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Functional analysis of TaABF1 during abscisic acid and gibberellin signalling in aleurone cells of cereal grains

Published online by Cambridge University Press:  08 April 2013

Lauren J. Harris ,
Sarah A. Martinez ,
Benjamin R. Keyser ,
William E. Dyer  and
Russell R. Johnson
Lauren J. Harris
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville, ME 04901, USA
Sarah A. Martinez
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville, ME 04901, USA
Benjamin R. Keyser
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville, ME 04901, USA
William E. Dyer
Affiliation:
Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59715, USA
Russell R. Johnson*
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville, ME 04901, USA
*
*Correspondence E-mail: [email protected]
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Abstract

The wheat transcription factor TaABF1 physically interacts with the protein kinase PKABA1 and mediates both abscisic acid (ABA)-induced and ABA-suppressed gene expression. In bombarded aleurone cells of imbibing grains, the effect of TaABF1 in down-regulating the gibberellin (GA)-induced Amy32b promoter was stronger in the presence of exogenous ABA. As these grains contained low levels of endogenous ABA, the effect of TaABF1 may also be mediated by ABA-induced activation even in the absence of exogenous ABA. Levels of TaABF1 protein decreased slightly during imbibition of afterripened grains. However, TaABF1 levels (especially in aleurone layers) were not substantially affected by exogenous ABA or GA, indicating that changes in TaABF1 protein level are not an important part of regulating its role in hormone signalling. We found that TaABF1 was phosphorylated in vivo in aleurone cells, suggesting a role for post-translational modification in regulating TaABF1 activity. Induction of Amy32b by overexpression of the transcription factor GAMyb could not be prevented by TaABF1, indicating that TaABF1 acts upstream of GAMyb transcription in the signalling pathway. Supporting this view, knockdown of TaABF1 by RNA interference resulted in increased expression from the GAMyb promoter. These results are consistent with a model in which TaABF1 is constitutively present in aleurone cells, while its ability to down-regulate GAMyb is regulated in response to ABA.

Keywords

abscisic acidgerminationgibberellinimbibitionwheat
Type
Research Papers
Information
Seed Science Research , Volume 23 , Issue 2 , June 2013 , pp. 89 - 98
Copyright
Copyright © Cambridge University Press 2013 

