Journal of Plant Research

, Volume 130, Issue 3, pp 587–598 | Cite as

CKB1 is involved in abscisic acid and gibberellic acid signaling to regulate stress responses in Arabidopsis thaliana

  • Congying Yuan
  • Jianping Ai
  • Hongping Chang
  • Wenjun Xiao
  • Lu Liu
  • Cheng Zhang
  • Zhuang He
  • Ji Huang
  • Jinyan Li
  • Xinhong Guo
Regular Paper


Casein kinase II (CK2), an evolutionarily well-conserved Ser/Thr kinase, plays critical roles in all higher organisms including plants. CKB1 is a regulatory subunit beta of CK2. In this study, homozygous T-DNA mutants (ckb1-1 and ckb1-2) and over-expression plants (35S:CKB1-1, 35S:CKB1-2) of Arabidopsis thaliana were studied to understand the role of CKB1 in abiotic stress and gibberellic acid (GA) signaling. Histochemical staining showed that although CKB1 was expressed in all organs, it had a relatively higher expression in conducting tissues. The ckb1 mutants showed reduced sensitivity to abscisic acid (ABA) during seed germination and seedling growth. The increased stomatal aperture, leaf water loss and proline accumulation were observed in ckb1 mutants. In contrast, the ckb1 mutant had increased sensitivity to polyaluminum chloride during seed germination and hypocotyl elongation. We obtained opposite results in over-expression plants. The expression levels of a number of genes in the ABA and GA regulatory network had changed. This study demonstrates that CKB1 is an ABA signaling-related gene, which subsequently influences GA metabolism, and may play a positive role in ABA signaling.


Casein kinase II ABA GA Signaling T-DNA mutants Over-expression 



We thank Professor Xianming Chen, from Wheat Genetics, Quality, Physiology, and Disease Research Unit, USDA-ARS, and Department of Plant Pathology, Washington State University, for revising this paper. This research was supported by Grants from the National Key Laboratory of Plant Molecular Genetics (2015), the National Natural Science Foundation of China (31540064, 31071076 and 30871325), the Program for New Century Excellent Talents in University (NCET-10-0363), the Excellent Youth Foundation of Hunan Province (11JJ1005), the Ph.D. Programs Foundation of Ministry of Education of China (20130161110005), Hunan Provincial Innovation Foundation for Postgraduate (CX2015B073, CX2016B097), and Key Research and Development Project of Hunan Provincial Department of Science and Technology (2016WK2003).


