H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination

Journal of Experimental Botany

Volumn 61, Issue 11, 2010, Pages 2979-2990

  Liu, Yinggao ^a,b   Ye, Nenghui ^b   Liu, Rui ^b   Chen, Moxian ^b   Zhang, Jianhua ^b  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

ABA; ABA catabolism; Arabidopsis; GA; GA biosynthesis; Hydrogen peroxide (H 2O2); Nitric oxide (NO); Seed dormancy

Indexed keywords

ARABIDOPSIS;

ABSCISIC ACID; ARABIDOPSIS PROTEIN; GIBBERELLIC ACID; GIBBERELLIN; HYDROGEN PEROXIDE; PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; METABOLISM; PHYSIOLOGY; PLANT SEED;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; GIBBERELLINS; HYDROGEN PEROXIDE; PLANT GROWTH REGULATORS; SEEDS;

EID: 77954711641     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq125     Document Type: Article

References (63)

1. Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784.
2. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
3. Bailly C, El-Maarouf-Bouteau H, Corbineau F. 2008. From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. Comptes Rendu Biologies 331, 806-814.
4. Batak I, Devic M, Giba Z, Grubisic D, Poff KL, Konjevic R. 2002. The effects of potassium nitrate and NO-donors on phytochrome A and phytochrome B-specific induced germination of Arabidopsis thaliana seeds. Seed Science Research 12, 253-259.
5. Bethke PC, Gubler F, Jacobsen JV, Jones RL. 2004. Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219, 847-855.
6. Bethke PC, Jones RL. 2001. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. The Plant Journal 25, 19-29.
7. Bethke PC, Libourei IG, Jones RL. 2006. Nitric oxide reduces seed dormancy in Arabidopsis. Journal of Experimental Botany 57, 517-526.
8. Bewley JD. 1997. Seed germination and dormancy. The Plant Cell 9, 1055-1066.
9. Bewley JD, Black M. 1994. Seeds: physiology of development and germination. New York: Plenum Press.
10. 2 synthesis. The Plant Journal 113-122.
11. Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ. 2008. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. The Plant Journal 53, 214-224.
12. Clough SL, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
13. Davies E. 1993. Intercellular and intracellular signals in plants and their transduction via the membrane-cytoskeleton interface. Seminars in Cell Biology 4, 139-147.
14. Finch-Savage WE, Leubner-Metzger G. 2006. Seed dormancy and the control of germination. New Phytologist 171, 501-523.
15. Finkelstein RR, Gampala SSL, Rock CD. 2002. Abscisic acid signaling in seeds and seedlings. The Plant Cell 14, S15-S45.
16. Fontaine O, Huault C, Pavis N, Billard JP. 1994. Dormancy breakage of Hordeum vulgare seeds: effects of hydrogen peroxide and scarification on glutathione level and glutathione reductase activity. Plant Physiology and Biochemistry 32, 677-683.
17. Foyer CH, Noctor G. 2005. Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell and Environment 28, 1056-1071.
18. Fujii H, Verslues PE, Zhu JK. 2007. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. The Plant Cell 19,485-494.
19. Ghassemian M, Nambara E, Cutler E, Kawaide H, Kamiya Y, McCourt P. 2000. Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. The Plant Cell 12, 1117-1126.
20. Gómez-Cadenas A, Zentalla R, Walker-Simmons M, Ho THD. 2001. Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. The Plant Cell 13, 667-679.
21. Groot SPC, Karssen CM. 1987. Gibberellins regulate seed germination in tomato by endosperm weakening: a study with gibberellin-deficient mutants. Planta 1 71, 525-531.
22. Han SY, Kitahata N, Sekimata K, Saito T, Kobayashi M, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K, Yoshida S, Asami T. 2004. A novel inhibitor of 9- cis-epoxycarotenoid dioxygenase in abscisic acid biosynthesis in higher plants. Plant Physiology 135, 1574-1582.
23. Himmelbach A, Yang Y, Grill E. 2003. Relay and control of abscisic acid signaling. Current Opinion in Plant Biology 6, 470-479.
24. Hoffmann-Benning S, Kende H. 1992. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physioogy 99, 1156-1161.
25. Holdsworth MJ, Bentsink L, Soppe WJJ. 2008. Molecular networks regulating Arabidopsis seed maturation, afterripening, dormancy and germination. New Phytologist 179, 33-54.
26. Jacobsen SE, Olszewski NE. 1993. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. The Plant Cell 5, 887-896.
27. Kauss H, Jeblick W. 1995. Pre-treatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2 Plant Physiology 108, 1171-1178.
28. Kauss H, Jeblick W. 1996. Influence of salicylic acid on the induction of competence for H2O2 elicitation. Plant Physiology 111, 755-763.
29. Kitahat N, Saito S, Miyazawa Y, et al. 2005. Chemical regulation of abscisic acid catabolism in plants by cytochrome P450 inhibitors. Bioorganic and Medicinal Chemistry 13, 4491-4498.
