Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 124, Issue 3, pp 459–469

ZmCIPK8, a CBL-interacting protein kinase, regulates maize response to drought stress

  • Fuju Tai
  • Zhiheng Yuan
  • Shipeng Li
  • Qi Wang
  • Fuyang Liu
  • Wei Wang
Original Article

Abstract

Plant CBL-interacting protein kinases (CIPKs) play an important role in stress signaling transduction and enhancing plant stress tolerance. However, the functions of most CIPKs in crop plants such as maize have not been studied. Here, a novel CIPK gene, ZmCIPK8, was cloned and characterized from maize (Zea mays). The ZmCIPK8 gene has 14 introns and its encoded protein shares high homology to Arabidopsis and rice CIPKs. Yeast two-hybrid and bimolecular fluorescence complementation assay demonstrated that ZmCIPK8 interacted with ZmCBL1, ZmCBL4 and ZmCBL9. Quantitative RT-PCR analysis revealed that the mRNA accumulation of ZmCIPK8 in maize leaves and roots was promoted by drought stress. GUS gene expression driven by the ZmCIPK8 promoter was in an organ-dependent pattern and induced in Arabidopsis seedlings under drought stress. Over-expression of ZmCIPK8 in tobacco induced the expression of the NAC, CBF, and Rd29A genes and enhanced drought tolerance of transgenic tobacco seedlings. Thus, ZmCIPK8 perhaps is involved in plant response to drought and other abiotic stress through regulating stress-related genes.

Keywords

Maize CIPK Drought stress Transgenic plants 

Supplementary material

11240_2015_906_MOESM1_ESM.ppt (225 kb)
Supplementary material 1 (PPT 225 kb)
11240_2015_906_MOESM2_ESM.ppt (3.3 mb)
Supplementary material 2 (PPT 3417 kb)

