Mechanisms of ozone tolerance in rice: Characterization of two QTLs affecting leaf bronzing by gene expression profiling and biochemical analyses

Journal of Experimental Botany

Volumn 61, Issue 5, 2010, Pages 1405-1417

  Frei, Michael ^a   Tanaka, Juan Pariasca ^a   Chen, Charles P ^a   Wissuwa, Matthias ^a  

^a JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

Author keywords

Antioxidants; Ascorbate oxidase; Ascorbic acid; Global change; Microarray; Oryza sativa; Oxidative stress; Tolerance breeding

Indexed keywords

ANTIOXIDANT; OZONE; REACTIVE OXYGEN METABOLITE;

ARTICLE; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE;

ANTIOXIDANTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA SATIVA; OZONE; PHOTOSYNTHESIS; QUANTITATIVE TRAIT LOCI; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ORYZA SATIVA;

EID: 77949374839     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq007     Document Type: Article

References (51)

1. Ainsworth EA. 2008. Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biology 14, 1642-1650.
2. Altschul SF, Gish W, Miller W, Myers EW, David JL. 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403-410.
3. Badrakhan CD, Petrat F, Holzhauser M, Fuchs A, Lomonosova EE, de Groot H, Kirsch M. 2004. The methanol method for the quantification of ascorbic acid and dehydroascorbic acid in biological samples. Journal of Biochemical and Biophysical Methods 58, 207-218.
4. Baier M, Kandlbinder A, Golldack D, Dietz KJ. 2005. Oxidative stress and ozone: perception, signaling and response. Plant, Cell and Environment 28, 1012-1020.
5. Battisti DS, Naylor RL. 2009. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240-244.
6. Blokhina O, Virolainen E, Fagerstedt KV. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179-194.
7. Burkey KO, Wei C, Eason G, Ghosh P, Fenner GP. 2000. Antioxidant metabolite levels in ozone sensitive and tolerant genotypes of snap bean. Physiologia Plantarum 110, 195-200.
8. Cho K, Shibato J, Agrawal GK, et al. 2008. Integrated transcriptomics, proteomics, and metabolomics analysis to survey ozone response in the leaves of rice seedlings. Journal of Proteome Research 7, 2980-2998.
9. Conklin PL, 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 and Environment 27, 959-970.
10. DellaPenna D, Pogson BJ. 2006. Vitamin synthesis in plants: tocopherols and carotenoids. Annual Review of Plant Biology 57, 711-738.
11. Dowdle J, Ishikawa T, Gatzek SP, Rolinski S, Smirnoff N. 2007. Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. The Plant Journal 52, 673-689.
12. Eltayeb AM, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K. 2007. Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225, 1255-1264.
13. Fiscus EL, Booker FL, Burkey KO. 2005. Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant, Cell and Environment 28, 997-1011.
14. Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21-25.
15. Frei M, Tanaka JP, Wissuwa M. 2008. Genotypic variation in tolerance to elevated ozone in rice: dissection of distinct genetic factors linked to tolerance mechanisms. Journal of Experimental Botany 59, 3741-3752.
16. Gibson G, Wolfinger R. 2004. Gene expression profiling using mixed models. In: Saxton AM, Balzarni MG, Cappio-Borlino A, eds. Genetic analysis of complex traits using SAS. Cary, NC: SAS Press, 252-277.
17. Griffith OW. 1980. Determination of glutathione disulfide using glutathione reductase and 2-vinylpyridine. Analytical Biochemistry 106, 207-212.
18. Hayashi K, Hiradate S, Ishikawa S, Nouchi I. 2008. Ammonia exchange between rice leaf blades and the atmosphere: effect of broadcast urea and changes in xylem sap and leaf apoplastic ammonium concentrations. Soil Science and Plant Nutrition 54, 807-818.
19. Hossain MA, Asada K. 1984. Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant and Cell Physiology 25, 85-92.
20. Hossain MA, Nakano Y, Asada K. 1984. Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology 25, 385-395.
21. Hoen PAC, Turk R, Boer JM, Sterrenburg E, de Menezes RX, van Ommen GJB, den Dunnen JT. 2004. Intensity-based analysis of two color microarrays enables efficient and flexible hybridization designs. Nucleic Acids Research 32, e41.
22. Inada H, Yamagichi M, Satoh R, Hoshino D, Nagasawa A, Negishi Y, Nouichi I, Kobayashi K, Izuta T. 2008. Effects of ozone on photosynthetic components and radical scavenging systems in leaves of rice (Oryza sativa L.) Journal of Agricultural Meteorology 64, 243-255