  1. Allada R, Meissner RA (2005) Casein kinase 2, circadian clocks, and the flight from mutagenic light. Mol Cell Biochem 274:141–149. doi: 10.1007/s11010-005-2943-1 CrossRefPubMedGoogle Scholar
  2. Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889. doi: 10.1074/jbc.M307151200 CrossRefPubMedGoogle Scholar
  3. Bolduc N, Hake S (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene GA2ox1. Plant Cell 21:1647–1658. doi: 10.1105/tpc.109.068221 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bu Q, Zhu L, Dennis MD, Yu L, Lu SX, Person MD, Tobin EM, Browning KS, Huq E (2010) Phosphorylation by CK2 enhances the rapid light-induced degradation of phytochrome interacting factor 1 in Arabidopsis. J Biol Chem 286:12066–12074. doi: 10.1074/jbc.M110.186882 CrossRefGoogle Scholar
  5. Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M, Hell R, Zhu JK, Xiang CB (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:04–615. doi: 10.1111/tpj.12407 CrossRefGoogle Scholar
  6. Chen J, Wang Y, Wang F, Yang J, Gao M, Li C, Liu Y, Liu Y, Yamaji N, Ma JF, Paz-Ares J, Nussaume L, Zhang S, Yi K, Wu Z, Wu P (2015) The rice CK2 kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell 114:135335. doi: 10.1105/tpc.114.135335 Google Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi: 10.1046/j.1365-313x.199800343.x CrossRefPubMedGoogle Scholar
  8. Collinge MA, Walker JC (1994) Isolation of an Arabidopsis thaliana casein kinase II beta subunit by complementation in Saccharomyces cerevisiae. Plant Mol Biol 25:649–658CrossRefPubMedGoogle Scholar
  9. Galán-Caridad JM, Calabokis M, Uzcanga G, Aponte F, Bubis J (2004) Identification of casein kinase 1, casein kinase 2, and cAMP dependent protein kinase-like activities in Trypanosoma evansi. Memórias do Instituto Oswaldo Cruz 99:845–854. doi: 10.1590/S0074-02762004000800011 CrossRefPubMedGoogle Scholar
  10. Galau GA, Hughes DW, Dure L 3rd (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155–170. doi: 10.1007/bf00021327 CrossRefPubMedGoogle Scholar
  11. Godoy J, Lunar R, Torres-Schumann S, Moreno J, Rodrigo R, Pintor-Toro J (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26:1921–1934. doi: 10.1007/BF00019503 CrossRefPubMedGoogle Scholar
  12. Gong X, Zhang J, Liu JH (2014) A stress responsive gene of Fortunella crassifolia FcSISP functions in salt stress resistance. Plant Physiol Biochem 83:10–19. doi: 10.1016/j.plaphy.2014.07.003 CrossRefPubMedGoogle Scholar
  13. Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C (2015) Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27:1945–1954. doi: 10.1105/tpc.15.00421 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hardtke CS, Deng XW (2000) The cell biology of the COP/DET/FUS proteins. Regulating proteolysis in photo morphogenesis and beyond? Plant Physiol 124:1548–1557. doi: 10.1104/pp.124.4.1548 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hong JY, Chae MJ, Lee IS, Lee YN, Nam MH, Kim DY, Byun MO, Yoon IS (2011) Phosphorylation-mediated regulation of arice ABA responsive element binding factor. Photochemistry 72:27–36. doi: 10.1016/j.phytochem.2010.10.005 CrossRefGoogle Scholar
  16. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403. doi: 10.1146/annurev.arplant.47.1.377 CrossRefPubMedGoogle Scholar
  17. Lee HG, Lee K, Seo PJ (2015) The Arabidopsis MYB96 transcription factor plays a role in seed dormancy. Plant Mol Biol 87:371–381. doi: 10.1007/s11103-015-0283-4 CrossRefPubMedGoogle Scholar
  18. Li C, Liu Z, Zhang Q, Wang R, Xiao L, Ma H, Chong K, Xu Y (2012) SKP1 is involved in abscisic acid signaling to regulate seed germination, stomatal opening and root growth in Arabidopsis thaliana. Plant Cell Environ 35:952–965. doi: 10.1111/j.1365-3040.201102464.x CrossRefPubMedGoogle Scholar
  19. Lim CW, Baek W, Han SW, Lee SC (2013) Arabidopsis PYL8 plays an important role for ABA signaling and drought stress responses. Plant Pathol J 29:471–476. doi: 10.5423/PPJ.NT.07.2013.0071 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Liu Y, Wang L, Jiang S, Pan J, Cai G, Li D (2014) Group 5 LEA protein, ZmLEA5C, enhance tolerance to osmotic and low temperature stresses in transgenic tobacco and yeast. Plant Physiol Biochem 84:22–31. doi: 10.1016/j.plaphy.2014.08.016 CrossRefPubMedGoogle Scholar
