Abstract
This paper describes the isolation of wheat mutants in the hard red spring Scarlet resulting in reduced sensitivity to the plant hormone abscisic acid (ABA) during seed germination. ABA induces seed dormancy during embryo maturation and inhibits the germination of mature seeds. Wheat sensitivity to ABA gradually decreases with dry after-ripening. Scarlet grain normally fails to germinate when fully dormant, shows ABA sensitive germination when partially after-ripened, and becomes ABA insensitive when after-ripened for 8–12 months. Scarlet ABA-insensitive (ScABI) mutants were isolated based on the ability to germinate on 5 μM ABA after only 3 weeks of after-ripening, a condition under which Scarlet would fail to germinate. Six independent seed-specific mutants were recovered. ScABI1, ScABI2, ScABI3 and ScABI4 are able to germinate more efficiently than Scarlet at up to 25 μM ABA. The two strongest ABA insensitive lines, ScABI3 and ScABI4, both proved to be partly dominant suggesting that they result from gain-of-function mutations. The ScABI1, ScABI2, ScABI3, ScABI4, and ScABI5 mutants after-ripen more rapidly than Scarlet. Thus, ABA insensitivity is associated with decreased grain dormancy in Scarlet wheat. This suggests that ABA sensitivity is an important factor controlling grain dormancy in wheat, a trait that impacts seedling emergence and pre-harvest sprouting resistance.
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Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI (1999) Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell 11:1785–1798
Appleford NEJ, Wilkinson MD, Ma Q, Evans DJ, Stone MC, Pearce SP, Powers SJ, Thomas SG, Jones HD, Phillips AL, Hedden P, Lenton JR (2007) Decreased shoot stature and grain α-amylase activity following ectopic expression of a gibberellin 2-oxidase gene in transgenic wheat. J Exp Bot 56:3213–3226
Barrero J, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150:1006–1021
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Bewley JD, Black M (1994) Seeds: physiology of development and germination. Plenum Press, New York
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. J Exp Bot 57:2421–2434
Dave A, Hernández ML, He Z, Andriotis ME, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599
Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866
Dupeux F, Antoni R, Betz K, Santiago J, Gonzalez-Guzman M, Rodriguez L, Rubio S, Park S-Y, Cutler SR, Rodriguez PL, Márquez JA (2011) Modulation of abscisic acid signaling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiol 156:106–116
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415
Flintham JE (2000) Different genetic components control coat-imposed and embryo-imposed dormancy in wheat. Seed Sci Res 10:43–50
Galili S, Avivi Y, Millet E, Feldman M (2000) RFLP-based analysis of three RbcS subfamilies in diploid and polyploid species of wheat. Mol Genet Genomics 263:674–680
Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126
Groot SPC, Karssen CM (1992) Dormancy and germination of abscisic acid-deficient tomato seeds: studies with the sitiens mutant. Plant Physiol 99:952–958
Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol 8:183–187
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. J Exp Bot 53:1569–1574
Himi E, Maekawa M, Miura H, Noda K (2011) Development of PCR markers for Tamyb10 related to R-1, red grain color gene in wheat. Theor Appl Genet 122:1561–1576
Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54
Jiang J, Gill BS (1994) New 18S·26S ribosomal RNA gene loci: chromosomal landmarks for the evolution of polyploid wheats. Chromosoma 103:179–185
Karssen CM, Laçka E (1986) A revision of the hormone balance theory of seed dormancy: studies on gibberellin and/or abscisic acid-deficient mutants of Arabidopsis thaliana. In: Bopp M. (ed.) Plant growth substances 1985: proceedings of the 12th international conference on plant growth substances. Springer, New York, pp 315–323
Kawakami N, Miyake Y, Noda K (1997) ABA insensitivity and low ABA levels during seed development of non-dormant wheat mutants. J Exp Bot 48:1415–1421
Keith K, Kraml M, Dengler NG, McCourt P (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6:589–600
Kidwell KK, Shelton GB, Morris CF, Line RF, Miller BC, Davis MA, Konzak CF (1999) Registration of ‘Scarlet’ wheat. Crop Sci 39:1255
Klinger JP, Batelli G, Zhu J-K (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199–3210
Kobayashi F, Takumi S, Egawa C, Ishibashi M, Nakamura C (2006) Expression patterns of low temperature responsive genes in a dominant ABA-less-sensitive mutant line of common wheat. Physiol Plantarum 127:612–623
Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh. Theor Appl Genet 61:385–393
Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plantarum 61:377–383
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 J 23:1647–1656
Lalonde S, Saini HS (1992) Comparative requirement for endogenous ethylene during seed germination. Ann Bot Lond 69:423–428
Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christman A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
McCallum JA, Walker JRL (1990) Phenolic biosynthesis during grain development in wheat: changes in phenylalanine ammonia-lyase activity and soluble phenolic content. J Cereal Sci 11:35–49
McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905
McKibbin RS, Wilkinson MD, Bailey PC, Flintham JE, Andrew LM, Lazzeri PA, Gale MD, Lenton JR, Holdsworth MJ (2002) Transcripts of Vp-1 homeologues are misspliced in modern wheat and ancestral species. Proc Natl Acad Sci USA 99:10203–10208
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. Plant J 45:942–954
Miyamoto T, Everson EH (1958) Biochemical and physiological studies of wheat seed pigmentation. Agron J 50:733–734
Molina-Cano JL, Sopena A, Swanston JS, Casas AM, Moralejo MA, Ubieto A, Lara I, Pérez-Vendrell AM, Romagosa I (1999) A mutant induced in the malting barley cv Triumph with reduced dormancy and ABA response. Theor Appl Genet 98:347–355
Morris CF, Moffatt JM, Sears RG, Paulsen GM (1989) Seed dormancy and responses of caryopses, embryos, and calli to abscisic acid in wheat. Plant Physiol 90:643–647
Nishimura N, Yoshida T, Murayama M, Asami T, Shinozaki K, Hirayama T (2004) Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant Cell Physiol 45:1485–1499
Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007) ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50:935–949
Nishimura N, Sarkeshik A, Nito K, Park S-Y, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, Yates JR, Schroeder JI (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299
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 indispensible for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107
Okubara PA, Steber CM, DeMacon VL, Walter NL, Paulitz TC, Kidwell KK (2009) Scarlet-Rz1, and EMS-generated hexaploid wheat with tolerance to the soilborne necrotrophic pathogens Rhizoctonia solani AG-8 and R. oryzae. Theor Appl Genet 119:293–303
Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071
Prada D, Romagosa I, Ullrich SE, Molina-Cano JL (2005) A centromeric region on chromosome 6 (6H) affects dormancy in an induced mutant in barley. J Exp Bot 56:47–54
Raskin I, Ladyman JAR (1988) Isolation and characterization of a barley mutant with abscisic acid-insensitive stomata. Planta 173:73–78
Rikiishi K, Maekawa M (2010) Characterization of a novel wheat (Triticum aestivum L.) mutant with reduced seed dormancy. J Cereal Sci 51:292–298
Romagosa I, Prada D, Moralejo MA, Sopena A, Muñoz P, Casas AM, Swanston JS, Molina-Cano JL (2001) Dormancy, ABA content and sensitivity of a barley mutant to ABA application during seed development and after ripening. J Exp Bot 52:1499–1506
Schlüter U, Muschak M, Berger D, Altmann T (2003) Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes. J Exp Bot 54:867–874
Schramm EC, Abellera JC, Strader LC, Campbell KG, Steber CM (2010) Isolation of ABA-responsive mutants in allohexaploid bread wheat (Triticum aestivum L.): drawing connections to grain dormancy, preharvest sprouting, and drought tolerance. Plant Sci 179:620–629
Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by Vp14 of maize. Science 276:1872–1874
Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 125:763–769
Torada A, Amano Y (2002) Effect of seed coat color on seed dormancy in different environments. Euphytica 126:99–105
Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138
Visser K, Vissers APA, Çağirgan MI, Kijne JW, Wang M (1996) Rapid germination of a barley mutant is correlated with a rapid turnover of abscisic acid outside the embryo. Plant Physiol 111:1127–1133
Walker-Simmons M (1987) ABA levels and sensitivity in developing wheat embryos of sprouting resistant and susceptible cultivars. Plant Physiol 84:61–66
Warner RL, Kudrna DA, Spaeth SC, Jones SS (2000) Dormancy in white-grain mutants of Chinese Spring wheat (Triticum aestivum L.). Seed Sci Res 10:51–60
Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2005) ABA-Hypersensitive Germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126
Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119
Acknowledgments
The authors would like to thank K. Kidwell for providing seeds of Scarlet wheat, and S. Abrams for providing (+)-ABA. Thanks are due to R. Parveen and A. Burke for expert technical assistance, to K. Garland Campbell for advice and assistance, and to C. Walker for assistance with statistical analysis. This work was supported by NIH Protein Biotechnology training grant funding (ECS), a fellowship from ARCS (Seattle chapter) (ECS), and USDA CSREES grant number 2005-01099 (CMS).
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Schramm, E.C., Nelson, S.K. & Steber, C.M. Wheat ABA-insensitive mutants result in reduced grain dormancy. Euphytica 188, 35–49 (2012). https://doi.org/10.1007/s10681-012-0669-1
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DOI: https://doi.org/10.1007/s10681-012-0669-1