Induction of secondary dormancy by hypoxia in barley grains and its hormonal regulation

Journal of Experimental Botany

Volumn 64, Issue 7, 2013, Pages 2017-2025

  Hoang, Hai Ha ^a   Bailly, Christophe ^a   Corbineau, Françoise ^a   Leymarie, Juliette ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Abscisic acid; Germination; Gibberellins; Hypoxia; Secondary dormancy; Seed

Indexed keywords

ABSCISIC ACID; GIBBERELLIN; VEGETABLE PROTEIN;

ARTICLE; CELL HYPOXIA; DRUG EFFECT; GENETICS; GERMINATION; HORDEUM; METABOLISM; PHYSIOLOGY; PLANT SEED; SIGNAL TRANSDUCTION; TEMPERATURE;

ABSCISIC ACID; CELL HYPOXIA; GERMINATION; GIBBERELLINS; HORDEUM; PLANT PROTEINS; SEEDS; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 84886084104     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert062     Document Type: Article

References (55)

1. Al-Ani A., Bruzeau F, Raymond P., Saint-Ges V, Leblanc JM, Pradet A. 1985. Germination, respiration, and adenylate energy charge of seeds at various oxygen partial pressures. Plant Physiology 79, 885-890.
2. Asif M, Trivedi P, Misra P., Nath P. 2009. Prolyl-4-hydroxylase (AtP4H1) mediates and mimics low oxygen response in Arabidopsis thaliana. Functional & Integrative Genomics 9, 525-535.
3. Bahin E, Bailly C, Sotta B., Kranner I, Corbineau F, Leymarie J. 2011. Crosstalk between reactive oxygen species and hormonal signalling pathways regulates grain dormancy in barley. Plant, Cell & Environment 34, 980-993.
4. Bailey-Serres J., Fukao T, Gibbs D.J., Holdsworth MJ, Lee SC, Licausi F, Perata P., Voesenek LACJ, Van Dongen JT. 2012. Making sense of low oxygen sensing. Trends in Plant Science 17, 129-138.
5. Bailey-Serres J., Voesenek LACJ. 2008. Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313-339.
6. Baskin C, Baskin J. 1998. Seeds: ecology, biogeography and evolution of dormancy and germination. San Diego: Academic Press.
7. Benech-Arnold R.L., Gualano N, Leymarie J., Côme D, Corbineau F. 2006. Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. Journal of Experimental Botany 57, 1423-1430.
8. Benvenuti S, Macchia M. 1995. Effect of hypoxia on buried weed seed-germination. Weed Research 35, 343-351.
9. Bewley JD. 1997. Seed germination and dormancy. Plant Cell 9, 1055-1066.
10. Borisjuk L, Rolletschek H. 2009. The oxygen status of the developing seed. New Phytologist 182, 17-30.
11. Bradford K, Côme D, Corbineau F. 2007. Quantifying the oxygen sensitivity of seed germination using a population-based threshold level. Seed Science Research 17, 33-43.
12. Bradford KJ, Benech-Arnold RL, Côme D, Corbineau F. 2008. Quantifying the sensitivity of barley seed germination to oxygen, abscisic acid, and gibberellin using a population-based threshold model. Journal of Experimental Botany 59, 335-347.
13. Chono M, Honda I, Shinoda S., Kushiro T, Kamiya Y, Nambara E., Kawakami N, Kaneko S, Watanabe Y. 2006. Field studies on the regulation of abscisic acid content and germinability during grain development of barley: molecular and chemical analysis of pre-harvest sprouting. Journal of Experimental Botany 57, 2421-2434.
14. Côme D., Corbineau C, Lecat S. 1988. Some aspects of metabolic regulation of cereal seed germination and dormancy. Seed Science & Technology 16, 175-186.
15. Côme D., Tissaoui T. 1968. Induction d'une dormance embryonnaire secondaire chez le Pommier (Pirus malus L.) par des atmosphères très appauvries en oxygène. Comptes Rendus de l'Académie des Sciences, Paris, série D 266, 477-479.