  21. Liu J, He H, Vitali M, Visentin I, Charnikhova T, Haider I, Schubert A, Ruyter-Spira C, Bouwmeester HJ, Lovisolo C, Cardinale F (2015) Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241:1435–1451. doi: 10.1007/s00425-015-2266-8 CrossRefPubMedGoogle Scholar
  22. Loizou JI, El-Khamisy SF, Zlatanou A, Moore DJ, Chan DW, Qin J, Sarno S, Meggio F, Pinna LA, Caldecott KW (2004) The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell 117:17–28. doi: 10.1016/S0092-8674(04)00206 CrossRefPubMedGoogle Scholar
  23. Marquès-Bueno MM, Moreno-Romero J, Abas L, de Michele R, Martínez MC (2011) Linking protein kinase CK2 and auxin transport. Plant Signal Behav 6:1603–1605. doi: 10.4161/psb.6.10.17136 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349–368. doi: 10.1096/fj.02-0473rev CrossRefPubMedGoogle Scholar
  25. Ogiso E, Takahashi Y, Sasaki T, Yano M, Izawa T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820. doi: 10.1104/pp.109.148908 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Olesen SH, Ingles DJ, Zhu JY, Martin MP, Betzi S, Georg GI, Tash JS, Schönbrunn E (2015) Stability of the human Hsp90-p50Cdc37 chaperone complex against nucleotides and Hsp90 inhibitors, and the influence of phosphorylation by casein kinase 2. Molecules 20:1643–1660. doi: 10.3390/molecules20011643 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Olsten ME, Litchfield DW (2004) Order or chaos? An evaluation of the regulation of protein kinase CK2. Biochem Cell Biol 82:681–693. doi: 10.1139/o04-116 CrossRefPubMedGoogle Scholar
  28. Pinedo I, Ledger T, Greve M, Poupin MJ (2015) Burkholderia phytofirmans PsJN induces long-term metabolic and transcriptional changes involved in Arabidopsis thaliana salt tolerance. Front Plant Sci 6:466. doi: 10.3389/fpls.2015.00466 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, 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. doi: 10.1105/tpc.108.061515 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pizzio GA, Rodriguez L, Antoni R, Gonzalez-Guzman M, Yunta C, Merilo E, Kollist H, Albert A, Rodriguez PL (2013) The PYL4 A194T mutant uncovers a key role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signaling and plant drought resistance. Plant Physiol 163:441–455. doi: 10.1104/pp.113.224162 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Plana M, Itarte E, Eritja R, Goday A, Pages M, Martinez MC (1991) Phosphorylation of maize RAB-17 protein by casein kinase 2. J Biol Chem 266:22510–22514PubMedGoogle Scholar
  32. Portolés S, Más P (2007) Altered oscillator function affects clock resonance and is responsible for the reduced day-length sensitivity of CKB4 overexpressing plants. Plant J 51:966–977. doi: 10.1111/j.1365-313X.200703186.x CrossRefPubMedGoogle Scholar
  33. Qin LX, Li Y, Li DD, Xu WL, Zheng Y, Li XB (2014) Arabidopsis drought-induced protein Di19-3 participates in plant response to drought and high salinity stresses. Plant Mol Biol 86:609–625. doi: 10.1007/s11103-014-0251-4 CrossRefPubMedGoogle Scholar
  34. Regnault T, Davière JM, Heintz D, Lange T, Achard P (2014) The gibberellin biosynthetic genes AtKAO1 and AtKAO2 have overlapping roles throughout Arabidopsis development. Plant J 80:462–474. doi: 10.1111/tpj.12648 CrossRefPubMedGoogle Scholar
  35. Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158. doi: 10.1199/tab.0158 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Salinas P, Fuentes D, Vidal E, Jordana X, Echeverria M, Holuigue L (2006) An extensive survey of CK2 alpha and beta subunits in Arabidopsis: multiple isoforms exhibit differential subcellular localization. Plant Cell Physiol 47:1295–1308. doi: 10.1093/pcp/pcj100 CrossRefPubMedGoogle Scholar
  37. Sanchez-Casalongue ME, Lee J, Diamond A, Shuldiner S, Moir RD, Willis IM (2015) Differential phosphorylation of a regulatory subunit of protein kinase CK2 by TOR complex 1 signaling and the Cdc-like kinase. J Biol Chem 290:7221–7233. doi: 10.1074/jbc.M114.626523 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:327–330. doi: 10.1038/35066500 CrossRefPubMedGoogle Scholar
  39. Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signaling. Curr Opin Plant Biol 12:57–62. doi: 10.1016/j.pbi.2008.09.004 CrossRefPubMedGoogle Scholar
  40. Seiler C, Harshavardhan VT, Reddy PS, Hensel G, Kumlehn J, Eschen-Lippold L, Rajesh K, Korzun V, Wobus U, Lee J, Selvaraj G, Sreenivasulu N (2013) Abscisic acid flux alterations result in differential abscisic acid signaling responses and impact assimilation efficiency in barley under terminal drought stress. Plant Physiol 164:1677–1696. doi: 10.1104/pp.113.229062 CrossRefGoogle Scholar
