Mutation of Arabidopsis HY1 causes UV-C hypersensitivity by impairing carotenoid and flavonoid biosynthesis and the down-regulation of antioxidant defence

Journal of Experimental Botany

Volumn 63, Issue 10, 2012, Pages 3869-3884

  Xie, Yanjie ^a   Xu, Daokun ^a   Cui, Weiti ^a   Shen, Wenbiao ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Antioxidant defences; Arabidopsis; carotenoid; flavonoid; hy1; UV C hypersensitivity

Indexed keywords

ANTIOXIDANT; ARABIDOPSIS PROTEIN; CAROTENOID; CHLOROPHYLL; FLAVONOID; HEME OXYGENASE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; DOWN REGULATION; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; OXIDATIVE STRESS; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

ANTIOXIDANTS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOSYNTHETIC PATHWAYS; CAROTENOIDS; CHLOROPHYLL; DOWN-REGULATION; FLAVONOIDS; HEME OXYGENASE (DECYCLIZING); MUTATION; OXIDATIVE STRESS; ULTRAVIOLET RAYS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; GLYCINE MAX;

EID: 84863671572     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers078     Document Type: Article

References (70)

1. Applegate LA, Luscher P, Tyrrell RM. 1991. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Research 51, 974-978.
2. Balestrazzi A, Locato V, Bottone MG, Gara LD, Biggiogera M, Pellicciari C, Botti S, Gesù D, Donà M, Carbonera D. 2009. Response to UV-C radiation in topo I-deficient carrot cells with low ascorbate levels. Journal of Experimental Botany 61, 575-585.
3. Bartley GE, Scolnik DA. 1995. Plant carotenoids: pigments for photoprotection, visual attraction, and human health. The Plant Cell 7, 1027-1038.
4. Bashandy T, Taconnat L, Renou JP, Meyer Y, Reichheld JP. 2009. Accumulation of flavonoids in an ntra ntrb mutant leads to tolerance to UV-C. Molecular Plant 2, 249-258.
5. Bauer M, Huse K, Settmacher U, Claus RA. 2008. The heme oxygenase-carbon monoxide system: regulation and role in stress response and organ failure. Intensive Care Medicine 34, 640-648.
6. Bieza K, Lois R. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiology 126, 1105-1115.
7. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. 2008. Heme oxygenase and carbon monoxide initiate homeostatic signaling. Journal of Molecular Medicine 86, 267-279.
8. Bin Alam MDZ, Otaki M, Furumai H, Ohgaki S. 2001. Direct and indirect inactivation of Microcystis aeruginosa by UV-radiation. Water Research 35, 1008-1014.
9. Booij-James IS, Dube SK, Jansen MA, Edelman M, Mattoo AK. 2000. Ultraviolet-B radiation impacts light-mediated turnover of the photosystem II reaction center heterodimer in Arabidopsis mutants altered in phenolic metabolism. Plant Physiology 124, 1275-1284.
10. Buer CS, Imin N, Djordjevic MA. 2010. Flavonoids: new roles for old molecules. Journal of Integrative Plant Biology 52, 98-111.
11. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP. 2010. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxidants and Redox Signaling 13, 1763-1811.
12. Cao ZY, Geng BB, Xu S, Xuan W, Nie L, Shen WB, Liang YC, Guan RZ. 2011. BnHO1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. Journal of Experimental Botany 62, 4675-4689.
13. Cao ZY, Huang BK, Wang QY, Xuan W, Ling TF, Zhang B, Chen X, Shen WB. 2007. Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chinese Science Bulletin 52, 2365-2373.
14. Castells E, Molinier J, Drevensek S, Genschik P, Barneche F, Bowler C. 2010. Det1-1-induced UV-C hyposensitivity through UVR3 and PHR1 photolyase gene over-expression. The Plant Journal 63, 392-404.
15. Chary P, Dillon D, Schroeder AL, Natvig DO. 1994. Superoxide dismutase (sod-1) null mutants of Neurospora crassa: oxidative stress sensitivity, spontaneous mutation rate and response to mutagens. Genetics 137, 723-730.
16. Close DC, MuArthur C, Hagerman AE, Davies NW, Beadle CL. 2007. Phenolic acclimation to ultraviolet-A irradiation in Eucalyptus nitens seedlings raised across a nutrient environment gradient. Photosynthetica 45, 36-42.
17. Cornah JE, Terry MJ, Smith AG. 2003. Green or red: what stops the traffic in the tetrapyrrole pathway. Trends in Plant Science 8, 224-230.
