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Transcriptional regulatory activity of the cereal grain bZip protein TaABF1 can be either stimulated or inhibited by phosphorylation

Published online by Cambridge University Press:  01 February 2019

Alison E. Smith ,
Xi Yang ,
Justin Lutian ,
David Chelimo ,
Juvenal Lopez ,
Grace Uwase  and
Russell R. Johnson Open the ORCID record for Russell R. Johnson [Opens in a new window]
Alison E. Smith
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
Xi Yang
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
Justin Lutian
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
David Chelimo
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
Juvenal Lopez
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
Grace Uwase
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
Russell R. Johnson*
Affiliation:
Department of Biology, Colby College, 5723 Mayflower Hill, Waterville ME 04901, USA
*
Author for correspondence: Russell R. Johnson, Email: russ.johnson@colby.edu
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Abstract

The wheat bZip transcription factor TaABF1 mediates both abscisic acid (ABA)-induced and ABA-suppressed gene expression. As levels of TaABF1 protein do not change in response to ABA, and TaABF1 is in a phosphorylated state in vivo, we investigated whether TaABF1 could be regulated at the post-translational level. In bombarded aleurone cells, a TaABF1 protein carrying phosphomimetic mutations (serine to aspartate) at four sites (S36D, S37D, S113D, S115D) was three to five times more potent than wild-type TaABF1 in activating HVA1, an ABA-responsive gene. The phosphomimetic mutations also increased the ability of TaABF1 to downregulate the ABA-suppressed gene Amy32b. These findings strongly suggest that phosphorylation at these sites increases the transcriptional regulatory activity of TaABF1. In contrast to the activation observed by the quadruple serine to aspartate mutation, a single S113D mutation completely eliminated the ability of TaABF1 to upregulate HVA1 or downregulate Amy32b. Thus phosphorylation of TaABF1 can either stimulate or inhibit the activity of TaABF1 in regulating downstream genes, depending on the site and pattern of phosphorylation. Mutation of S318 and S322 (in the bZIP domain) eliminated the ability of TaABF1 to activate HVA1, but had no effect on the ability of TaABF1 to downregulate Amy32b, suggesting that TaABF1 represses Amy32b expression through a mechanism other than direct DNA binding. An important step towards understanding how ABA and gibberellin (GA) signals are integrated through TaABF1 phosphorylation to regulate downstream gene expression is to clarify the effects of those hormones on the expression of specific genes. In contrast to some other ABA-induced genes, we found that HVA1 induction by ABA or TaABF1 is not inhibited by GA.

Keywords

abscisic acidgerminationgibberellinimbibitionphosphorylationwheat
Type
Research Paper
Information
Seed Science Research , Volume 29 , Issue 1 , March 2019 , pp. 21 - 28
Copyright
Copyright © Cambridge University Press 2019 

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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.Google Scholar
Chen, K. and An, Y.-Q.C. (2006) Transcriptional responses to gibberellin and abscisic acid in barley aleurone. Journal of Integrative Plant Biology 48, 591–612.Google Scholar
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.Google Scholar
Feng, C.-Z., Chen, Y., Wang, C., Hong, Y.-H., Wu, W.-H. and Chen, Y.-F. (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant Journal 80, 654–668.Google Scholar
Finkelstein, R., Gampala, S.S.L., Lynch, T.J., Thomas, T.L. and Rock, C.D. (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR(ABF)3. Plant Molecular Biology 59, 253–267.Google Scholar
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 of the USA 106, 8380–8385.Google Scholar
Fujita, Y., Yoshida, T. and Yamaguchi-Shinozaki, (2013) Pivotal role of the AREB/ABF-SnRK pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiologia Plantarum 147, 15–27.Google Scholar
Furihata, T., Maruyama, K., Umezawa, T., Yoshida, R., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences of the USA 103, 1988–1993.Google Scholar
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.Google Scholar
Guo, G.Liu, X., Sun, F., Cao, J., Huo, N., Wuda, B., Xin, M., Hu, Z., Du, J., Xia, R., Rossi, V., Peng, H., Ni, Z., Sun, Q. and Yao, Y. (2018) Wheat miR9678 affects seed germination by generating phased siRNAs and modulating abscisic acid/gibberellin signaling. Plant Physiology 30, 796–814.Google Scholar
Harris, L.J., Martinez, S.A., Keyser, B.R., Dyer, W.E. and Johnson, R.R. (2013) Functional analysis of TaABF1 during abscisic acid and gibberellin signaling in aleurone cells of cereal grains. Seed Science Research 23, 89–98.Google Scholar
Hong, B., Barg, R. and Ho, T.-H.D. (1992) Developmental and organ-specific expression of an ABA- and stress-induced protein in barley. Plant Molecular Biology 18, 663–674.Google Scholar
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.Google Scholar
Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T. and Parcy, F. (2002) bZIP transcription factors in Arabidopsis. Trends in Plant Science 7, 106–111.Google Scholar
Johnson, R.R. (2003) Seed development: Germination, pp. 1298–1304 in Thomas, B., Murphy, D. and Murray, B. (eds), Encyclopedia of Applied Plant Sciences. London, Academic Press.Google Scholar
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.Google 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.Google Scholar
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.Google Scholar
Lanahan, M.B., Ho, T.-H., Rogers, S.W. and Rogers, J.C. (1992) A gibberellin response complex in cereal alpha-amylase gene promoters. Plant Cell 4, 203–211.Google Scholar
Li, X., Feng, B., Zhang, F., Tang, Y., Zhang, L., Ma, L., Zhao, C. and Gao, S. (2016) Bioinformatic analyses of sugroup-A members of the wheat bZIP transcription factor family and functional identification of TabZIP174 involved in drought stress response. Frontiers in Plant Science 7, 1643.Google Scholar
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 of the USA 98, 4782–4787.Google Scholar
Lovegrove, A. and Hooley, R. (2000) Gibberellin and abscisic acid signaling in aleurone. Trends in Plant Science 5, 102–110.Google Scholar
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.Google 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.Google Scholar
Park, S.-Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H.F., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.-F., Alfred, S.E., Bonetta, D., Finkelstein, R., Provart, N.J., Desveaux, D., Rodriguez, P.L., McCourt, P., Zhu, J.-K., Schroeder, J.I., Volkman, B.F. and Cutler, S.R. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071.Google Scholar
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.Google 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.Google Scholar
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.Google Scholar
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.Google 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 Scholar
Student (1908) The probable error of a mean. Biometrika 6, 1–25.Google Scholar
Uwase, G., Enrico, T.P., Chelimo, D.S., Keyser, B.J. and Johnson, R.R. (2018) Measuring gene expression in bombarded aleurone layers with increased throughput. Journal of Visualized Experiments 133, e56728.Google Scholar
Zheng, Y., Schumaker, K.S. and Guo, Y. (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisis acid response in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 109, 12822–12827.Google Scholar
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.Google Scholar
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