Regulation of abscisic acid metabolism in relation to the dormancy and germination of cereal grains

Justyna Fidler, Edyta Zdunek-Zastocka, Wiesław Bielawski

Abstract


Seed dormancy is of particular importance in the cultivation of cereals, as it directly affects the quality of crop yield. If the dormancy period is too short, this may lead to pre-harvest sprouting, whereas a dormancy period that is too long may cause uneven germination; both of these scenarios are associated with economic losses. Most enzymes engaged in the metabolism of abscisic acid (ABA) have been identified, and significant progress has been made in understanding the role of this phytohormone in the induction and maintenance of dormancy, mainly as a result of research conducted in Arabidopsis. Much less is known about the metabolism and function of ABA in cereal grains, especially in relation to dormancy and germination. This review focuses on the regulation of ABA metabolism in dormant and non-dormant cereal grains, in both the dry state and upon imbibition. Moreover, this review describes the influence of factors such as after-ripening, light, temperature, nitric oxide, and reactive oxygen species (ROS) on the dormancy and germination of cereal grains. These factors, with the exception of ROS, appear to affect the level of dormancy and germination of grains through regulation of ABA metabolism.

Keywords


9-cis-epoxycarotenoid dioxygenase; ABA 8'-hydroxylase; abscisic acid; abscisic acid metabolism; dormancy; germination

Full Text:

PDF

References


Bewley JD. Seed germination and dormancy. Plant Cell. 1997;9:1055–1066. http://dx.doi.org/10.1105/tpc.9.7.1055

Finch-Savage WE, Leubner-Metzger G. Seed dormancy and the control of germination. New Phytol. 2006;171:501–523. http://dx.doi.org/10.1111/j.1469-8137.2006.01787.x

Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ. Molecular mechanisms of seed dormancy. Plant Cell Environ. 2012;35:1769–1786. http://dx.doi.org/10.1111/j.1365-3040.2012.02542.x

Kumar S, Hirani AH, Asif M, Goyal A. Molecular mechanisms controlling dormancy and germination in barley. In: Asif M, Goyal A, editors. Crop production. ??: InTech; 2013. p. 69–98. http://dx.doi.org/10.5772/55473

Gerjets T, Scholefield D, Foulkes MJ, Lenton JR, Holdsworth MJ. An analysis of dormancy, ABA responsiveness, after-ripening and pre-harvest sprouting in hexaploid wheat (Triticum aestivum L.) caryopses. J Exp Bot. 2010;61:597–607. http://dx.doi.org/10.1093/jxb/erp329

Gubler F, Millar AA, Jacobsen JV. Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol. 2005;8:183–187. http://dx.doi.org/10.1016/j.pbi.2005.01.011

Corbineau F, Come D. Barley seed dormancy. Bios. 1996;261:113–119

Koornneef M, Bentsink L, Hilhorst H. Seed dormancy and germination. Curr Opinion Plant Biol. 2002;5:33–36. http://dx.doi.org/10.1016/S1369-5266(01)00219-9

Finkelstein R, Gampala SSL, Rock CD. Abscisic acid signaling in seeds and seedlings. Plant Cell. 2002;14:S15-S45. http://dx.doi.org/10.1105/tpc.010441

Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN. Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant. 2002;115:428–441. http://dx.doi.org/10.1034/j.1399-3054.2002.1150313.x

Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y. Abscisic acid and the control of seed dormancy and germination. Seed Sci Res. 2010;20:55–67. http://dx.doi.org/10.1017/S0960258510000012

Rodriguez MV, Mendiondo GM, Cantoro R, Auge GA, Luna V, Masciarelli O, et al. Expression of seed dormancy in grain sorghum lines with contrasting pre-harvest sprouting behavior involves differential regulation of gibberellin metabolism genes. Plant Cell Physiol. 2012;53:64–80. http://dx.doi.org/10.1093/pcp/pcr154

Rodriguez-Gacio MC, Matilla-Vazquez MA, Matilla AJ. Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav. 2009;4:1035–1048. http://dx.doi.org/10.4161/psb.4.11.9902

Millar A, Jacobsen J, Ross J, Helliwell C, Poole A, Scofield G, et al. Seed dormancy and ABA metabolism in Arabidopsis and barley: the role of ABA 8’-hydroxylase. Plant J. 2006;45:942–954. http://dx.doi.org/10.1111/j.1365-313X.2006.02659.x

Gubler F, Hughes T, Waterhouse P, Jacobsen J. Regulation of dormancy in barley by blue light and after-ripening: effects on abscisic acid and gibberellin metabolism. Plant Physiol. 2008;147:886–896. http://dx.doi.org/10.1104/pp.107.115469