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References

Casaretto, J. and Ho, T.-H.D. (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15, 271–284.CrossRefGoogle ScholarPubMed
Casaretto, J.A. and Ho, T.-H.D. (2005) Transcriptional regulation by abscisic acid in barley (Hordeum vulgare L.) seeds involves autoregulation of the transcription factor HvABI5. Plant Molecular Biology 57, 21–34.CrossRefGoogle ScholarPubMed
Christensen, A.H. and Quail, P.H. (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research 5, 213–218.CrossRefGoogle ScholarPubMed
Fujii, H. and Zhu, J.-K. (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proceedings of the National Academy of Sciences, USA 106, 8380–8385.CrossRefGoogle ScholarPubMed
Garcia, M.E., Lynch, T., Peeters, J., Snowden, C. and Finkelstein, R. (2008) A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Molecular Biology 67, 643–658.CrossRefGoogle ScholarPubMed
Gómez-Cadenas, A., Verhey, S.D., Hollapa, L.D., Shen, Q., Ho, T.-H.D. and Walker-Simmons, M.K. (1999) An abscisic acid-induced protein kinase, PKABA1, mediates abscisic-acid suppressed gene expression in barley aleurone layers. Proceedings of the National Academy of Sciences, USA 96, 1767–1772.CrossRefGoogle ScholarPubMed
Gómez-Cadenas, A., Zentella, R., Walker-Simmons, M.K. and Ho, T.-H.D. (2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. Plant Cell 13, 667–679.CrossRefGoogle ScholarPubMed
Gubler, F., Raventos, D., Keys, M., Watts, R., Mundy, J. and Jacobsen, J.V. (1999) Target genes and regulatory domains of the GAMYB transcription activator in cereal aleurone. Plant Journal 17, 1–9.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hong, J.Y., Chae, M.J., Lee, Y.N., Nam, M.H., Kim, D.Y. and Byun, M.O. (2011) Phosphorylation-mediated regulation of a rice ABA responsive element binding factor. Phytochemistry 72, 27–36.CrossRefGoogle ScholarPubMed
Hong, Y.-F., Ho, T.-H.D., Wu, C.-F., Lo, S.-L., Yeh, R.-H., Lu, C.-A., Chen, P.-W., Yu, L.-C., Chao, A. and Yu, S.-M. (2012) Convergent starvation signals and hormone crosstalk in regulating nutrient mobilization upon germination in cereals. Plant, Cell and Environment 24, 2857–2873.CrossRefGoogle ScholarPubMed
Jacobsen, J., Pearce, D.W., Poole, A.T., Pharis, R.T. and Mander, L.N. (2002) Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiologia Plantarum 115, 428–441.CrossRefGoogle ScholarPubMed
Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedeman, J., Kroj, T. and Parcy, F. (2002) bZIP transcription factors in Arabidopsis. Trends in Plant Science 7, 106–111.CrossRefGoogle ScholarPubMed
Johnson, R. (2003) Seed development: germination. pp. 1298–1304in Thomas, B.; Murphy, D.; Murray, B. (Eds) Encyclopedia of applied plant science. London, Academic Press.CrossRefGoogle Scholar
Johnson, R.R., Wagner, R.L., Verhey, S.D. and Walker-Simmons, M.K. (2002) The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiology 130, 837–846.CrossRefGoogle ScholarPubMed
Johnson, R.R., Shin, M. and Shen, J.Q. (2008) The wheat PKABA1-interacting factor TaABF1 mediates both abscisic acid-suppressed and abscisic acid-induced gene expression in bombarded aleurone cells. Plant Molecular Biology 68, 93–103.CrossRefGoogle ScholarPubMed
Kagaya, Y., Hobo, T., Murata, M., Ban, A. and Hattori, T. (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14, 3177–3189.CrossRefGoogle ScholarPubMed
Lanahan, M.B., Ho, T.-H.D., Rogers, S.W. and Rogers, J.C. (1992) A gibberellin response complex in cereal alpha-amylase gene promoters. Plant Cell 4, 203–211.Google ScholarPubMed
Lopez-Molina, L., Mongrand, S. and Chua, N.-H. (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proceedings of the National Academy of Sciences, USA 98, 4782–4787.CrossRefGoogle ScholarPubMed
Lovegrove, A. and Hooley, R. (2000) Gibberellin and abscisic acid signaling in aleurone. Trends in Plant Science 5, 102–110.CrossRefGoogle ScholarPubMed
Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A. and Grill, E. (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064–1068.CrossRefGoogle ScholarPubMed
Mendiondo, G.M., Leymarie, J., Farrant, J.M., Corbineau, F. and Benech-Arnold, R.L. (2010) Differential expression of abscisic acid metabolism and signalling genes induced by seed-covering structures or hypoxia in barley (Hordeum vulgare L.) grains. Seed Science Research 20, 69–77.CrossRefGoogle Scholar
