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Stress responses mediated by the CBL calcium sensors in plants

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Abstract

Calcium ions (Ca2+) are involved as second messenger in plant responses to a broad array of environmental stimuli, including biotic and abiotic stresses. Therefore, understanding Ca2+-signaling mechanisms may lead to the development of transgenic crops with enhanced tolerance to adverse environmental conditions. In order to initiate the signaling cascades and give rise to relevant cellular and physiological responses, changes in the parameters of Ca2+ transients should be first detected by appropriate Ca2+ sensors in plant cells. In this regard, elucidations of plant Ca2+ sensors and their target molecules are critical steps for unraveling the Ca2+ signal transduction pathways. Recent studies have revealed that plants possess many Ca2+-binding proteins with different properties, which can serve as distinct Ca2+ sensors. This present review mainly focuses on a family of calcineurin B-like Ca2+ sensors which has been most recently identified from higher plants including Arabidopsis, rice, maize and pea.

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References

  • Akaboshi M, Hashimoto H, Ishida H, Saijo S, Koizumi N, Sato M, Shimizu T (2008) The crystal structure of plant-specific calcium-binding protein AtCBL2 in complex with the regulatory domain of AtCIPK14. J Mol Biol 377:246–257

    Article  PubMed  CAS  Google Scholar 

  • 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 20:1051–1063

    Article  PubMed  CAS  Google Scholar 

  • Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470

    Article  PubMed  CAS  Google Scholar 

  • Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342

    Article  PubMed  CAS  Google Scholar 

  • Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46:356–366

    Article  PubMed  CAS  Google Scholar 

  • Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924

    Article  PubMed  CAS  Google Scholar 

  • Batistic O, Kudla J (2009) Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophys Acta 1793:985–992

    Article  PubMed  CAS  Google Scholar 

  • 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 20:1346–1362

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR (2000) Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221–241

    Article  PubMed  CAS  Google Scholar 

  • Chandran V, Stollar EJ, Lindorff-Larsen K, Harper JF, Chazin WJ, Dobson CM, Luisi BF, Christodoulou J (2006) Structure of the regulatory apparatus of a calcium-dependent protein kinase (CDPK): a novel mode of calmodulin-target recognition. J Mol Biol 357:400–410

    Article  PubMed  CAS  Google Scholar 

  • Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239

    Article  PubMed  CAS  Google Scholar 

  • D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke 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 48:857–872

    Article  PubMed  Google Scholar 

  • Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386:855–858

    Article  PubMed  CAS  Google Scholar 

  • Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933–936

    Article  PubMed  CAS  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681

    Article  PubMed  CAS  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420

    Article  PubMed  CAS  Google Scholar 

  • Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H + -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Halfter U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13:1383–1400

    PubMed  CAS  Google Scholar 

  • Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK (2002) A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signaling in Arabidopsis. Dev Cell 3:233–244

    Article  PubMed  CAS  Google Scholar 

  • 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 97:3735–3740

    Article  PubMed  CAS  Google Scholar 

  • Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288

    Article  PubMed  CAS  Google Scholar 

  • Hernandez Sebastia C, Hardin SC, Clouse SD, Kieber JJ, Huber SC (2004) Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch Biochem Biophys 428:81–91

    Article  PubMed  Google Scholar 

  • Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9:1999–2010

    PubMed  CAS  Google Scholar 

  • Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    Article  PubMed  CAS  Google Scholar 

  • Huang CL, Ding S, Zhang H, Du H, An LZ (2011) CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci 181:57–64

    Article  PubMed  CAS  Google Scholar 

  • Jeong HJ, Jwa NS, Kim KN (2005) Identification and characterization of protein kinase that interact with the CBL3 calcium sensor in Arabidopsis. Plant Sci 169:1125–1135

    Article  CAS  Google Scholar 

  • Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11:277–295

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Cheong YH, Gupta R, Luan S (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol 124:1844–1853

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423

    Article  PubMed  CAS  Google Scholar 

  • Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schultke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484

