Re-evaluating the role of ascorbic acid and phenolic glycosides in ozone scavenging in the leaf apoplast of Arabidopsis thaliana L.

Plant, Cell and Environment

Volumn 35, Issue 8, 2012, Pages 1456-1466

  Booker, Fitzgerald L ^a   Burkey, Kent O ^a   Jones, Alan M ^b  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Air pollution; Flavonoids; Kaempferol; Reactive oxygen; Sinapoyl malate; Vitamin C

Indexed keywords

ASCORBIC ACID; GLYCOSIDE; OZONE; PHENOL DERIVATIVE; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT; ASCORBIC ACID; ATMOSPHERIC POLLUTION; DICOTYLEDON; GENE; OZONE; PHENOLIC COMPOUND; SCAVENGING (CHEMISTRY); SUBSTRATE;

ARABIDOPSIS; ARTICLE; BIOMASS; METABOLISM; PLANT LEAF;

ARABIDOPSIS; ASCORBIC ACID; BIOMASS; GLYCOSIDES; OZONE; PHENOLS; PLANT LEAVES; REACTIVE OXYGEN SPECIES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84863520939     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2012.02502.x     Document Type: Article

References (63)

1. Baier M., Kandlbinder A., Golldack D. & Dietz K.J. (2005) Oxidative stress and ozone: perception, signalling and response. Plant, Cell & Environment 28, 1012-1020.
2. Beltran-Heredia J., Torregrosa J., Dominzuez J.R. & Peres J.A. (2001) Kinetics of the reaction between ozone and phenolic acids present in agro-industrial wastewaters. Water Research 35, 1077-1085.
3. Benitez F.J., Beltran-Heredia J., Acero J.L. & Pinilla M.L. (1997) Ozonation kinetics of phenolic acids present in wastewaters from olive oil mills. Industrial & Engineering Chemistry Research 36, 638-644.
4. Besseau S., Hoffmann L., Geoffroy P., Lapierre C., Pollet B. & Legranda M. (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. The Plant Cell 19, 148-162.
5. Booker F., Burkey K., Morgan P., Fiscus E. & Jones A. (2012) Minimal influence of G-protein null mutations on ozone-induced changes in gene expression, foliar injury, gas exchange and peroxidase activity in Arabidopsis thaliana L. Plant, Cell & Environment 35, 668-681.
6. Booker F.L., Burkey K.O., Overmyer K. & Jones A.M. (2004) Differential responses of G-protein Arabidopsis thaliana mutants to ozone. New Phytologist 162, 633-641.
7. Bors W., Langebartels C., Michel C. & Sandermann H.J. (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28, 1589-1595.
8. Bors W., Heller W., Michel C. & Saran M. (1990) Flavonoids as antioxidants: determination of radical-scavenging efficiences. Methods in Enzymology 186, 343-355.
9. Burkey K.O. (1999) Effects of ozone on apoplast/cytoplasm partitioning of ascorbic acid in snap bean. Physiologia Plantarum 107, 188-193.
10. Burkey K.O. & Eason G. (2002) Ozone tolerance in snap bean is associated with elevated ascorbic acid in the leaf apoplast. Physiologia Plantarum 114, 387-394.
11. Burkey K.O., Eason G. & Fiscus E.L. (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiologia Plantarum 117, 51-57.
12. Burkey K.O., Neufeld H.S., Souza L., Chappelka A.H. & Davison A.W. (2006) Seasonal profiles of leaf ascorbic acid content and redox state in ozone-sensitive wildflowers. Environmental Pollution 143, 427-434.
13. Buxton G.V., Greenstock C.L., Helman W.P. & Ross A.B. (1988) Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (·OH/·O-) in aqueous solution. Journal of Physical and Chemical Reference Data 17, 513-886.
14. Castillo F.J. & Greppin H. (1988) Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure. Environmental and Experimental Botany 28, 231-2387.
15. Chameides W.L. (1989) The chemistry of ozone deposition to plant leaves: role of ascorbic acid. Environmental Science and Technology 23, 595-600.
16. 3 tolerance of two soybean cultivars. Environmental Pollution 150, 355-362.