Jacobsen JV, Barrero JM, Hughes T, Julkowska M, Taylor JM, Xu Q, et al. Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.). Planta. 2013;238:121–138. http://dx.doi.org/10.1007/s00425-013-1878-0

Finkelstein R. Abscisic acid synthesis and response. Arabidopsis Book. 2013;11:1–36. http://dx.doi.org/10.1199/tab.0166

Nambara E, Marion-Poll A. Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol. 2005;56:165–185. http://dx.doi.org/10.1146/annurev.arplant.56.032604.144046

Schwartz SH, Qin X, Zeevaart JAD. Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol. 2003;131:1591–1601. http://dx.doi.org/10.1104/pp.102.017921

Schwartz SH, Zeevaart JAD. Abscisic acid biosynthesis and metabolism. In: Davies PJ, editor. Plant hormones. Dordrecht: Springer Netherlands; 2010. p. 137–155. http://dx.doi.org/10.1007/978-1-4020-2686-7_7

Seo M, Koshiba T. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 2002;7:41–48. http://dx.doi.org/10.1016/S1360-1385(01)02187-2

Taylor IB, Sonneveld T, Bugg TD, Thompson AJ. Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. J Plant Growth Regul. 2005;24:253–273. http://dx.doi.org/10.1007/s00344-005-0070-6

Xu ZY, Kim DH, Hwang I. ABA homeostasis and signaling involving multiple subcellular compartments and multiple receptors. Plant Cell Rep. 2013;32:807–813. http://dx.doi.org/10.1007/s00299-013-1396-3

Liu A, Gao F, Kanno Y, Jordan MC, Kamiya Y, Seo M, et al. Regulation of wheat seed dormancy by after-ripening is mediated by specific transcriptional switches that induce changes in seed hormone metabolism and signaling. PLoS ONE. 2013;8:1–18. http://dx.doi.org/10.1371/journal.pone.0056570

Chono M, Hondo I, Shinoda S, Kushiro T, Kamiya Y, Nambara E, et al. Field studies in the regulation of abscisic acid content and germinability during grain development of barley: molecular and chemical analysis of pre-harvest sprouting. J Exp Bot. 2006;57:2421–2434. http://dx.doi.org/10.1093/jxb/erj215

Kermode AR. Role of abscisic acid in seed dormancy. J Plant Growth Regul. 2005;24:319–344. http://dx.doi.org/10.1007/s00344-005-0110-2

Liu Y, Fang J, Xu F, Chu J, Yan C, Schlappi MR, et al. Expression patterns of ABA and GA metabolism genes and hormone levels during rice seed development and imbibition: a comparison of dormant and non-dormant rice cultivars. J Genet Genomics. 2014;41:327–338. http://dx.doi.org/10.1016/j.jgg.2014.04.004

Barrero JM, Jacobsen JV, Talbot M, White R, Swain M, Garvin D, et al. Grain dormancy and light quality effects on germination in the model grass Brachypodium distachyon. New Phytol. 2012;193:376–386. http://dx.doi.org/10.1111/j.1469-8137.2011.03938.x

Walker-Simmons M. ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiol. 1987;84:61–66. http://dx.doi.org/10.1104/pp.84.1.61

Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F. Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol. 2009;150:1006–1021. http://dx.doi.org/10.1104/pp.109.900293

Chono M, Matsunaka H, Seki M, Fujita M, Kiribuchi-Otobe C, Oda S, et al. Isolation of a wheat (Triticum aestivum L.) mutant in ABA 8’-hydroxylase gene: effect of reduced ABA catabolism on germination inhibition under field condition. Breed Sci. 2013;63:104–115. http://dx.doi.org/10.1270/jsbbs.63.104

Liu F, Zhang H, Wu G, Sun J, Hao L, Ge X, et al. Sequence variation and expression analysis of seed dormancy- and germination-associated ABA- and GA-related genes in rice cultivars. Front Plant Sci. 2011;2:1–13. http://dx.doi.org/10.3389/fpls.2011.00017

Hwang SG, Chen HC, Huang WY, Chu YC, Shii CT, Cheng WH. Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. Plant Sci. 2010;178:12–22. http://dx.doi.org/10.1016/j.plantsci.2009.09.014

Sawada Y, Aoki M, Nakaminami K, Mitsuhashi W, Tatematsu K, Kushiro T, et al. Phytochrome and gibberellin-mediated regulation of abscisic acid metabolism during germination of photoblastic lettuce seeds. Plant Physiol. 2008;146:1386–1396. http://dx.doi.org/10.1104/pp.107.900248

Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, et al. Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J. 2006;48:354–366. http://dx.doi.org/10.1111/j.1365-313X.2006.02881.x

