity as the basis of senescence in chrysanthemum florets. Plant Growth Regul 53: 107-115
12. Chapin LJ, Jones M (2007) Nutrient remobilization during pollinationinduced corolla senescence in Petunia. Acta Hortic 755: 181-190
13. Chapin LJ, Jones ML (2009) Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. J Exp Bot 60: 2179-2190
14. 2+-dependent scavenging system. Plant J 62: 760-772
15. Dat J, Vandenabeele S, Vranová E, VanMontagu M, InzéD, Van BreusegemF (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57: 779-795
16. 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 gene network of Arabidopsis. Plant Cell 17: 268-281
17. Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15: 1129-1159
18. Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65: 3783-3798
19. Droillard MJ, Paulin A (1990) Isozymes of superoxide dismutase in mitochondria and peroxisomes isolated from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiol 94: 1187-1192
20. Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61: 1549-1566
21. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17: 1866-1875
22. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155: 2-18
23. Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18: 2087-2090
24. Friedman WE, Moore RC, Purugganan MD (2004) The evolution of plant development. Am J Bot 91: 1726-1741
25. Fukuchi-Mizutani M, Ishiguro K, Nakayama T, Utsunomiya Y, Tanaka Y, Kusumi T, Ueda T (2000) Molecular and functional characterization of a rose lipoxygenase cDNA related to flower senescence. Plant Sci 160: 129-137
26. Gan S, Fischer AM (2007) Nutrient remobilization during leaf senescence. In S Gan, ed, Senescence Processes in Plants. Annual Plant Reviews, Vol 26. Blackwell Publishing, Oxford, pp 87-107
27. García-Plazaola JI, Hernández A, Becerril JM (2003) Antioxidant and pigment composition during autumnal leaf senescence in woody deciduous species differing in their ecological traits. Plant Biol 5: 557-566
28. Garmier M, Carroll AJ, Delannoy E, Vallet C, Day DA, Small ID, Millar AH (2008) Complex I dysfunction redirects cellular and mitochondrial metabolism in Arabidopsis. Plant Physiol 148: 1324-1341
29. Gechev TS, Minkov IN, Hille J (2005) Hydrogen peroxide-induced cell death in Arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 57: 181-188
30. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, et al (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147: 595-610
31. Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C R Biol 333: 382-391
32. Guo Y, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27: 521-549
33. Guo Y, Gan SS (2012) Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments. Plant Cell Environ 35: 644-655
34. Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17: 3451-3469
35. Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 158: 1317-1323
36. Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57: 55-77
37. Hunter DA, Ferrante A, Vernieri P, Reid MS (2004) Role of abscisic acid in perianth senescence of daffodil (Narcissus pseudonarcissus "Dutch Master"). Physiol Plant 121: 313-321
38. Ishida H, Izumi M, Wada S, Makino A (2014) Roles of autophagy in chloroplast recycling. Biochim Biophys Acta 1837: 512-521
39. Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants 4: 393-411
40. Jones ML (2013) Mineral nutrient remobilization during corolla senescence in ethylene-sensitive and-insensitive flowers. AoB Plants 5: plt023
41. Jones ML, Woodson WR (1997) Pollination-induced ethylene in carnation: role of stylar ethylene in corolla senescence. Plant Physiol 115: 205-212
42. Juvany M, Müller M, Munné-Bosch S (2012) Leaves of field-grown mastic trees suffer oxidative stress at the two extremes of their lifespan. J Integr Plant Biol 54: 584-594
43. Juvany M, Müller M, Munné-Bosch S (2013) Photo-oxidative stress in emerging and senescing leaves: a mirror image? J Exp Bot 64: 3087-3098
44. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56: 337-346
45. Leszczyszyn OI, Imam HT, Blindauer CA (2013) Diversity and distribution of plant metallothioneins: a review of structure, properties and functions. Metallomics 5: 1146-1169
46. Leverentz MK, Wagstaff C, Rogers HJ, Stead AD, Chanasut U, Silkowski H, Thomas B, Weichert H, Feussner I, Griffiths G (2002) Characterization of a novel lipoxygenase-independent senescence mechanism in Alstroemeria peruviana floral tissue. Plant Physiol 130: 273-283
47. Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63: 215-237
48. Ljubesić N, Wrischer M, Devidé Z (1991) Chromoplasts: the last stages in plastid development. Int J Dev Biol 35: 251-258
49. Marano MR, Serra EC, Orellano EG, Carrrillo N (1993) The path of chromoplast development in fruits and flowers. Plant Sci 94: 1-17
50. 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
51. Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M, Van Breusegem F, Kangasjärvi J (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot http://dx.doi.org/10.1093/jxb/erw080
52. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33: 453-467
53. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498
54. Munné-Bosch S, Alegre L (2002) The function of tocopherols and toctrienols in plants. Crit Rev Plant Sci 21: 31-57
55. Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31: 203-213
56. Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161: 5-19
57. Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río LA (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57: 1747-1758
58. Panavas T, Rubinstein B (1998) Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Sci 133: 125-138
59. Penfold CA, Buchanan-Wollaston V (2014) Modelling transcriptional networks in leaf senescence. J Exp Bot 65: 3859-3873
60. Pintó-Marijuan M, Munné-Bosch S (2014) Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. J Exp Bot 65: 3845-3857
61. Price AM, Aros Orellana DF, Salleh FM, Stevens R, Acock R, Buchanan-Wollaston V, Stead AD, Rogers HJ (2008) A comparison of leaf and petal senescence in wallflower reveals common and distinct patterns of gene expression and physiology. Plant Physiol 147: 1898-1912
62. Prochazkova D, Sairam RK, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Sci 161: 765-771
63. 2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ 34: 21-32
64. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species: contribution to oxidative stress and interorganellar signaling. Plant Physiol 141: 357-366
65. Rogers HJ (2012) Is there an important role for reactive oxygen species and redox regulation during floral senescence? Plant Cell Environ 35: 217-233
66. Rogers HJ (2013) From models to ornamentals: how is flower senescence regulated? Plant Mol Biol 82: 563-574
67. Rosenwasser S, Fluhr R, Joshi JR, Leviatan N, Sela N, Hetzroni A, Friedman H (2013) ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiol 163: 1071-1083
68. Rosenwasser S, Rot I, Sollner E, Meyer AJ, Smith Y, Leviatan N, Fluhr R, Friedman H (2011) Organelles contribute differentially to reactive oxygen species-related events during extended darkness. Plant Physiol 156: 185-201
69. Rubinstein B (2000) Regulation of cell death in flower petals. Plant Mol Biol 44: 303-318
70. Shaikhali J, Norén L, de Dios Barajas-López J, Srivastava V, König J, Sauer UH, Wingsle G, Dietz KJ, Strand Å (2012) Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J Biol Chem 287: 27510-27525
71. Smykowski A, Zimmermann P, Zentgraf U (2010) G-box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol 153: 1321-1331
72. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2: 755-767
73. Stead AD, van Doorn WG (1994) Strategies of flower senescence: a review. In RJ Scott, AD Stead, eds, Molecular and Cellular Aspects of Plant Reproduction. Cambridge University Press, Cambridge, UK, pp 215-238
74. Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytol 197: 696-711
75. Thomas H, Ougham HJ, Wagstaff C, Stead AD (2003) Defining senescence and death. J Exp Bot 54: 1127-1132
76. Thompson JE, Froese CD, Madey E, Smith MD, Hong Y (1998) Lipid metabolism during plant senescence. Prog Lipid Res 37: 119-141
77. 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
78. van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, et al (2011) Morphological classification of plant cell deaths. Cell Death Differ 18: 1241-1246
79. van Doorn WG, Çelikel FG, Pak C, Harkema H (2013) Delay of iris flower senescence by cytokinins and jasmonates. Physiol Plant 148: 105-120
80. van Doorn WG, Woltering EJ (2004) Senescence and programmed cell death: substance or semantics? J Exp Bot 55: 2147-2153
81. Verlinden S (2003) Changes in the mineral nutrient concentrations in petunia corollas during development and senescence. HortScience 38: 71-74
82. Wagstaff C, Bramke I, Breeze E, Thornber S, Harrison L, Thomas B, Buchanan-Wollaston V, Stead AD, Rogers HJ (2010) A specific group of genes respond to cold dehydration stress in cut Alstroemeria flowers whereas ambient dehydration stress accelerates developmental senescence expression patterns. J Exp Bot 61: 2905-2921
83. Wagstaff C, Malcolm P, Rafiq A, Leverentz M, Griffiths G, Thomas B (2003) Programmed cell death (PCD) processes begin extremely early in Alstroemeria petal senescence. New Phytol 160: 49-59
84. Wagstaff C, Yang TJW, Stead AD, Buchanan-Wollaston V, Roberts JA (2009) A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. Plant J 57: 690-705
85. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718
86. Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munné-Bosch S, Antonio C, Tohge T, et al (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24: 482-506
87. Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20: 264-265
88. Ye Z, Rodríguez R, Tran A, Hoang H, de los Santos D, 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
89. Zavaleta-Mancera HA, Franklin KA, Ougham HJ, Thomas H, Scott IM (1999a) Regreening of senescent Nicotiana leaves. I. Reappearance of NADPH-protochlorophyllide oxidoreductase and light-harvesting chlorophyll a/b-binding protein. J Exp Bot 50: 1677-1682
90. Zavaleta-Mancera HA, Franklin KA, Ougham HJ, Thomas H, Scott IM (1999b) Regreening of senescent Nicotiana leaves. II. Redifferentiation of plastids. J Exp Bot 50: 1683-1689
91. Zechmann B (2014) Compartment-specific importance of glutathione during abiotic and biotic stress. Front Plant Sci 5: 566
92. Zhang Y, Guo WM, Chen SM, Han L, Li ZM (2007) The role of N-lauroylethanolamine in the regulation of senescence of cut carnations (Dianthus caryophyllus). J Plant Physiol 164: 993-1001