17. Conklin P.L. & Barth C. (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant, Cell & Environment 27, 959-970.
18. Conklin P.L., Pallanca J.E., Last R.L. & Smirnoff N. (1997) L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiology 115, 1277-1285.
19. 3-responsive genes in Arabidopsis thaliana by cDNA microarray analysis. Physiologia Plantarum 128, 70-79.
20. Downs R.J. & Thomas J.F. (1983) Phytotron Procedural Manual. (Technical Bulletin 244 Ed.). North Carolina Agricultural Research Service, NC State University, Raleigh, NC, USA.
21. Eckey-Kaltenbach H., Heller W., Sonnenbichler J., Zetl I., Schäfer W., Ernst D. & Sandermann H. (1993) Oxidative stress and plant secondary metabolism: 6″-O- malonylapiin in parsley. Phytochemistry 34, 687-691.
22. Foley S., Navaratnam S., McGarvey D.J., Land E.J., Truscott T.G. & Rice-Evans C.A. (1999) Singlet oxygen quenching and the redox properties of hydroxycinnamic acids. Free Radical Biology and Medicine 26, 1202-1208.
23. Foyer C.H. & Noctor G. (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056-1071.
24. Grace S.C. (2005) Phenolics as antioxidants. In Antioxidants and Reactive Oxygen Species in Plants (ed. N. Smirnoff), pp. 141-168. Blackwell Publishing Ltd, Oxford, UK.
25. Heath R.L. (2008) Modification of the biochemical pathways of plants induced by ozone: what are the varied routes to change? Environmental Pollution 155, 453-463.
26. Kachlicki P., Einhorn J., Muth D., Kerhoas L. & Stobiecki M. (2008) Evaluation of glycosylation and malonylation patterns in flavonoid glycosides during LC/MS/MS metabolite profiling. Journal of Mass Spectrometry 43, 572-586.
27. Kollist H., Moldau H., Mortensen L., Rasmussen S.K. & Jörgensen L.B. (2000) Ozone flux to plasmalemma of barley and wheat is controlled by stomata rather than by direct reaction of ozone with cell wall ascorbate. Journal of Plant Physiology 156, 645-651.
28. Landry L.G., Chapple C.C. & Last R.L. (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiology 109, 1159-1166.
29. Langebartels C., Kerner K., Leonardi S., Schraudner M., Trost M., Heller W. & Sandermann H.J. (1991) Biochemical plant responses to ozone I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiology 95, 882-889.
30. Langebartels C., Wohlgemuth H., Kschieschan S., Grün S. & Sandermann H. (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiology and Biochemistry 40, 567-575.
31. Li J., Ou-Lee T.-M., Raba R., Amundson R.G. & Last R.L. (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell 5, 171-179.
32. Li P., Mane S.P., Sioson A.A., Robinet C.V., Heath L.S., Bohnert H.J. & Grene R. (2006) Effects of chronic ozone exposure on gene expression in Arabidopsis thaliana ecotypes and in Thellungiella halophila. Plant, Cell & Environment 29, 854-868.
33. Littell R.C., Milliken G.A., Stroup W.W. & Wolfinger R.D. (1996) SAS System for Mixed Models. SAS Institute, Inc., Cary, NC, USA.
34. Ludwikow A., Gallois P. & Sadowski J. (2004) Ozone-induced oxidative stress response in Arabidopsis: transcription profiling by microarray approach. Cellular and Molecular Biology Letters 9, 829-842.
35. Luwe M. & Heber U. (1995) Ozone detoxification in the apoplasm and symplasm of spinach, broad bean and beech leaves at ambient and elevated concentrations of ozone in air. Planta 197, 448-455.
36. Luwe M.W.F., Takahama U. & Heber U. (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves. Plant Physiology 101, 969-976.
37. Mahalingam R., Jambunathan N., Gunjan S.K., Faustin E., Weng H. & Ayoubi P. (2006) Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana. Plant, Cell & Environment 29, 1357-1371.
38. Milkowski C. & Strack D. (2010) Sinapate esters in brassicaceous plants: biochemistry, molecular biology, evolution and metabolic engineering. Planta 232, 19-35.