Barrero JM, Downie AB, Xu Q, Gubler F. A Role for Barley CRYPTOCHROME1 in light regulation of grain dormancy and germination. Plant Cell. 2014;26:1094–1104. http://dx.doi.org/10.1105/tpc.113.121830

Goggin D, Steadman K, Powles S. Green and blue light photoreceptors are involved in maintenance of dormancy in imbibed annual ryegrass (Lolium rigidum) seeds. New Phytol. 2008;148:81–89. http://dx.doi.org/10.1111/j.1469-8137.2008.02570.x

Hoang HH, Sechet J, Bailly C, Leymarie J, Corbineau F. Inhibition of germination of dormant barley (Hordeum vulgare L.) grains by blue light as related to oxygen and hormonal regulation. Plant Cell Environ. 2014;37:1393–1403. http://dx.doi.org/10.1111/pce.12239

Benech-Arnold RL, Gualano N, Leymarie J, Come D, Corbineau F. Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. J Exp Bot. 2006;57:1423–1430. http://dx.doi.org/10.1093/jxb/erj122

Leymarie J, Robayo-Romero ME, Gendreau E, Benech-Arnold RL, Corbineau F. Involvement of ABA in induction of secondary dormancy in barley (Hordeum vulgare L.) seeds. Plant Cell Physiol. 2008;49:1830–1838. http://dx.doi.org/10.1093/pcp/pcn164

Corbineau F, Black M, Come D. Induction of thermodormancy in Avena sativa seeds. Seed Sci Res. 1993;3:111–117. http://dx.doi.org/10.1017/S0960258500001665

Argyris J, Dahal P, Hayashi E, Still DW, Bradford KJ. Genetic variation for lettuce seed thermoinhibition is associated with temperature sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiol. 2008;148:926–947. http://dx.doi.org/10.1104/pp.108.125807

Corbineau F, Come D. Dormancy of cereal seeds as related to embryo sensitivity to ABA and water potential. In: Viemont JD, Crabbe J, editors. Dormancy in plants: from whole plants behaviour to cellular control. Oxon: CAB International; 2000.

Leymarie J, Benech-Arnold RL, Farrant JM, Corbineau F. Thermodormancy and ABA metabolism in barley grains. Plant Signal Behav. 2009;4:205–207. http://dx.doi.org/10.1093/pcp/pcn164

Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, et al. High temperature induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol. 2008;146:1368–1385. http://dx.doi.org/10.1104/pp.107.113738

Bailly C, Kranner I. Methods for analyses of reactive oxygen species and antioxidants in relation to seed longevity and germination. Methods Mol Biol. 2011;773:343–367. http://dx.doi.org/10.1007/978-1-61779-231-1_20

Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, et al. Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J Exp Bot. 2011;63:1809–1822. http://dx.doi.org/10.1093/jxb/err336

El-Maarouf-Bouteau H, Bailly C. Oxidative signaling in seed germination and dormancy. Plant Signal Behav. 2008;3:175–182. http://dx.doi.org/10.4161/psb.3.3.5539

Caliskan M, Cuming AC. Spatial specificity of H2O2-generating oxalate oxidase gene expression during wheat embryo germination. Plant J. 1998;15:165–171. http://dx.doi.org/10.1046/j.1365-313X.1998.00191.x

Ishibashi Y, Tawaratsumida T, Zheng SH, Yuasa T, Iwaya-Inoue M. NADPH oxidases act as key enzyme on germination and seedling growth in barley (Hordeum vulgare L.). Plant Prod Sci. 2010;13:45–52. http://dx.doi.org/10.1626/pps.13.45

Ishibashi Y, Yamamoto K, Tawaratsumida T, Yuasa T, Iwaya-Inoue M. Hydrogen peroxide scavenging regulates germination ability during wheat (Triticum aestivum L.) seed maturation. Plant Signal Behav. 2008;3:183–188. http://dx.doi.org/10.4161/psb.3.3.5540

Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ, Albacete A, Faize L, Faize M, et al. Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant Cell Environ. 2010;33:981–994. http://dx.doi.org/10.1111/j.1365-3040.2010.02120.x

Fath A, Bethke P, Beligni V, Jones R. Active oxygen and cell death in cereal aleurone cells. J Exp Bot. 2002;53:1273–1282. http://dx.doi.org/10.1093/jexbot/53.372.1273

Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, et al. Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol. 2012;158:1705–1714. http://dx.doi.org/10.1104/pp.111.192740

Bahin E, Bailly C, Sotta B, Kranner I, Corbineau F, Leymarie J. Crosstalk between reactive oxygen species and hormonal signaling pathways regulates grain dormancy in barley. Plant Cell Environ. 2011;34:980–993. http://dx.doi.org/10.1111/j.1365-3040.2011.02298.x