    Article  PubMed  CAS  Google Scholar 

  • 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 134:43–58

    Article  PubMed  CAS  Google Scholar 

  • Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci USA 96:4718–4723

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Yoo BC, Harmon AC (1998) Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean. Biochemistry 37:6801–6809

    Article  PubMed  CAS  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    Article  PubMed  CAS  Google Scholar 

  • Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

    Article  PubMed  CAS  Google Scholar 

  • 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. Proc Natl Acad Sci USA 97:3730–3734

    Article  PubMed  CAS  Google Scholar 

  • 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(Suppl):S389–S400

    PubMed  CAS  Google Scholar 

  • Mahajan S, Sopory SK, Tuteja N (2006) Cloning and characterization of CBL–CIPK signalling components from a legume (Pisum sativum). FEBS J 273:907–925

    Article  PubMed  CAS  Google Scholar 

  • McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585–598

    Article  CAS  Google Scholar 

  • Oh SI, Park J, Yoon S, Kim Y, Park S, Ryu M, Nam MJ, Ok SH, Kim JK, Shin JS, Kim KN (2008) The Arabidopsis calcium sensor calcineurin B-like 3 inhibits the 5′-methylthioadenosine nucleosidase in a calcium-dependent manner. Plant Physiol 148:1883–1896

    Article  PubMed  CAS  Google Scholar 

  • Ok SH, Jeong HJ, Bae JM, Shin JS, Luan S, Kim KN (2005) Novel CIPK1-associated proteins in Arabidopsis contain an evolutionarily conserved C-terminal region that mediates nuclear localization. Plant Physiol 139:138–150

    Article  PubMed  CAS  Google Scholar 

  • 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 abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924

    Article  PubMed  CAS  Google Scholar 

  • Pandey GK, Grant JJ, Cheong YH, Kim BG, le Li G, Luan S (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant 1:238–248

    Article  PubMed  CAS  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441

    Article  PubMed  CAS  Google Scholar 

  • Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431

    Article  PubMed  CAS  Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066

    Article  PubMed  CAS  Google Scholar 

  • Reddy VS, Ali GS, Reddy AS (2002) Genes encoding calmodulin-binding proteins in the Arabidopsis genome. J Biol Chem 277:9840–9852

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez Milla MA, Uno Y, Chang IF, Townsend J, Maher EA, Quilici D, Cushman JC (2006) A novel yeast two-hybrid approach to identify CDPK substrates: characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein. FEBS Lett 580:904–911

    Article  PubMed  CAS  Google Scholar 

  • Rudd JJ, Franklin-Tong VE (2001) Unravelling response-specificity in Ca2+ signalling pathways in plant cells. New Phytol 151:7–33

    Article  CAS  Google Scholar 

  • Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706

    PubMed  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417

    PubMed  CAS  Google Scholar 

  • 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 11:2393–2405

    PubMed  CAS  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • 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 3:217–223

    PubMed  CAS  Google Scholar 

  • Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducers in plants. New Phytol 151:35–66

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Tripathi V, Syed N, Laxmi A, Chattopadhyay D (2009) Role of CIPK6 in root growth and auxin transport. Plant Signal Behav 4:663–665

    Article  PubMed  CAS  Google Scholar 

  • Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56:505–516

    Article  PubMed  CAS  Google Scholar 

  • Wang MY, Gu D, Liu TS, Wang ZQ, Guo XY, Hou W, Bai YF, Chen XP, Wang GY (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65:733–746

    Article  PubMed  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot (Lond) 92:487–511

    Article  CAS  Google Scholar 

  • Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439

    Article  PubMed  CAS  Google Scholar 

  • 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 125:1347–1360

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191

    PubMed  CAS  Google Scholar 

  • Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the ministry of Education, Science and Technology (2010-0008839). This work was also supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (No. 2011-0029568).

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  1. Department of Molecular Biology, PERI, Sejong University, Seoul, 143-747, Korea

    Kyung-Nam Kim

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Kim, KN. Stress responses mediated by the CBL calcium sensors in plants. Plant Biotechnol Rep 7, 1–8 (2013). https://doi.org/10.1007/s11816-012-0228-1

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