18. Dai M, Hu Y, Zhao Y, Liu H, Zhou D. 2007. A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiology 144, 380-390.
19. Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD. 2001. The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiology 126, 656-669.
20. Desmard M, Foresti R, Daqoussat M, et al. 2012. Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules. Antioxidants and Redox Signaling 16, 153-163.
21. Filkowski J, Kovalchuk O, Kovalchuk I. 2004. Genome stability of vtc1, tt4, and tt5 Arabidopsis thaliana mutants impaired in protection against oxidative stress. The Plant Journal 38, 60-69.
22. Frohnmeyer H, Staiger D. 2003. Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiology 133, 1420-1428.
23. Gao CJ, Xing D, Li LL, Zhang LR. 2008. Implication of reactive oxygen species and mitochondrial dysfunction in the early stages of plant programmed cell death induced by ultraviolet-C overexposure. Planta 227, 755-767.
24. Gao Q, Zhang LX. 2008. Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana. Journal of Plant Physiology 165, 138-148.
25. García-Arnandis I, Guillé n MI, Gomar F, Casteión MA, Alcaraz MJ. 2011. Control of cell migration and inflammatory mediators production by CORM-2 in osteoarthritic synoviocytes. PLoS One 6, e24591.
26. Gisk B, Yasui Y, Kohchi T, Frankenberg-Dinkel N. 2010. Characterization of the haem oxygenase protein family in Arabidopsis thaliana reveals a diversity of functions. Biochemical Journal 425, 425-434.
27. Han Y, Zhang J, Chen XY, Gao ZZ, Xuan W, Xu S, Ding X, Shen WB. 2008. Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa. New Phytologist 177, 155-166.
28. Havaux M, Kloppstech K. 2001. The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npg and tt mutants. Planta 213, 953-966.
29. 2 in Arabidopsis. Journal of Biological Chemistry 283, 774-783.
30. Kazan K, Manners JM. 2011. The interplay between light and jasmonate signaling during defence and development. Journal of Experimental Botany 62, 4087-4100.
31. Kim YM, Pae HO, Park JE, Lee YC, Woo JM, Kim NH, Choi YK, Lee BS, Kim SR, Chung HT. 2011. Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxidants and Redox Signaling 14, 137-167.
32. Kirchgeßner HD, Reichert K, Hauff K, Steinbrecher R, Schnitzler JP, Pfündel EE. 2003. Light and temperature, but not UV radiation, affect chlorophylls and carotenoids in Norway spruce needles (Picea abies (L.) Karst.). Plant, Cell and Environment 26, 1169-1179.
33. Landry LG, Chapple CC, Last RL. 1995. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiology 109, 1159-1166.
34. Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. 2002. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. The Plant Cell 14, 2627-2641.
35. Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL. 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell 5, 171-179.
36. Lichtenthaler HK. 1987. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350-382.
37. Liu C, Cai L, Han X, Ying T. 2011. Temporary effect of postharvest UV-C irradiation on gene expression profile in tomato fruit. Gene 486, 56-64.
38. Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, Dulak J. 2008. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxidants and Redox Signaling 10, 1767-1812.
39. Matsumoto F, Obayashi T, Sasaki-Sekimoto Y, Ohta H, Takamiya K, Masuda T. 2004. Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiology 135, 2379-2391.
40. Mayfield SP, Taylor WC. 1984. Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. European Journal of Biochemistry 144, 79-84.
41. Moliné M, Libkind D, Dié guez Mdel C, van Broock M. 2009. Photoprotective role of carotenoids in yeast: response to UV-B of pigmented and naturally-occurring albino strains. Journal of Photochemistry and Photobiology. B, Biology 95, 156-161.
42. Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM. 1999. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of mutation in a plastid heme oxygenase. The Plant Cell 11, 335-348.
43. Noriega GO, Balestrasse KB, Batlle A, Tomaro ML. 2004. Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochemical and Biophysical Research Communications 323, 1003-1008.