Lu S, Su W, Li H, Guo Z. Abscisic acid improves drought tolerance of triploid bermuda grass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem. 2009;47:132–138. http://dx.doi.org/10.1016/j.plaphy.2008.10.006

Bethke PC, Gubler F, Jacobsen JV, Jones RL. Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta. 2004;219:847–855. http://dx.doi.org/10.1007/s00425-004-1282-x

Bethke PC, Libourel IGL, Reinöhl V, Jones RL. Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide–dependent manner. Planta. 2006;223:805–812. http://dx.doi.org/10.1007/s00425-005-0116-9

Liu Y, Shi L, Ye N, Liu R, Jia W, Zhang J. Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytol. 2009;183:1030–1042. http://dx.doi.org/10.1111/j.1469-8137.2009.02899.x

Matakiadis T, Albores A, Jikumaru Y, Tatematsu K, Pichon O, Renou JP, et al. The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol. 2009;149:949–960. http://dx.doi.org/10.1104/pp.108.126938

Barrero JM, Jacobsen J, Gubler F. Seed dormancy: approaches for finding new genes in cereals. In: Pua EC, Davey MR, editors. Plant developmental biology – biotechnological perspectives. Berlin: Springer; 2010. p. 361–381. http://dx.doi.org/10.1007/978-3-642-02301-9_18

Vain P. Brachypodium as a model system for grass research. J Cereal Sci. 2011;54:1–7. http://dx.doi.org/10.1016/j.jcs.2011.04.002

Agrawal GK, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H. Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion: tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol. 2001;125:1248–1257. http://dx.doi.org/10.1104/pp.125.3.1248

Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR. Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA. 1997;94:12235–12240.

Zhang SJ, Song GQ, Li YL, Gao J, Liu JJ, Fan QQ, et al. Cloning of 9-cis-epoxycarotenoid dioxygenase gene (TaNCED1) from wheat and its heterologous expression in tobacco. Biol Plant. 2014;58:89–98. http://dx.doi.org/10.1007/s10535-013-0373-6

Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, et al. ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. J Exp Bot. 2011;62:2615–2632. http://dx.doi.org/10.1093/jxb/erq446

Ji X, Dong B, Shiran B, Talbot MJ, Edlington JE, Hughes T, et al. Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiol. 2011;156:647–662. http://dx.doi.org/10.1104/pp.111.176164

Vallabhaneni R, Wurtzel ET. From epoxycarotenoids to ABA: the role of ABA 8’-hydroxylases in drought-stressed maize roots. Arch Biochem Biophys. 2010;504:112–117. http://dx.doi.org/10.1016/j.abb.2010.07.005

Capelle V, Remoue C, Moreau L, Reyss A, Mahe A, Massonneau A, et al. QTLs and candidate genes for desiccation and abscisic acid content in maize kernels. BMC Plant Biol. 2010;10:2. http://dx.doi.org/10.1186/1471-2229-10-2

Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR. Specific oxidative cleavage of carotenoids by VP14 of maize. Science. 1997;276:1872–1874. http://dx.doi.org/10.1126/science.276.5320.1872

Chen QF, Ya HY, Feng YR, Jiao Z. Expression of the key genes involved in ABA biosynthesis in rice implanted by ion beam. Appl Biochem Biotechnol. 2014;137:239–247. http://dx.doi.org/10.1007/s12010-014-0837-y

Zhang CL, He XY, He ZH, Wang LH, Xia XC. Cloning of TaCYP707A1 gene that encodes ABA 8’-hydroxylase in common wheat (Triticum aestivum L.). Agric Sci China. 2009;8:902–909. http://dx.doi.org/10.1016/S1671-2927(08)60294-1

Nakamura S, Chono M, Abe F, Miura H. Mapping a diploid wheat abscisic acid 8’-hydroxylase homologue in the seed dormancy QTL region on chromosome 5Am. Euphytica. 2010;171:111–120. http://dx.doi.org/10.1007/s10681-009-0002-9

Yang SH, Choi D. Characterization of genes encoding ABA 8’-hydroxylase in ethylene-induced stem growth of deepwater rice (Oryza sativa L.). Biochem Biophys Res Commun. 2006;350:685–690. http://dx.doi.org/10.1016/j.bbrc.2006.09.098

Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S, Jikumaru Y, et al. Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8’-hydroxylase in rice. Plant Cell Physiol. 2007;48:287–298. http://dx.doi.org/10.1093/pcp/pcm003




DOI: https://doi.org/10.5586/asbp.2015.004

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society