Drought stress has contrasting effects on antioxidant enzymes activity and phenylpropanoid biosynthesis in Fraxinus ornus leaves: An excess light stress affair?

Journal of Plant Physiology

Volumn 169, Issue 10, 2012, Pages 929-939

  Fini, Alessio ^a   Guidi, Lucia ^b   Ferrini, Francesco ^a   Brunetti, Cecilia ^a   Di Ferdinando, Martina ^a   Biricolti, Stefano ^a   Pollastri, Susanna ^a   Calamai, Luca ^a   Tattini, Massimiliano ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

Antioxidant enzymes; Drought stress; Phenylpropanoids; Violaxanthin cycle pigments; Water relations

Indexed keywords

1-PHENYLPROPANOL; ANTIOXIDANT; CARBON DIOXIDE; HYDROGEN PEROXIDE; MALONALDEHYDE; PHENYLPROPANOL; PIGMENT; PROPANOL;

ANALYSIS OF VARIANCE; ARTICLE; CYTOLOGY; DROUGHT; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; FRAXINUS; LIGHT; MESOPHYLL CELL; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PRINCIPAL COMPONENT ANALYSIS; RADIATION EXPOSURE; TIME;

ANALYSIS OF VARIANCE; ANTIOXIDANTS; CARBON DIOXIDE; DROUGHTS; FRAXINUS; HYDROGEN PEROXIDE; LIGHT; MALONDIALDEHYDE; MESOPHYLL CELLS; MICROSCOPY, FLUORESCENCE; PHOTOSYNTHESIS; PIGMENTS, BIOLOGICAL; PLANT LEAVES; PRINCIPAL COMPONENT ANALYSIS; PROPANOLS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

FRAXINUS; FRAXINUS ORNUS;

EID: 84861783930     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2012.02.014     Document Type: Article

References (93)

