Dynamic subnuclear relocalisation of WRKY40 in response to Abscisic acid in Arabidopsis thaliana

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Geilen, Katja ^a   Böhmer, Maik ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; PHYTOCHROME B; TRANSCRIPTION FACTOR; WRKY40 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; CELL NUCLEUS; DRUG EFFECTS; FLUORESCENCE; METABOLISM; PLANT LEAF; PROTEIN TRANSPORT; PROTOPLAST; TOBACCO;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; FLUORESCENCE; PHYTOCHROME B; PLANT LEAVES; PROTEIN TRANSPORT; PROTOPLASTS; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84939824612     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13369     Document Type: Article

References (68)

1. Kim, T. H., Böhmer, M., Hu, H., Nishimura, N. & Schroeder, J. I. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2 + signaling. Annu Rev Plant Biol 61, 561-591, doi: 10.1146/annurev-arplant-042809-112226 (2010).
2. Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R. & Abrams, S. R. Abscisic Acid: Emergence of a Core Signaling Network. Annual Review of Plant Biology 61, doi: 10.1146/annurev-arplant-042809-112122 (2010).
3. Sawinski, K., Mersmann, S., Robatzek, S. & Böhmer, M. Guarding the green: pathways to stomatal immunity. Mol Plant Microbe Interact 26, 626-632, doi: 10.1094/MPMI-12-12-0288-CR (2013).
4. Hoth, S. et al. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115, 4891-4900 (2002).
5. Leonhardt, N. et al. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16, 596-615 (2004).
6. Okamoto, M. et al. Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62, 39-51, doi: 10.1111/j.1365-313X.2010.04135.x (2010).
7. Ma, Y. et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068, doi: 10.1126/science.1172408 (2009).
8. Park, S. Y. et al. Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science 324, 1068-1071, doi: 10.1126/science.1173041 (2009).
9. Yoshida, R. et al. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281, 5310-5318 (2006).
10. Umezawa, T. et al. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 106, 17588-17593, doi: 10.1073/pnas.0907095106 (2009).
11. Vlad, F. et al. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21, 3170-3184, doi: 10.1105/tpc.109.069179 (2009).
12. Kwak, J. M. et al. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. Embo J 22, 2623-2633 (2003).
13. Sirichandra, C. et al. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. Febs Letters 583, 2982-2986, doi: 10.1016/j.febslet.2009.08.033 (2009).
14. Böhmer, M. & Schroeder, J. I. Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen speciesdependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant Journal 67, 105-118, doi: 10.1111/j.1365-313X.2011.04579.x (2011).
15. Fujita, Y. et al. Three SnRK2 Protein Kinases are the Main Positive Regulators of Abscisic Acid Signaling in Response to Water Stress in Arabidopsis. Plant and Cell Physiology 50, 2123-2132, doi: 10.1093/pcp/pcp147 (2009).
16. Nakashima, K. et al. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant and Cell Physiology 50, 1345-1363, doi: 10.1093/pcp/pcp083 (2009).
17. Fujii, H., Verslues, P. E. & Zhu, J. K. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19, 485-494, doi: 10.1105/tpc.106.048538 (2007).
18. Sirichandra, C. et al. 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, doi: 10.1371/journal.pone.0013935 (2010).
19. Cominelli, E. et al. A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Current Biology 15, 1196-1200 (2005).
20. Jung, C. et al. Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146, 623-635, doi: 10.1104/pp.107.110981 (2008).
21. Li, W. X. et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20, 2238-2251, doi: 10.1105/tpc.108.059444 (2008).
22. Nelson, D. E. et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104, 16450-16455, doi: 10.1073/pnas.0707193104 (2007).
23. Liang, Y. K. et al. AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Current Biology 15, 1201-1206 (2005).
24. Song, C. P. et al. Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384-2396, doi: 10.1105/tpc.105.033043 (2005).
25. Rushton, P., Macdonald, H., Huttly, A., Lazarus, C. & Hooley, R. Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy2 genes. Plant Molecular Biology 29, 691-702 (1995).
26. Jiang, W. & Yu, D. Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid. Bmc Plant Biology 9, 96 (2009).
27. Ren, X. et al. ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant Journal 63, 417-429, doi: 10.1111/j.1365-313X.2010.04248.x (2010).
28. Shang, Y. et al. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22, 1909-1935, doi: 10.1105/tpc.110.073874 (2010).
29. Chen, H. et al. Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10, 281, doi: 10.1186/1471-2229-10-281 (2010).
30. Ding, Z. J. et al. Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79, 13-27, doi: 10.1111/tpj.12538 (2014).
31. Eulgem, T., Rushton, P., Robatzek, S. & Somssich, I. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199-206 (2000).
32. Pandey, S. P., Roccaro, M., Schön, M., Logemann, E. & Somssich, I. E. Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64, 912-923, doi: 10.1111/j.1365-313X.2010.04387.x (2010).
33. Schön, M. et al. Analyses of wrky18 wrky40 plants reveal critical roles of SA/EDS1 signaling and indole-glucosinolate biosynthesis for G. orontii resistance and a loss-of resistance towards Pto AvrRPS4. Mol Plant Microbe Interact, doi: 10.1094/MPMI-11-12-0265-R (2013).