Miura, K., Lee, J., Jin, J.B., Yoo, C.Y., Miura, T. and Hasegawa, P.M. (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signalling. Proceedings of the National Academy of Sciences, USA 106, 5418–5423.CrossRefGoogle Scholar
Ohnishi, N., Himi, E., Yamasaki, Y. and Noda, K. (2008) Differential expression of three ABA-insensitive five binding protein (AFP)-like genes in wheat. Genes and Genetic Systems 83, 167–177.CrossRefGoogle ScholarPubMed
Park, S.-Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H.F., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.-f.F., et al, (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071.CrossRefGoogle ScholarPubMed
Piskurewicz, U., Jikumara, Y., Kinoshita, N., Nambara, E., Kamiya, Y. and Lopez-Molina, L. (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20, 2729–2745.CrossRefGoogle ScholarPubMed
Reid, J.L. and Walker-Simmons, M.K. (1990) Synthesis of abscisic acid-responsive, heat-stable proteins in embryonic axes of dormant wheat grain. Plant Physiology 93, 662–667.CrossRefGoogle Scholar
Rikiishi, K., Matsuura, T. and Maekawa, M. (2010) TaABF1, ABA response element binding factor 1, is related to seed dormancy and ABA sensitivity in wheat (Triticum aestivum) seeds. Journal of Cereal Science 52, 236–238.CrossRefGoogle Scholar
Ritchie, S. and Gilroy, S. (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proceedings of the National Academy of Sciences, USA 95, 2697–2702.CrossRefGoogle ScholarPubMed
Schoonheim, P.J., Sinnige, M.P., Casaretto, J.A., Veiga, H., Bunney, T.D., Quatrano, R.S. and de Boer, A.H. (2007) 14-3-3 adaptor proteins are intermediates in ABA signal transduction during barley seed germination. Plant Journal 49, 289–301.CrossRefGoogle ScholarPubMed
Schoonheim, P.J., Da Costa Pereira, D. and De Boer, A.H. (2009) Dual role for 14-3-3 proteins and ABF transcription factors in gibberellic acid and abscisic acid signalling in barley aleurone cells. Plant, Cell and Environment 32, 439–447.CrossRefGoogle Scholar
Schutze, K., Harter, K. and Chaban, C. (2008) Post-translational regulation of plant bZIP factors. Trends in Plant Science 13, 247–255.CrossRefGoogle ScholarPubMed
Shen, Q., Uknes, S.J. and Ho, T.-H.D. (1993) Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene. Journal of Biological Chemistry 268, 23652–23660.CrossRefGoogle Scholar
Shen, Q., Zhang, P. and Ho, T.-H.D. (1996) Modular nature of abscisic acid (ABA) response complexes; composite promoter units that are necessary and sufficient for ABA induction of gene expression. Plant Cell 8, 1107–1119.Google ScholarPubMed
Sirichandra, C., Davanture, M., Turk, B.E., Zivy, M., Valot, B., Leung, J. and Merlot, S. (2010) The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5, e13935.CrossRefGoogle ScholarPubMed
Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D. and Callis, J. (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development is involved in abscisic acid signaling. Plant Cell 18, 3415–3428.CrossRefGoogle ScholarPubMed
Takemiya, A. and Shimazaki, K. (2010) Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase 1. Plant Physiology 153, 1555–1562.CrossRefGoogle ScholarPubMed
Xie, Z., Zhang, Z.-L., Zou, X., Yang, G., Komatsu, S. and Shen, Q.J. (2006) Interactions of two abscisic acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant Journal 46, 231–242.CrossRefGoogle ScholarPubMed
Zhang, Y., Yang, C., Li, Y., Zheng, N., Chen, H., Zhao, Q., Gao, T., Guo, H. and Xie, Q. (2007) SDIR1 is a RING finger E3 ligase that positively regulates abscisic acid signaling in Arabidopsis. Plant Cell 19, 1912–1929.CrossRefGoogle ScholarPubMed
Zhang, Z.-L., Shin, M., Zou, X., Huang, J., Ho, T.-H.D. and Shen, Q.J. (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Molecular Biology 70, 139–151.CrossRefGoogle ScholarPubMed
Zou, M., Guan, Y., Ren, H., Zhang, F. and Chen, F. (2008) A bZIP transcription factor, OSABI5, is involved in rice fertility and stress tolerance. Plant Molecular Biology 66, 675–683.CrossRefGoogle ScholarPubMed
Zou, X., Seeman, J.R., Neuman, D. and Shen, Q.J. (2004) A WRKY gene from creosote bush encodes an activator of the abscisic acid signaling pathway. Journal of Biological Chemistry 279, 55770–55779.CrossRefGoogle ScholarPubMed
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