1. Agati G., Tattini M. Multiple functional roles of flavonoids in photoprotection. New Phytol 2010, 186:786-793.
2. Agati G., Matteini P., Goti A., Tattini M. Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol 2007, 174:77-89.
3. Agati G., Stefano G., Biricolti S., Tattini M. Mesophyll distribution of 'antioxidant' flavonoids glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance. Ann Bot 2009, 104:853-861.
4. Agati G., Biricolti S., Guidi L., Ferrini F., Fini A., Tattini M. The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J Plant Physiol 2011, 168:204-212.
5. Akhtar T.A., Lees H.A., Lampi M.A., Enstone D., Brain R.A., Greenberg B.M. Photosynthetic redox imbalance influences flavonoid biosynthesis in Lemna gibba. Plant Cell Environ 2010, 33:1205-1219.
6. Apel K., Hirt H. Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 2004, 55:373-399.
7. Bartoli C.G., Simontacchi M., Tambussi E., Beltrano J., Montaldi E., Puntarulo S. Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 1999, 50:375-383.
8. Bota J., Medrano H., Flexas J. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress?. New Phytol 2004, 162:671-681.
9. Castellarin S.D., Pfeiffer A., Sivilotti P., Degan M., Peterlunger E., Di Gaspero G. Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 2007, 30:1381-1399.
10. Chaves M.M., Flexas J., Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 2009, 103:551-560.
11. Cheeseman J.M. Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 2007, 1:4-15.
12. Close D.C., McArthur C. Rethinking the role of many plant phenolics - protection from photodamage not herbivores?. Oikos 2002, 99:166-172.
13. Demmig B., Winter K., Krüger A., Czygan F.C. Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. Plant Physiol 1988, 87:17-24.
14. Demmig-Adams B., Adams W.W. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1996, 1:21-26.
15. Du H., Wang N., Cui F., Li X., Xiao J., Xiong L. Characterization of the β-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing the xanthophylls and abscisic acid synthesis in rice. Plant Physiol 2010, 154:1304-1318.
16. Dubos C., Stracke R., Grotewold E., Weisshaar B., Martin C., Lepiniec L. MYB transcriptor factors in Arabidopsis. Trends Plant Sci 2010, 15:573-581.
17. English-Loeb G., Stout M.J., Duffey S.S. Drought stress in tomatoes: changes in plant chemistry and potential non-linear consequences for insect herbivores. Oikos 1997, 79:456-468.
18. Evans R.J., von Caemmerer S. Carbon dioxide diffusion inside leaves. Plant Physiol 1996, 110:339-346.
19. 2 affair?. J Exp Bot 2011, 62:2841-2854.
20. Fini A., Brunetti C., Di Ferdinando M., Ferrini F., Tattini M. Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 2011, 65:709-711.
21. Flexas J., Medrano H. Energy dissipation in C3 plants under drought. Funct Plant Biol 2002, 29:1209-1215.
22. 3 plants. Plant Biol 2004, 6:269-279.
23. Foyer C.H., Noctor G. Oxygen processing in photosynthesis: regulation and signalling. New Phytol 2000, 146:359-388.
24. Foyer C.H., Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 2003, 119:355-364.
25. García-Plazaola J.I., Becerril J.M. A rapid HPLC method to measure lipophylic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 1999, 10:1-7.
26. 2 in red and green leaves after mechanical injury. Plant Cell Environ 2002, 25:1261-1269.
27. Grace S.C., Logan B.A., Adams W.W. Seasonal differences in foliar content of chlorogenic acid, a phenylpropanoid antioxidant in Mahonia repens. Plant Cell Environ 1998, 21:513-521.
28. Grace S.C., Logan B.A. Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Phil Trans Royal Soc B 2000, 355:1499-1510.
29. Gratani L., Foti I. Estimating forest structure and shade tolerance of the species in a mixed deciduous broad-leaved forest in Abruzzo, Italy. Ann Bot Fenn 1998, 35:75-83.
30. Guidi L., Degl'Innocenti E., Remorini D., Massai R., Tattini M. Interaction of water stress and solar irradiance on the physiology and biochemistry of Ligustrum vulgare. Tree Physiol 2008, 28:873-883.
31. Guidi L., Degl'Innocenti E., Remorini D., Biricolti S., Fini A., Ferrini F., et al. The impact of UV-radiation on the physiology and biochemistry of Ligustrum vulgare exposed to different visible-light irradiance. Environ Exp Bot 2011, 70:86-95.
32. Hatier J.H.B., Gould K.S. Foliar anthocyanins as modulators of stress signals. J Theor Biol 2008, 253:625-627.
33. Havaux M., Tardy F. Loss of chlorophyll with limited reduction of photosynthesis as an adaptive response of Syrian barley landraces to high-light and heat stress. Aust J Plant Physiol 1999, 26:569-578.