30. Koornneef M, van der Veen JH. 1980. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theoretical and Applied Genetics 58, 257-263.
31. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E. 2004. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism. EMBO Journal 23, 1647-1656.
32. Kuwabara A, Ikegami K, Koshiba T, Nagata T. 2003. Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata (Onagraceae). Planta 217, 880-887.
33. Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Taylor SAT, Low PS, Lee Y. 1999. Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reaction oxygen species from guard cells of tomato and Commelina communis. Plant Physiology 121, 147-152.
34. Leon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JA, Koornneef M. 1996. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. The Plant Journal 10, 655-661.
35. Levine A, Tenhaken R, Dixon RA, Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive response. Cell 79, 583-593.
36. Liu YG, Shi L, Ye NH, Liu R, Jia WS, Zhang JH. 2009. Nitric oxideinduced rapid decrease of ABA concentration is required in seed dormancy break in Arabidopsis. New Phytologist 183, 1030-1042.
37. Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid JB, Gubler F. 2006. Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8'-hydroxylase. The Plant Journal 45, 942-954.
38. Mittler R, Vanderauwera S, Gollery M, Van-Breusegem F. 2004. The reactive oxygen gene network in plants. Trends in Plant Science 9, 490-498.
39. Mur LAJ, Naylor G, Warner SAJ, Sugars JM, White RF, Draper J. 1996. Salicylic acid potentiates defense gene expression in leaf tissue exhibiting acquired resistance to pathogen attack. The Plant Journal 9, 559-571.
40. Nakajima M, Shimada A, Takashi Y, et al. 2006. Identification and characterization of Arabidopsis gibberellin receptors. The Plant Journal 46, 880-889.
41. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165-185.
42. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S. 2003. Gibberellin biosynthesis and response during Arabidopsis seed germination. The Plant Cell 15, 1591-1604.
43. Ogawa K, Iwabuchi M. 2001. A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant and Cell Physiology 42, 286-291.
44. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E. 2006. CYP707A1 and CYP707A2, which encode abscisic acid 8'-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiology 141, 97-107.
45. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. The Plant Cell 13, 179-191.
46. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731-734.
47. Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR. 1988. A monoclonal antibody to (S)-abscisic acid: its characterization and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173, 330-339.
48. Raz V, Bergervoet JH, Koornneef M. 2001. Sequential steps for developmental arrest in Arabidopsis seeds. Development 128, 243-252.
49. Razem FA, Baron K, Hill RD. 2006. Turning on gibberellin and abscisic acid signaling. Current Opinion in Plant Biology 9, 454-459.
50. Rogers JC, Rogers SW. 1992. Definition and functional implications of gibberellin and abscisic acid cis-acting hormone response complexes. The Plant Cell 4, 1443-1451.
51. Rose JK, Braam J, Fry SC, Nishitani K. 2002. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant and Cell Physiology 43, 1421-1435.
52. Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M. 2004. Arabidopsis CYP707As encode (+)-abscisic acid 8'-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiology 134, 1439-1449.
53. Sarath G, Hou G, Baird LM, Mitchell RB. 2007. Reactive oxygen species, ABA and nitric oxide interactions on the germination of warmseason C4-grasses. Planta 226, 697-708.
54. Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. The Plant Cell 9, 261-270.
55. Toh S, Imamura A, Watanabe A, et al. 2008. High temperatureinduced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiology 146, 1368-1385.
56. Weiss D, Ori N. 2007. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiology 144, 1240-1246.
57. White CN, Proebsting WM, Hedden P, Rivin CJ. 2000. Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. Plant Physiology 122, 1081-1088.
58. 2produced via AtMPK6-coupled signaling in Arabidopsis. The Plant Journal 54, 440-451.
59. Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S. 2004. Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. The Plant Cell 16, 367-378.
60. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.
61. Zeevaart JAD, Creelman RA. 1988. Metabolism and physiology of abscisic acid. Annual Review of Plant Physiology and Plant Molecular Biology 39, 439-473.
62. Zentella R, Yamauchi D, Ho THD. 2002. Molecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. The Plant Cell 14, 2289-2301.
63. Zhou L, Jang JC, Jones TL, Sheen J. 1998. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucoseinsensitive mutant. Proceedings of the National Academy of Sciences, USA 95, 10294-10299.