Abstract
WD40 repeat-containing protein 55 (WDR55) is one of the damaged DNA-binding WD40 (DWD) proteins in Arabidopsis, which is known to be involved in plant development of the reproductive and vegetative stages. In this study, we found that WDR55 was induced in plants treated with the phytohormone abscisic acid (ABA) or abiotic stresses, such as drought. Transgenic Arabidopsis plants that overexpress WDR55 showed ABA-hypersensitive phenotypes and tolerance to drought, whilst the wdr55 mutant showed the opposite results. In addition, transcriptome analysis showed that the transcript levels of ABA- and drought-responsive genes were increased in WDR55-overexpresing plants. Furthermore, some ABA-responsive genes, such as RD29B, were regulated through the histone modifications in its promoter region in a WDR55-dependent manner. Taken together, these results suggest that WDR55 plays as a positive regulator in ABA-mediated drought stress response in Arabidopsis.
Similar content being viewed by others
References
Ausubel FM, Brent R, Kingston RE, Moore DD, Seid-Man JG, Smith JA, Struhl K (1987) Phenol/SDS method for plant RNA preparation. Curr Protoc Mol Biol 1:431–434
Bjerkan KN, Grini PE (2013) The Arabidopsis DDB1 interacting protein WDR55 is required for vegetative development. Plant Signal Behav. https://doi.org/10.4161/psb.25347
Bjerkan KN, Jung-Romeo S, Jurgens G, Genschik P, Grini PE (2012) Arabidopsis WD repeat domain55 interacts with DNA damaged binding protein1 and is required for apical patterning in the embryo. Plant Cell 24(3):1013–1033. https://doi.org/10.1105/tpc.111.089425
Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61(12):3345–3353. https://doi.org/10.1093/jxb/erq154
Clement M, Leonhardt N, Droillard MJ, Reiter I, Montillet JL, Genty B, Lauriere C, Nussaume L, Noel LD (2011) The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiol 156(3):1481–1492. https://doi.org/10.1104/pp.111.174425
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Commun 3:740. https://doi.org/10.1038/ncomms1732
Farras R, Ferrando A, Jasik J, Kleinow T, Okresz L, Tiburcio A, Salchert K, del Pozo C, Schell J, Koncz C (2001) SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 20(11):2742–2756. https://doi.org/10.1093/emboj/20.11.2742
Fong HK, Hurley JB, Hopkins RS, Miake-Lye R, Johnson MS, Doolittle RF, Simon MI (1986) Repetitive segmental structure of the transducin beta subunit: homology with the CDC4 gene and identification of related mRNAs. Proc Natl Acad Sci USA 83(7):2162–2166. https://doi.org/10.1073/pnas.83.7.2162
Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19(2):485–494. https://doi.org/10.1105/tpc.106.048538
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17(12):3470–3488. https://doi.org/10.1105/tpc.105.035659
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50(12):2123–2132. https://doi.org/10.1093/pcp/pcp147
Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54(5):767–781. https://doi.org/10.1023/B:PLAN.0000040902.06881.d4
He YJ, McCall CM, Hu J, Zeng Y, Xiong Y (2006) DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev 20(21):2949–2954. https://doi.org/10.1101/gad.1483206
Higa LA, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8(11):1277–1283. https://doi.org/10.1038/ncb1490
Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24(16):1695–1708. https://doi.org/10.1101/gad.1953910
Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47(1):141–153. https://doi.org/10.1093/pcp/pci230
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) ArabidopsisCBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280(5360):104–106. https://doi.org/10.1126/science.280.5360.104
Kim JM, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49(10):1580–1588. https://doi.org/10.1093/pcp/pcn133
Lamke J, Baurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18(1):124. https://doi.org/10.1186/s13059-017-1263-6
Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20(1):152–167. https://doi.org/10.1105/tpc.107.055418
Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22(6):1716–1732. https://doi.org/10.1105/tpc.109.073783
Lee JH, Terzaghi W, Deng XW (2011) DWA3, an Arabidopsis DWD protein, acts as a negative regulator in ABA signal transduction. Plant Sci 180(2):352–357. https://doi.org/10.1016/j.plantsci.2010.10.008
Nakagawa T, Xiong Y (2011) X-linked mental retardation gene CUL4B targets ubiquitylation of H3K4 methyltransferase component WDR5 and regulates neuronal gene expression. Mol Cell 43(3):381–391. https://doi.org/10.1016/j.molcel.2011.05.033
Pandey G, Sharma N, Sahu PP, Prasad M (2016) Chromatin-based epigenetic regulation of plant abiotic stress response. Curr Genom 17(6):490–498. https://doi.org/10.2174/1389202917666160520103914
Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6(1):9–20. https://doi.org/10.1038/nrm1547
Rice JC, Allis CD (2001) Code of silence. Nature 414(6861):258–261. https://doi.org/10.1038/35104721
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290(3):998–1009. https://doi.org/10.1006/bbrc.2001.6299
Seo KI, Lee JH, Nezames CD, Zhong S, Song E, Byun MO, Deng XW (2014) ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling. Plant Cell 26(2):695–711. https://doi.org/10.1105/tpc.113.119974
Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826. https://doi.org/10.1038/nature05176
Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24(5):181–185. https://doi.org/10.1016/s0968-0004(99)01384-5
Struhl K (1998) Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12(5):599–606. https://doi.org/10.1101/gad.12.5.599
Tsugama D, Liu S, Takano T (2013) Arabidopsis heterotrimeric G protein beta subunit, AGB1, regulates brassinosteroid signalling independently of BZR1. J Exp Bot 64(11):3213–3223. https://doi.org/10.1093/jxb/ert159
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97(21):11632–11637. https://doi.org/10.1073/pnas.190309197
van Nocker S, Ludwig P (2003) The WD-repeat protein superfamily in Arabidopsis: conservation and divergence in structure and function. BMC Genom 4(1):50. https://doi.org/10.1186/1471-2164-4-50
Wu FQ, Xin Q, Cao Z, Liu ZQ, Du SY, Mei C, Zhao CX, Wang XF, Shang Y, Jiang T, Zhang XF, Yan L, Zhao R, Cui ZN, Liu R, Sun HL, Yang XL, Su Z, Zhang DP (2009) The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol 150(4):1940–1954. https://doi.org/10.1104/pp.109.140731
Xu DB, Chen M, Ma YN, Xu ZS, Li LC, Chen YF, Ma YZ (2015) A G-protein beta subunit, AGB1, negatively regulates the ABA response and drought tolerance by down-regulating AtMPK6-related pathway in Arabidopsis. PLoS ONE 10(1):e0116385. https://doi.org/10.1371/journal.pone.0116385
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61(4):672–685. https://doi.org/10.1111/j.1365-313X.2009.04092.x
Zhao Y, Shen Y, Yang S, Wang J, Hu Q, Wang Y, He Q (2010) Ubiquitin ligase components Cullin4 and DDB1 are essential for DNA methylation in Neurospora crassa. J Biol Chem 285(7):4355–4365. https://doi.org/10.1074/jbc.M109.034710
Zou XD, Hu XJ, Ma J, Li T, Ye ZQ, Wu YD (2016) Genome-wide analysis of WD40 protein family in human. Sci Rep 6:39262. https://doi.org/10.1038/srep39262
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Park, SR., Hwang, J. & Kim, M. The Arabidopsis WDR55 is positively involved in ABA-mediated drought tolerance response. Plant Biotechnol Rep 14, 407–418 (2020). https://doi.org/10.1007/s11816-020-00615-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11816-020-00615-8