34. Havaux M., Dall'Osto L., Bassi R. Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 2007, 145:1506-1520.
35. Hernández I., van Breusegem F. Opinion on the possible role of flavonoids as energy escape valves: novel tools for nature's Swiss army knife. Plant Sci 2010, 179:297-301.
36. Hernández J.A., Jiménez A., Mullineaux P.M., Sevilla F. Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 2000, 23:853-862.
37. Hernández I., Alegre L., Munné-Bosch S. Enhanced oxidation of flavan-3-ols and proanthocyanidin accumulation in water-stressed tea plants. Phytochemistry 2006, 67:1120-1126.
38. Hernández I., Alegre L., van Breusegem F., Munné-Bosch S. How relevant are flavonoids as antioxidants in plants?. Trends Plant Sci 2009, 14:125-132.
39. Hernández I., Algre L., Munné-Bosch S. Plant aging and excess light enhance flavan-3-ol content in Cistus clusii. J Plant Physiol 2011, 168:96-102.
40. Janz D., Behnke K., Schnitzler J.-P., Kanawati B., Schmitt-Kopplin P., Polle A. Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol 2010, 10:150.
41. Jubany-Marí T., Munné-Bosch S., López-Carbonell M., Alegre L. Hydrogen peroxide is involved in the acclimation of the Mediterranean shrub, Cistus albidus L., to summer drought. J Exp Bot 2009, 60:107-120.
42. Jubany-Marí T., Munné-Bosch S., Alegre L. Redox regulation of water stress responses in field-grown plants. Role of hydrogen peroxide and ascorbate. Plant Physiol Biochem 2010, 48:351-358.
43. Jubany-Marí T., Prielsen E., Munné-Bosch S., Alegre L. The timing of methyl jasmonate, hydrogen peroxide and ascorbate accumulation during water deficit and subsequent recovery in the Mediterranean shrub Cistus albidus L. Environ Exp Bot 2010, 69:47-55.
44. Kalefetoĝlu Macar T., Ekmekçi Y. Alterations in photochemical and physiological activities if chickpea (Cicer arietinum L.) cultivars under drought stress. J Agron Crop Sci 2009, 195:335-346.
45. Karpinski S., Reynolds H., Karpinska B., Wingle G., Greissen G., Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999, 284:654-657.
46. Keselman H.J., Algina J., Kowalchuk R.K. The analysis of repeated measure designs: a review. Br J Math Stat Psychol 2001, 54:1-20.
47. Kostova I., Iossifova T. Chemical components of Fraxinus species. Fitoterapia 2007, 78:85-106.
48. Koussevitzky S., Suzuki N., Huntington S., Arnijo I., Sha W., Cortes D., et al. Ascorbate Peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 2008, 283:34197-34203.
49. Krammer I., Beckett R.P., Wornik S., Zorn M., Pfeifhofer H.W. Revival of a resurrection plant correlates with its antioxidant status. Plant J 2003, 31:13-24.
50. Krieger-Liszkay A. Singlet oxygen production in photosynthesis. J Exp Bot 2005, 56:337-346.
51. Kyparissis A., Petropoulou Y., Manetas Y. Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L., Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. J Exp Bot 1995, 46:1825-1831.
52. Kyparissis A., Petropoulou Y., Manetas Y. Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L., Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. J Exp Bot 2000, 46:1825-1831.
53. Kyparissis A., Drilias P., Manetas Y. Seasonal fluctuations in photoprotective (xamthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Funct Plant Biol 2000, 27:265-272.
54. Kytridis V.-P., Manetas Y. Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. J Exp Bot 2006, 57:2203-2210.
55. Lee B.C., Lee S.Y., Lee H.J., Sim G.S., Kim J.H., Kim J.H., et al. Anti-oxidative and photo-protective effects of coumarins isolated from Fraxinus chinensis. Arch Pharm Res 2007, 30:1293-1301.
56. Li Z., Wakao S., Fusher B.B., Niyogi K.K. Sensing and responding to excess light stress. Annu Rev Plant Biol 2009, 50:239-260.
57. Lichtenthaler H.K. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 1987, 148:350-382.
58. Liu C., Liu Y., Guo K., Fan D., Li G., Zheng Y., et al. Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 2011, 71:174-183.
59. Logan B.A., Demmig-Adams B., Adams W.W., Grace S.C. Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. J Exp Bot 1998, 49:1869-1879.
60. Melgar J.C., Guidi L., Remorini D., Agati G., Degl'Innocenti E., Castelli S., et al. Antioxidant defences and oxidative damage in salt-treated olive plants under contrasting sunlight irradiance. Tree Physiol 2009, 29:1187-1198.
61. Mittler R., Vanderauwera S., Gollery M., van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004, 9:490-498.
62. Mullineaux P., Karpinski S. Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 2002, 5:43-48.
63. 2 and its implication to signalling. J Exp Bot 2010, 61:3577-3587.