16. Corbineau F, Black M, Côme D. 1993. Induction of thermodormancy in Avena sativa seeds. Seed Science Research 3, 111-117.
17. Corbineau F, Côme D. 1980. Quelques caractéristiques de la dormance du caryopse d'Orge (Hordeum vulgare L., variété Sonja). Comptes Rendus de l'Académie des Sciences, Paris, série D 290, 547-550.
18. Corbineau F, Côme D. 1996. Barley seed dormancy. BIOS Boissons conditionnement 27, 113-119.
19. Debeaujon I, Leon KK, Koornneef M. 2000. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403-413.
20. Debeaujon I, Lepiniec L, Pourcel L., Routaboul J. 2007. Seed coat development and dormancy. In: Bradford K, Nonogaki H, eds. Seed development, dormancy and germination. Oxford: Blackwell Publishing, 25-49.
21. Edwards MM. 1973. Seed dormancy and seed environment-internal oxygen relationships. In: Heydecker W, ed. Seed ecology. London: Butterworths, 169-188.
22. Esashi Y, Okazaki M, Yanai N., Hishinuma K. 1978. Control of germination of secondary dormant cocklebur seeds by various germination stimulants. Plant & Cell Physiology 19, 1497-1506.
23. Flintham JE. 1993. Grain colour and sprout-resistance in wheat. In: Walker-Simmons MK, Reed JL, eds. Pre-harvest sprouting in cereals 1992. American Association of Cereal Chemist, St Paul, Minnesota, USA, 30-36.
24. Footitt S, Douterelo-Soler I, Clay H., Finch-Savage WE. 2011. Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences, U S A 108, 20236-20241.
25. Gambrell RP, DeLaune, RD, Patrick WH Jr. 1991. Redox processes in soils following oxygen depletion. In: Jackson MB, Davies DD, Lambers H, eds. Plant life under oxygen stress. The Hague: Academic Publishing, 101-117.
26. Gibbs DJ, Lee SC, Isa NMD, et al 2011. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479, 415-418.
27. Gubler F, Hughes T, Waterhouse P and Jacobsen J. 2008. Regulation of dormancy in barley by blue light and after-ripening: effects on abscisic acid and gibberellin metabolism. Plant Physiology 147, 886-896.
28. Gubler F, Millar AA, Jacobsen JV 2005. Dormancy release, ABA and pre-harvest sprouting. Current Opinion in Plant Biology 8, 183-187.
29. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.
30. Hilhorst HWM. 2007. Definitions and hypotheses of seed dormancy. In: Bradford KJ, Nonogaki H, eds. Seed development, dormancy and germination. Oxford: Blackwell Publishing, 50-71.
31. Himi E, Mares DJ, Yanagisawa A, Noda K. 2002. Effect of grain colour gene (R) on grain dormancy and sensitivity of the embryo to abscisic acid (ABA) in wheat. Journal of Experimental Botany 53, 1569-1574.
32. Hirsilä M, Koivunen P, Günzler V, Kivirikko KI, Myllyharju J. 2003. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. Journal of Biological Chemistry 278, 30772-30780.
33. Hoang HH, Sotta B, Gendreau E., Bailly C, Leymarie J, Corbineau F. 2012. Water content: a key factor of the induction of secondary dormancy in barley grains as related to ABA metabolism. Physiologia Plantarum, DOI: 10.1111/j.1399-3054.2012.01710.x.
34. Hughes BT, Espenshade PJ 2008. Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl hydroxylase family member. EMBO Journal 27, 1491-1501.
35. Hughes BT, Nwosu CC, Espenshade PJ 2009. Degradation of sterol regulatory element-binding protein precursor requires the endoplasmic reticulum-associated degradation components Ubc7 and Hrd1 in fission yeast. Journal of Biological Chemistry 284, 20512-20521.
36. Julliard J, Maldiney R, Sotta B., Miginiac E, Kerhoas L, Einhorn J. 1994. HPLC-ELISA and MS as complementary techniques to study plant hormone metabolites. Analysis 22, 483-489.