39. Moldau H. (1998) Hierarchy of ozone scavenging reactions in the plant cell wall. Physiologia Plantarum 104, 617-622.
40. Moldau H., Bichele I. & Hüve K. (1998) Dark-induced ascorbate deficiency in leaf cell walls increases plasmalemma injury under ozone. Planta 207, 60-66.
41. Mudd J.B. (1996) Biochemical basis for the toxicity of ozone. In Plant Response to Air Pollution (eds M. Yunus & M. Iqbal), pp. 267-283. John Wiley & Sons Ltd, Chichester, UK.
42. 3 enrichment. New Phytologist 165, 131-142.
43. Parsons H.T. & Fry S.C. (2010) Reactive oxygen species-induced release of intracellular ascorbate in plant cell-suspension cultures and evidence for pulsing of net release rate. New Phytologist 187, 332-342.
44. Pell E., Schlagnhaufer C.D. & Arteca R.N. (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiologia Plantarum 100, 264-273.
45. Pignocchi C., Fletcher J.M., Wilkinson J.E., Barnes J.D. & Foyer C.H. (2003) The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631-1641.
46. Ranieri A., D'Urso G., Nali C., Lorenzini G. & Soldatini G.F. (1996) Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. Physiologia Plantarum 97, 381-387.
47. Ranieri A., Petacco F., Castagna A. & Soldatini G.F. (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Science 159, 159-167.
48. Rao M.V. & Davis K.R. (2001) The physiology of ozone induced cell death. Planta 213, 682-690.
49. von Roepenack-Lahaye E., Degenkolb T., Zerjeski M., Franz M., Roth U., Wessjohann L., Schmidt J., Scheel D. & Clemens S. (2004) Profiling of Arabidopsis secondary metabolites by capillary liquid chromatography coupled to electrospray ionization quadrupole time-of-flight mass spectrometry. Plant Physiology 134, 548-559.
50. Ruegger M., Meyer K., Cusumano J.C. & Chapple C. (1999) Regulation of ferulate-5-hydroxylase expression in Arabidopsis in the context of sinapate ester biosynthesis. Plant Physiology 119, 101-110.
51. Sharma Y.K. & Davis K.R. (1997) The effects of ozone on antioxidant responses in plants. Free Radical Biology and Medicine 23, 480-488.
52. Speer M. & Kaiser W.M. (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiology 97, 990-997.
53. Stobiecki M., Skirycz A., Kerhoas L., Kachlicki P., Muth D., Einhorn J. & Mueller-Roeber B. (2006) Profiling of phenolic glycosidic conjugates in leaves of Arabidopsis thaliana using LC/MS. Metabolomics 2, 197-219.
54. Takahama U. (1998) Ascorbic acid-dependent regulation of redox levels of chlorogenic acid and its isomers in the apoplast of leaves of Nicotiana tabacum L. Plant and Cell Physiology 39, 681-689.
55. Takahama U. & Oniki T. (1997) A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiologia Plantarum 101, 845-852.
56. 2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytologist 172, 92-103.
57. 3-treated Arabidopsis plants. Plant, Cell & Environment 29, 1686-1702.
58. g) quenching. Journal of Photochemistry and Photobiology B: Biology 19, 205-215.
59. Veit M. & Pauli G.F. (1999) Major flavonoids from Arabidopsis thaliana leaves. Journal of Natural Products 62, 1301-1303.
60. Veljovic-Jovanovic S.D., Pignocchi C., Noctor G. & Foyer C.H. (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiology 127, 426-435.
61. Wallace G. & Fry S.C. (1994) Phenolic components of the plant cell wall. International Review of Cytology 151, 229-267.
62. Wohlgemuth H., Mittelstrass K., Kschieschan S., Bender J., Weigel H.-J., Overmyer K., Kangasjärvi J., Sandermann H.J. & Langebartels C. (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant, Cell & Environment 25, 717-726.
63. Zhao J. & Dixon R.A. (2010) The 'ins' and 'outs' of flavonoid transport. Trends in Plant Science 15, 72-80.