References

  1. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein–protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063PubMedCentralCrossRefPubMedGoogle Scholar
  2. Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470CrossRefPubMedGoogle Scholar
  3. Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924CrossRefPubMedGoogle Scholar
  4. Batistic O, Sorek N, Schultke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362PubMedCentralCrossRefPubMedGoogle Scholar
  5. Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signalling in Arabidopsis: how to obtain insights into a complex signalling network. J Exp Bot 62:1391–1397CrossRefPubMedGoogle Scholar
  6. Chen X, Gu Z, Xin D, Hao L, Liu C, Huang J, Ma B, Zhang H (2011) Identification and characterization of putative CIPK genes in maize. J Gen Genom 38:77–87CrossRefGoogle Scholar
  7. Chen L, Ren F, Zhou L, Wang QQ, Zhong H, Li XB (2012) The Brassica napus calcineurin B-like 1/CBL-interacting protein kinase 6 (CBL1/CIPK6) component is involved in the plant response to abiotic stress and ABA signaling. J Exp Bot 63:6211–6222PubMedCentralCrossRefPubMedGoogle Scholar
  8. Chung E, Park JM, Oh SK, Joung YH, Lee S, Choi D (2004) Molecular and biochemical characterization of the Capsicum annuum calcium-dependent protein kinase 3 (CaCDPK3) gene induced by abiotic and biotic stresses. Planta 220:286–295CrossRefPubMedGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  10. D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schültke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872CrossRefPubMedGoogle Scholar
  11. Drerup MM, Schlucking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569CrossRefPubMedGoogle Scholar
  12. Gao F, Xiong A, Peng R, Jin X, Xu J, Zhu B, Chen J, Yao Q (2010) OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. Plant Cell Tissue Organ Cult 100:255–262CrossRefGoogle Scholar
  13. Gong D, Guo Y, Schumaker KS, Zhu JK (2004) The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiol 134:919–926PubMedCentralCrossRefPubMedGoogle Scholar
  14. Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740PubMedCentralCrossRefPubMedGoogle Scholar
  15. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278CrossRefPubMedGoogle Scholar
  16. Hu L, Hu T, Zhang X, Pang H, Fu J (2012) Exogenous glycine betaine ameliorates the adverse effect of salt stress on perennial ryegrass. J Am Soc Hortic Sci 137:38–46Google Scholar
  17. Hwang Y, Bethke PC, Cheong YH, Chang HS, Zhu T, Jones RL (2005) A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol 138:1347–1358PubMedCentralCrossRefPubMedGoogle Scholar
  18. Kim KN, Cheong YH, Gupta R, Luan S (2000) Interaction specificity of Arabidopsis calcineurine B-like calcium sensor and their target kinases. Plant Physiol 124:1844–1853PubMedCentralCrossRefPubMedGoogle Scholar
  19. Kim KN, Lee JS, Han H, Choi SA, Go SJ, Yoon IS (2003a) Isolation and characterization of a novel rice Ca2+-regulated protein kinase gene involved in responses to diverse signals including cold, light, cytokinins, sugars and salts. Plant Mol Biol 52:1191–1202CrossRefPubMedGoogle Scholar
  20. Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003b) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423PubMedCentralCrossRefPubMedGoogle Scholar
  21. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267CrossRefPubMedGoogle Scholar
  22. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL–CIPK signaling networks. Plant Physiol 134:43–58PubMedCentralCrossRefPubMedGoogle Scholar
  23. Li G, Tai FJ, Zheng Y, Luo J, Gong SY, Zhang ZT, Li XB (2010) Two cotton Cys2/His2-type zinc-finger proteins, GhDi19-1 and GhDi19-2, are involved in plant response to salt/drought stress and abscisic acid signaling. Plant Mol Biol 74:437–452CrossRefPubMedGoogle Scholar
  24. Li D, Song S, Xia X, Yin W (2012) Two CBL genes from populus euphratica confer multiple stress tolerance in transgenic triploid white poplar. Plant Cell Tissue Organ Cult 109:477–489CrossRefGoogle Scholar
  25. Li J, Luan Y, Liu Z (2015) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. Plant Cell Tissue Organ Cult 123:67–81CrossRefGoogle Scholar
  26. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945CrossRefPubMedGoogle Scholar
  27. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. PNAS 97:3730–3734PubMedCentralCrossRefPubMedGoogle Scholar
  28. Liu LL, Ren HM, Chen LQ, Wang Y, Wu WH (2013) A protein kinase, calcineurin B-like protein-interacting protein kinase 9, interacts with calcium sensor calcineurin B-like protein 3 and regulates potassium homeostasis under low-potassium stress in Arabidopsis. Plant Physiol 161:266–277PubMedCentralCrossRefPubMedGoogle Scholar
  29. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B–like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400PubMedCentralPubMedGoogle Scholar
  30. Luan S, Lan W, Lee SC (2009) Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL–CIPK network. Curr Opin Plant Biol 12:339–346CrossRefPubMedGoogle Scholar
  31. Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, Boller T, Jones JD, Romeis T (2005) Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 102:10736–10741PubMedCentralCrossRefPubMedGoogle Scholar
  32. Mähs A, Steinhorst L, Han JP, Shen LK, Wang Y, Kudla J (2013) The calcineurin B-like Ca2+ Sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis. Mol Plant 6:1149–1162CrossRefPubMedGoogle Scholar
  33. Man D, Bao YX, Han LB, Zhang X (2011) Drought tolerance associated with proline and hormone metabolism in two tall fescue cultivars. Hortic Sci 46:1027–1032Google Scholar
  34. Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012PubMedCentralCrossRefPubMedGoogle Scholar
  35. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  36. Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105–1113CrossRefPubMedGoogle Scholar
  37. Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates ABA sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924PubMedCentralCrossRefPubMedGoogle Scholar
  38. Piao HL, Xuan YH, Park SH, Je BI, Park SJ, Kim CM, Huang J, Wang GK, Kim MJ, Kang SM, Lee IJ, Kwon TR, Kim YH, Yeo US, Yi G, Son D, Han CD (2010) OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. Mol Cell 30:19–27CrossRefGoogle Scholar
  39. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Nat/Ht exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441PubMedCentralCrossRefPubMedGoogle Scholar
  40. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72PubMedCentralCrossRefPubMedGoogle Scholar
  41. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B–like calcium sensors in Arabidopsis. Plant Cell 11:2393–2406PubMedCentralCrossRefPubMedGoogle Scholar
  42. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223CrossRefPubMedGoogle Scholar
  43. Tai F, Wang Q, Yuan Z, Yuan Z, Li H, Wang W (2013) Characterization of five CIPK genes expressions in maize under water stress. Acta Physiol Plant 35:1555–1564CrossRefGoogle Scholar
  44. Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX, Luan S (2015) Tonoplast CBL–CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci USA 112:3134–3139PubMedCentralCrossRefPubMedGoogle Scholar
  45. Torre F, Gutiérrez-Beltrán E, Pareja-Jaime Y, Chakravarthy S, Martin GB, Pozo O (2013) The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. Plant Cell 25:2748–2764PubMedCentralCrossRefPubMedGoogle Scholar
  46. Tsou PL, Lee SY, Allen NS, Winter-Sederoff H, Robertson D (2012) An ER-targeted calcium-binding peptide confers salt and drought tolerance mediated by CIPK6 in Arabidopsis. Planta 235:539–552CrossRefPubMedGoogle Scholar
  47. Wang M, Gu D, Liu T, Wang Z, Guo X, Hou W, Bai Y, Chen X, Wang G (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65:733–746CrossRefPubMedGoogle Scholar
  48. Wang C, Yuan Z, Li S, Wang W, Xue R, Tai F (2014) Characterization of eight CBL genes expressions in maize early seeding development. Acta Physiol Plant 36:3307–3314CrossRefGoogle Scholar
  49. Wang NN, Zhao LL, Lu R, Li Y, Li XB (2015) Cotton mitogen-activated protein kinase4 (GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses. Plant Cell Tissue Organ Cult. doi:10.1007/s11240-015-0865-5 Google Scholar
  50. Weinl S, Kudla J (2009) The CBL–CIPK Ca2+ -decoding signaling network: function and perspectives. N Phytol 184:517–528CrossRefGoogle Scholar
  51. Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid–inducible mitogen-activated protein kinase. Plant Cell 15:745–759PubMedCentralCrossRefPubMedGoogle Scholar
  52. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360CrossRefPubMedGoogle Scholar
  53. Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102CrossRefPubMedGoogle Scholar
  54. Zhao J, Sun Z, Zheng J, Guo X, Dong Z, Huai J, Gou M, He J, Jin Y, Wang J, Wang G (2009) Cloning and characterization of a novel CBL-interacting protein kinase from maize. Plant Mol Biol 69:661–674CrossRefPubMedGoogle Scholar
  55. Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1192PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Fuju Tai
    • 1
  • Zhiheng Yuan
    • 1
  • Shipeng Li
    • 1
  • Qi Wang
    • 1
  • Fuyang Liu
    • 1
  • Wei Wang
    • 1
  1. 1.Collaborative Innovation Center of Henan Grain Crops, State Key Laboratory of Wheat and Maize Crop Science, College of Life ScienceHenan Agricultural UniversityZhengzhouChina

Personalised recommendations