  41. Shan H, Chen S, Jiang J, Chen F, Chen Y, Gu C, Li P, Song A, Zhu X, Gao H, Zhou G, Li T, Yang X (2012) Heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Mol Biotechnol 51:160–173. doi: 10.1007/s12033-011-9451-1 CrossRefPubMedGoogle Scholar
  42. Shi CC, Feng CC, Yang MM, Li JL, Li XX, Zhao BC, Huang ZJ, Ge RC (2014) Overexpression of the receptor-like protein kinase genes AtRPK1 and OsRPK1 reduces the salt tolerance of Arabidopsis thaliana. Plant Sci 217–218:63–70. doi: 10.1016/j.plantsci.2013.12.00 CrossRefPubMedGoogle Scholar
  43. Shi H, Qian Y, Tan DX, Reiter RJ, He C (2015) Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J Pineal Res 59:334–342. doi: 10.1111/jpi.1226 CrossRefPubMedGoogle Scholar
  44. Shinozaki S, Tomita-Yokotani K (2003) Growth of endophyte (Neotyphodium) during seed germination of tall fescue (Festuca arundinacea). Biol Sci Space 17:214 doi: 10.2187/bss.17.57 PubMedGoogle Scholar
  45. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. Plos Genet 9:e1003577. doi: 10.1371/journal.pgen.1003577 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365. doi: 10.1105/tpc.9.3.355 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149:509–521PubMedPubMedCentralGoogle Scholar
  48. Sun X, Kang X, Ni M (2012) Hypersensitive to red and blue 1 and its modification by protein phosphatase 7 are implicated in the control of Arabidopsis stomatal aperture. PLos Genet 8:e1002674. doi: 10.1371/journal.pgen.1002674 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198. doi: 10.1146/annurev.arplant.58.032806.103830 CrossRefPubMedGoogle Scholar
  50. Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212. doi: 10.1093/jxb/erj026 CrossRefPubMedGoogle Scholar
  51. Wang Y, Chang H, Hu S, Lu X, Yuan C, Zhang C, Wang P, Xiao W, Xiao L, Xue GP, Guo X (2014) Plastid casein kinase 2 knockout reduces abscisic acid (ABA) sensitivity, thermotolerance, and expression of ABA- and heat-stress-responsive nuclear genes. J Exp Bot 65:4159–4175. doi: 10.1093/jxb/eru190 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36. doi: 10.1104/pp.103.025395 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Xu ZY, Kim SY, Hyeon do Y, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC, Hwang D, Hwang I (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25:4708–4724. doi: 10.1105/tpc.113.119099 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xu M, Lu Y, Yang H, He J, Hu Z, Hu X, Luan M, Zhang L, Fan Y, Wang L (2015) ZmGRF, a GA regulatory factor from maize, promotes flowering and plant growth in Arabidopsis. Plant Mol Biol 87:157–167. doi: 10.1007/s11103-014-0267-9 CrossRefPubMedGoogle Scholar
  55. Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 38:35–49. doi: 10.1111/pce.12351 CrossRefPubMedGoogle Scholar
  56. Yunta C, Martínez-Ripoll M, Zhu JK, Albert A (2011) The structure of Arabidopsis thaliana OST1 provides insights into the kinase regulation mechanism in response to osmotic stress. J Mol Biol 414:135–144. doi: 10.1016/j.jmb.2011.09.041 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zhang Y, Liu Z, Wang L, Zheng S, Xie J, Bi Y (2010) Sucrose-induced hypocotyl elongation of Arabidopsis seedlings in darkness depends on the presence of gibberellins. J Plant Physiol 167:1130–61136. doi: 10.1016/j.jplph.2010.03.007 CrossRefPubMedGoogle Scholar
  58. Zhu Q, Dugardeyn J, Zhang C, Mühlenbock P, Eastmond PJ, Valcke R, De Coninck B, Oden S, Karampelias M, Cammue BP, Prinsen E, Van Der Straeten D (2014) The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. Mol Plant 7:290–310. doi: 10.1093/mp/sst102 CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Congying Yuan
    • 1
  • Jianping Ai
    • 2
  • Hongping Chang
    • 1
  • Wenjun Xiao
    • 1
  • Lu Liu
    • 3
  • Cheng Zhang
    • 1
  • Zhuang He
    • 1
  • Ji Huang
    • 1
  • Jinyan Li
    • 1
  • Xinhong Guo
    • 1
  1. 1.College of Biology, State Key Laboratory of Chemo/Biosensing and ChemometricsHunan UniversityChangshaPeople’s Republic of China
  2. 2.College of Life SciencesHunan Normal UniversityChangshaChina
  3. 3.Department of Plant PathologyWashington State UniversityPullmanUSA

Personalised recommendations