23. Kangasjä rvi J, Jaspers P, Kollist H. 2005. Signalling and cell death in ozone-exposed plants. Plant, Cell and Environment 28, 1021-1036.
24. Kim BR, Nam HY, Kim SU, Kim SI, Chang YI. 2003. Normalization of reverse transcription quantitative-PCR with housekeeping genes in rice. Biotechnology Letters 25, 1869-1872.
25. Leaky ADB, Ainsworth EA, Bernard SM, et al. 2009. Gene expression profiling: opening the black box of plant ecosystem response to global change. Global Change Biology 15, 1201-1213.
26. Li P, Mane SP, Sioson AA, Robinet CV, Heath LS, Bohnert H, Grene R. 2006. Effects of chronic ozone exposure on gene expression in Arabidopsis thaliana ecotypes and in Thellungiella halophila. Plant, Cell and Environment 29, 854-868.
27. Long SP, Ainsworth EA, Leakey ADB, Morgan PB. 2005. Global food insecurity. Treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields. Philosophical Transactions of the Royal Society B: Biological Science 360, 2011-2020.
28. Lowry OH, Passonneau JV. 1972. A collection of metabolite assays. In: A flexible system of enzymatic analyses. New York: Academic Press, 146-222.
29. Ludwikow A, Gallois P, Sadawski J. 2004. Ozone induced stress response in Arabidopsis thaliana: transcription profiling by microarray approach. Cellular and Molecular Biology Letters 9, 829-842.
30. Mahalingam R, Jambunathan N, Gunjan SK, Faustin E, Weng H, Ayoubi P. 2006. Analysis of oxidative signaling induced by ozone in Arabidopsis thaliana. Plant, Cell and Environment 29, 1357-1371.
31. Marrs KA. 1996. The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 127-158.
32. 3. Field Crops Research 90, 47-59.
33. Nakano Y, Asada K. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867-880.
34. Noctor G, Arisi A, Jouanin L, Kunert K, Rennenberg H, Foyer C. 1998. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. Journal of Experimental Botany 49, 623-647.
35. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
36. Pang J, Kobayashi K, Zhu J. 2009. Yield and photosynthetic characteristics of flaf leaves in Chinese rice (Oryza sativa L.) varieties subjected to free-air release of ozone. Agriculture Ecosystems and Environment 132, 203-211.
37. Pariasca-Tanaka J, Satoh K, Rose T, Mauleon R, Wissuwa M. 2009. Stress response versus stress tolerance: a transcriptome analysis of two rice lines contrasting in tolerance to phosphorus deficiency. Rice 2, 167-185.
38. Pignocchi C, Fletcher JM, Wilkonson JE, Barnes JD, Foyer C. 2003. The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631-1641.
39. Rao MV, Davis KR. 2001. The physiology of ozone induced cell death. Planta 213, 682-690.
40. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologists. Methods in Molecular Biology 132, 365-386
41. stcentury: future trends, impacts and policy implications. Science Policy Report 15/08. The Royal Society, London.
42. Sanmartin M, Drogoudi PD, Lyons T, Pateraki I, Barnes J, Kanellis AK. 2003. Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216, 918-928.
43. Schmidhuber J, Tubiello FN. 2007. Global food security under climate change. Proceedings of the National Academy of Sciences, USA 104, 19703-19708.
44. Sharma YK, Leon J, Raskin I, Davis KR. 1996. Ozone induced response in Arabidopsis thaliana: the role os salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proceedings of the National Academy of Sciences, USA 93, 5099-5104.
45. Shi G, Yang L, Wang Y, Kobayashi K, Zhu J, Tang H, Pan S, Chen T, Liu G, Wang Y. 2009. Impact of elevated ozone concentration on yield of four Chinese rice cultivars under open air field condition. Agriculture Ecosystems and Environment 131, 178-184.
46. Tosti N, Pasqualini S, Borgogni A, Ederli L, Falistocco E, Crispi S, Paolocci F. 2006. Gene expression profiles of O-3-treated Arabidopsis plants. Plant, Cell and Environment 29, 1686-1702.
47. Van Camp W, Willekens H, Bowler C, van Montagu M, Inze D, Reupold-Popp P, Sandermann H, Langebartels C. 1994. Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. Nature Biotechnology 12, 165-168.
48. Wheeler GL, Jones MA, Smirnoff N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393, 365-369.
49. Winkel-Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218-223.
50. Wissuwa M, Ismail A, Yanagihara S. 2006. Effects of zinc deficiency on rice growth and genetic factors contributing to tolerance. Plant Physiology 142, 731-741.
51. Yamamoto A, Bhuiyan NHB, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Tababe T. 2005. Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. Journal of Experimental Botany 56, 1785-1796.