64. Munné-Bosch S., Jubany-Marí T., Alegre L. Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant Cell Environ 2001, 24:1319-1327.
65. Niinemets Ü., Kollist H., García-Plazaola J.I., Hernández A., Becerril J.M. Do the capacity and kinetics for modification of xanthophyll cycle pool size depend on growth irradiance in temperate trees?. Plant Cell Environ 2003, 26:1787-1801.
66. 3 plants: a predominant role for photorespiration. Ann Bot 2002, 89:841-850.
67. Paul M.J., Pellny T.K. Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 2003, 54:539-547.
68. Paździoch-Czochra M., Wideńska A. Spectrofluorimetric determination of hydrogen peroxide scavenging activity. Anal Chim Acta 2002, 452:177-184.
69. Peltzer D., Polle A. Diurnal fluctuations of antioxidative systems in leaves of field-grown beech trees (Fagus sylvatica): responses to light and temperature. Physiol Plant 2001, 111:158-164.
70. Peltzer D., Dreyer E., Polle A. Differential temperature dependencies of antioxidant enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiol Biochem 2002, 40:141-150.
71. Pérez-Bueno M.L., Horton P. The role of lutein in the acclimation of higher plant chloroplast membrane to suboptimal conditions. Physiol Plant 2008, 134:227-236.
72. Pérez-Rodríguez E., Aguilera J., Figueroa F.L. Tissular localization of coumarins in the green alga Dasycladus vermicularis (Scopoli) Krasser: a photoprotective role?. J Exp Bot 2003, 54:1093-1100.
73. Pollastri S., Tattini M. Flavonols: old compounds for old roles. Ann Bot 2011, 108:1225-1233.
74. Polle A. Dissecting the superoxide dismutase-ascorbate-peroxidase-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 2001, 126:445-462.
75. Ren J., Dai W., Xuan Z., Yao Y., Korpelainen H., Li C. The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species. Forest Ecol Manag 2007, 239:112-119.
76. Sakihama Y., Mano J., Sano S., Asada K., Yamasaki H. Reduction of phenoxyl radicals mediated by monodehydroascorbate reductase. Biochem Biophys Res Commun 2000, 279:949-954.
77. 2 concentrations. J Exp Bot 2001, 52:133-143.
78. Schreiber U., Bilger W., Neubaer C. Chlorophyll fluorescence as a non-intruder indicator of rapid assessment of in vivo photosynthesis. Ecophysiology of photosynthesis 1995, 49-70. Springer Verlag, Berlin. E.D. Schulze, M.M. Caldwell (Eds.).
79. Sharma P., Dubey R.S. Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectants. J Plant Physiol 2005, 16:854-864.
80. Smirnoff N. Plant resistance to environmental stresses. Curr Opin Plant Biol 1998, 9:214-219.
81. Street N.R., Skogström O., Sjödin A., Tucker A., Rodríguez-Acosta M., Nilsson P., et al. The genetics and genomics of the drought response in Populus. Plant J 2006, 48:321-341.
82. Tattini M., Galardi C., Pinelli P., Massai R., Remorini D., Agati G. Differential accumulation of flavonoids and hydroxycinnmates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol 2004, 163:547-561.
83. Tattini M., Guidi L., Morassi-Bonzi L., Pinelli P., Remorini D., Degl'Innocenti E., et al. On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytol 2005, 167:457-470.
84. Tattini M., Remorini D., Pinelli P., Agati G., Saracini E., Traversi M.L., et al. Morpho-anatomical and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytol 2006, 170:779-794.
85. Taylor L.P., Grotewold E. Flavonoids as developmental regulators. Curr Opin Plant Biol 2005, 8:317-323.
86. Triantaphylidés C., Krischke M., Hoeberichts F.A., Ksad B., Gresser G., Havaux M., et al. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 2008, 148:960-968.
87. 2 and is indispensable for stress defence in C3 plants. EMBO J 1997, 16:4806-4816.
88. Walia H., Wilson C., Condamine P., Liu X., Ismail A.M., Zeng L., et al. Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 2005, 139:822-835.
89. Wang R., Chen S., Zhou X., Shen X., Deng L., Zhu H., et al. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol 2008, 28:947-957.
90. Wolf L., Rizzini L., Stracke R., Ulm R., Rensing S.A. The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol 2010, 153:1123-1134.
91. Zechmann B., Stumpe M., Mauch Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta 2011, 233:1-12.
92. Zhou Y., Lam H.M., Zhang J. Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot 2007, 58:1207-1217.
93. Zhu J.J., Zhang J.L., Liu H.C., Cao K.F. Photosynthesis, non-photochemical pathways and activities of antioxidant enzymes in a resilient evergreen oak under different climatic conditions from a valley-savanna in Southwest China. Physiol Plant 2009, 135:62-72.