37. Kaelin WGJ, Ratcliffe PJ 2008. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Molecular Cell 30, 393-402.
38. Krochko JE, Abrams GD, Loewen M.K., Abrams SR, Cutler AJ 1998. (+)-Abscisic acid 8'-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiology 118, 849-860.
39. Lehner A, Mamadou N, Poels P., Côme D, Bailly C., Corbineau F. 2008. Changes in soluble carbohydrates, lipid peroxidation and antioxidant enzyme activities in the embryo during ageing in wheat grains. Journal of Cereal Science 47, 555-565.
40. Lenoir C, Corbineau F, Côme D. 1986. Barley (Hordeum vulgare) seed dormancy as related to glumella characteristics. Physiologia Plantarum 68, 301-307.
41. Leymarie J, Benech-Arnold RL, Farrant J.M., Corbineau F. 2007. Identification of transcripts potentially involved in barley seed germination and dormancy using cDNA-AFLP. Journal of Experimental Botany 3, 425-437.
42. Leymarie J, Robayo-Romero ME, Gendreau E., Benech-Arnold RL, Corbineau F. 2008. Involvement of ABA in induction of secondary dormancy in barley (Hordeum vulgare L.) seeds. Plant & Cell Physiology 49, 1830-1838.
43. Licausi F, Kosmacz M, Weits D.A., Giuntoli B., Giorgi FM, Voesenek LACJ, Perata P, Van Dongen JT. 2011. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419-423.
44. Lonchamp JP, Gora M. 1979. Influence d'anoxies partielles sur la germination de semences de mauvaises herbes. Oecologia Plantarum 14, 121-128.
45. Mendiondo GM, Leymarie J, Farrant J., Corbineau F, Benech-Arnold RL. 2010. Differential expression of abscisic acid metabolism and signalling genes induced by seed covering structures or hypoxia in barley (Hordeum Vulgare L). Seed Science Research 20, 69-77.
46. Millar A.A., Jacobsen J V, Ross J J, Helliwell C A, Poole A T, Scofield G, Reid J B, Gubler F. 2006. Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8'-hydroxylase. The Plant Journal 45, 942-954.
47. Pekrun C, Lutman P J W Baeumer K. 1997. Induction of secondary dormancy in rape seeds (Brassica napus L.) by prolonged imbibition under conditions of water stress or oxygen deficiency in darkness. European Journal of Agronomy 6, 245-255.
48. Richard G, Boiffin J. 1990. Effet de l'état structural du lit de semences sur la germination et la levée des cultures. In: La structure du sol et son évolution. Paris: INRA éditions, 112-136.
49. Sutton F, Kenefick D. 1994. Nucleotide sequence of a cDNA encoding an elongation factor (EF-1) from barley primary leaf. Plant Physiology 104, 807.
50. Symons SJJM, Naylor GM, Simpson G.M., Adkins SW 1986. Secondary dormancy in Avena fatua: induction and characteristics in genetically pure dormant lines. Physiologia Plantarum 68, 27-33.
51. Verwoerd TC, Dekker BMM, Hoekema A. 1989. A small scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Research 17, 2362.
52. Vlad F, Spano T, Vlad D., Bou Daher F, Ouelhadj A, Kalaitzis P. 2007. Arabidopsis prolyl 4-hydroxylases are differentially expressed in response to hypoxia, anoxia and mechanical wounding. Physiologia Plantarum 130, 471-483.
53. White J, Pacey-Miller T, Bundock P., Henry R. 2008. Differential LongSAGE tag abundance analysis in a barley seed germination time course and validation with relative real-time RT-PCR. Plant Science 175, 858-867.
54. 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. Plant Cell 16, 367-378.
55. Zou XL, Jiang YY, Zheng Y.L., Zhang MD, Zhang ZX 2011. Prolyl 4-hydroxylase genes are subjected to alternative splicing in roots of maize seedlings under waterlogging. Annals of Botany 108, 1323-1335.