34. Chen, C. & Chen, Z. Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129, 706-716, doi: 10.1104/pp.001057 (2002).
35. Xu, X., Chen, C., Fan, B. & Chen, Z. Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18, 1310-1326, doi: 10.1105/tpc.105.037523 (2006).
36. Wenke, K. et al. Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J 70, 445-459, doi: 10.1111/j.1365-313X.2011.04891.x (2012).
37. Brotman, Y. et al. Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9, e1003221, doi: 10.1371/journal.ppat.1003221 (2013).
38. Liu, Z. Q. et al. Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis. J Exp Bot 63, 6371-6392, doi: 10.1093/jxb/ers293 (2012).
39. Li, J. et al. Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 418, 793-797 (2002).
40. Ng, C. K., Kinoshita, T., Pandey, S., Shimazaki, K. & Assmann, S. M. Abscisic acid induces rapid subnuclear reorganization in guard cells. Plant Physiol 134, 1327-1331, doi: 10.1104/pp.103.034728 (2004).
41. Riera, M., Redko, Y. & Leung, J. Arabidopsis RNA-binding protein UBA2a relocalizes into nuclear speckles in response to abscisic acid. FEBS Lett 580, 4160-4165, doi: 10.1016/j.febslet.2006.06.064 (2006).
42. Misteli, T. Beyond the sequence: cellular organization of genome function. Cell 128, 787-800, doi: 10.1016/j.cell.2007.01.028 (2007).
43. Shaw, P. J. & Brown, J. W. Plant nuclear bodies. Curr Opin Plant Biol 7, 614-620, doi: 10.1016/j.pbi.2004.09.011 (2004).
44. Sakamoto, K. & Nagatani, A. Nuclear localization activity of phytochrome B. Plant J 10, 859-868 (1996).
45. Kircher, S. et al. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. Plant Cell 11, 1445-1456 (1999).
46. Yamaguchi, R., Nakamura, M., Mochizuki, N., Kay, S. A. & Nagatani, A. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J Cell Biol 145, 437-445 (1999).
47. Kircher, S. et al. Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14, 1541-1555 (2002).
48. Chen, M., Schwab, R. & Chory, J. Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc Natl Acad Sci USA 100, 14493-14498, doi: 10.1073/pnas.1935989100 (2003).
49. Chen, M. Phytochrome nuclear body: an emerging model to study interphase nuclear dynamics and signaling. Curr. Opinion in Plant Biol. 11, 503-508, doi: http://dx.doi.org/10.1016/j.pbi.2008.06.012 (2008).
50. Trupkin, S., Legris, M., Buchovsky, A. S., Tolava Rivero, M. B. & Casal, J. Phytochrome B nuclear bodies respond to the low red/far-red ratio and to the reduced irradiance of canopy shade in Arabidopsis. Plant Physiol, doi: 10.1104/pp.114.242438 (2014).
51. Van Buskirk, E. K., Decker, P. V. & Chen, M. Photobodies in light signaling. Plant Physiol 158, 52-60, doi: 10.1104/pp.111.186411 (2012).
52. Ni, M., Tepperman, J. M. & Quail, P. H. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400, 781-784, doi: 10.1038/23500 (1999).
53. Huq, E. & Quail, P. H. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21, 2441-2450, doi: 10.1093/emboj/21.10.2441 (2002).
54. Llorca, C. M., Potschin, M. & Zentgraf, U. bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front Plant Sci 5, 169, doi: 10.3389/fpls.2014.00169 (2014).
55. Liu, D., Leib, K., Zhao, P., Kogel, K. H. & Langen, G. Phylogenetic analysis of barley WRKY proteins and characterization of HvWRKY1 and-2 as repressors of the pathogen-inducible gene HvGER4c. Mol Genet Genomics 289, 1331-1345, doi: 10.1007/s00438-014-0893-6 (2014).
56. Yang, Y., Costa, A., Leonhardt, N., Siegel, R. S. & Schroeder, J. I. Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4, 6, doi: 1746-4811-4-6 [pii]10.1186/1746-4811-4-6 (2008).
57. Rausenberger, J. et al. An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS One 5, e10721, doi: 10.1371/journal.pone.0010721 (2010).
58. Lopez-Molina, L., Mongrand, S., Kinoshita, N. & Chua, N. H. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17, 410-418, doi: 10.1101/gad.1055803 (2003).
59. Liu, R. et al. Light-harvesting chlorophyll a/b-binding proteins, positively involved in abscisic acid signalling, require a transcription repressor, WRKY40, to balance their function. J Exp Bot 64, 5443-5456, doi: 10.1093/jxb/ert307 (2013).
60. Xu, D. et al. Convergence of Light and ABA signaling on the ABI5 promoter. PLoS Genet 10, e1004197, doi: 10.1371/journal. pgen.1004197 (2014).
61. Seo, M. et al. Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48, 354-366, doi: 10.1111/j.1365-313X.2006.02881.x (2006).
62. Monte, E. et al. The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development. Proc Natl Acad Sci USA 101, 16091-16098, doi: 10.1073/pnas.0407107101 (2004).
63. Chen, H. et al. Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105, 4495-4500, doi: 10.1073/pnas.0710778105 (2008).
64. Fujii, H. & Zhu, J. K. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106, 8380-8385, doi: 10.1073/pnas.0903144106 (2009).
65. Feys, B. J. et al. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601-2613, doi: 10.1105/tpc.105.033910 (2005).
66. Jakoby, M. J. et al. Analysis of the subcellular localization, function, and proteolytic control of the Arabidopsis cyclin-dependent kinase inhibitor ICK1/KRP1. Plant Physiol 141, 1293-1305, doi: 10.1104/pp.106.081406 (2006).
67. Marion, J. et al. Systematic analysis of protein subcellular localization and interaction using high-throughput transient transformation of Arabidopsis seedlings. Plant J 56, 169-179, doi: 10.1111/j.1365-313X.2008.03596.x (2008).
68. Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2, 1565-1572, doi: 10.1038/nprot.2007.199 (2007).