44. Oravecz A, Baumann A, Máté Z, Brzezinska A, Molinier J, Oakeley EJ, Adám E, Schäfer E, Nagy F, Ulm R. 2006. CONSTITUTIVELY PHOTOMORPHOGENICI is required for the UV-B response in Arabidopsis. The Plant Cell 18, 1975-1990.
45. Otterbein LE, Soares MP, Yamashita K, Bach FH. 2003. Heme oxygenase-1: unleashing the protective properties of heme. Trends in Immunology 24, 449-455.
46. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. 2010. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochemical Pharmacology 80, 1895-1903.
47. Prawan A, Kundu JK, Surh YJ. 2005. Molecular basis of heme oxygenase-1 induction: implications for chemoprevention and chemoprotection. Antioxidants and Redox Signaling 7, 1688-1703.
48. Qin G, Gu HY, Ma LG, Peng YB, Deng XW, Chen ZL, Qu LJ. 2007. Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Research 17, 471-482.
49. Ramsay NA, Glover BJ. 2005. MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in Plant Science 10, 63-70.
50. Renzing J, Hansen S, Lane DP. 1996. Oxidative stress is involved in the UV activation of p53. Journal of Cell Science 109, 1105-1112.
51. Sakai H, Katayama H, Oguma K, Ohgaki S. 2009. Kinetics of Microcystis aeruginosa growth and intracellular microcystins release after UV irradiation. Environmental Science and Technology 43, 896-901.
52. Santa-Cruz DM, Pacienza NA, Polizio AH, Balestrasse KB, Tomaro ML, Yannarelli GG. 2010. Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants. Phytochemistry 71, 1700-1707.
53. Saxena SC, Joshi PK, Grimm B, Arora S. 2011. Alleviation of ultraviolet-C-induced oxidative damage through overexpression of cytosolic ascobate peroxidase. Biologia 66, 1052-1059.
54. 2+ transporters mediate virus-induced acquired resistance to oxidative stress. Plant, Cell and Environment 34, 406-417.
55. Shekhawat GS, Verma K. 2010. Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. Journal of Experimental Botany 61, 2255-2270.
56. Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R. 2010. The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell and Environment 33, 88-103.
57. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. The Plant Journal 50, 660-677.
58. Suttner DM, Dennery PA. 1999. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB Journal 13, 1800-1809.
59. Tao Y, Zhang XH, Au DW, Mao X, Yuan K. 2010. The effects of sub-lethal UV-C irradiation on growth and cell integrity of cyanobacteria and green algae. Chemosphere 78, 541-547.
60. Terry MJ, Kendrick RE. 1999. Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore deficient aurea and yellow-green-2 mutants of tomato. Plant Physiology 119, 143-152.
61. Tossi V, Amenta M, Lamattina L, Cassia R. 2011. Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant, Cell and Environment 34, 909-921.
62. USEPA. 2006. Ultraviolet disinfection guidance manual for the final long term 2 enhanced surface water treatment rule. Appendix C, 1-12. http://www.epa.gov/safewater/disinfection/It2/compliance.html.
63. von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, Kleinig H. 1997. Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. The Plant Journal 12, 625-634.
64. Wu MZ, Huang JJ, Xu S, Ling TF, Xie YJ, Shen WB. 2011. Haem oxygenase delays programmed cell death in wheat aleurone layers by modulation of hydrogen peroxide metabolism. Journal of Experimental Botany 62, 235-248.
65. Xie YJ, Cui WT, Yuan XX, Shen WB, Yang Q. 2011a. Heme oxygenase-1 is associated with wheat salinity acclimation by modulating reactive oxygen species homeostasis. Journal of Integrative Plant Biology 53, 653-670.
66. Xie YJ, Ling TF, Han Y, et al. 2008. Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant, Cell and Environment 31, 1864-1881.
67. Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB. 2011b. Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohDderived reactive oxygen species synthesis. The Plant Journal 66, 280-292.
68. Xu S, Zhang B, Cao ZY, Ling TF, Shen WB. 2011. Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24, 181-191.
69. Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB. 2008. The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiology 148, 881-893.
70. Yannarelli GG, Noriega GO, Batlle A, Tomaro ML. 2006. Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224, 1154-1162.