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Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought tolerance in Arabidopsis

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Abstract

Calmodulin-binding proteins (CBPs) have been known to be involved in both biotic and abiotic stress responses. Recently, two closely related CBPs, Arabidopsis SAR Deficient 1 and CBP60g, were found to belong to a new family of transcription factors that regulate salicylic acid (SA) biosynthesis triggered by microbe-associated molecular patterns. In this study, we found that overexpression of CBP60g in Arabidopsis caused elevated SA accumulation, increased expression of the defense genes, and enhanced resistance to Pseudomonas syringae. In addition to the enhanced defense response, the CBP60g overexpression lines showed hypersensitivity to abscisic acid (ABA) and enhanced tolerance to drought stress. We also found that treatment with ABA and drought stress leads to a higher expression level of the ICS1 gene, which encodes isochorismate synthase, in the CBP60g overexpression lines than in the wild-type control plants. Our results suggest that CBP60g serves as a molecular link that positively regulates ABA- and SA-mediated pathways in plants.

Key message Overexpression of CBP60g in Arabidopsis enhanced the defense response, hypersensitivity to abscisic acid and tolerance to drought stress.

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References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  PubMed  CAS  Google Scholar 

  • Ali GS, Reddy VS, Lindgren PB, Jakobek JL, Reddy ASN (2003) Differential expression of genes encoding calmodulin-binding proteins in response to bacterial pathogens and inducers of defense responses. Plant Mol Biol 51:803–815

    Article  PubMed  CAS  Google Scholar 

  • Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez JA, Nicolas G, Lopez-Climent M, Gomez-Cadenas A, Nicolas C (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344

    Article  PubMed  CAS  Google Scholar 

  • Bartels S, Anderson JC, Gonzalez Besteiro MA, Carreri A, Hirt H, Buchala A, Metraux JP, Peck SC, Ulm R (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21:2884–2897

    Article  PubMed  CAS  Google Scholar 

  • Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393

    PubMed  CAS  Google Scholar 

  • Bouche N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861

    Article  PubMed  CAS  Google Scholar 

  • Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Yang X, He K, Liu M, Li J, Gao Z, Lin Z, Zhang Y, Wang X, Qiu X, Shen Y, Zhang L, Deng X, Luo J, Deng X-W, Chen Z, Gu H, Qu L-J (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  Google Scholar 

  • Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  PubMed  CAS  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  PubMed  CAS  Google Scholar 

  • de Torres Zabala M, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J 59:375–386

    Article  PubMed  Google Scholar 

  • de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bogre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–1443

    Article  PubMed  Google Scholar 

  • DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40

    Article  CAS  Google Scholar 

  • Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984

    Article  PubMed  CAS  Google Scholar 

  • Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, Poovaiah BW (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158

    Article  PubMed  CAS  Google Scholar 

  • Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol 150:1750–1761

    Article  PubMed  CAS  Google Scholar 

  • Finkler A, Ashery-Padan R, Fromm H (2007) CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Lett 581:3893–3898

    Article  PubMed  CAS  Google Scholar 

  • Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582:943–948

    Article  PubMed  CAS  Google Scholar 

  • Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Mol Plant 3:653–669

    Article  PubMed  CAS  Google Scholar 

  • Ge X, Li GJ, Wang SB, Zhu H, Zhu T, Wang X, Xia Y (2007) AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol 145:204–215

    Article  PubMed  CAS  Google Scholar 

  • Grant JJ, Chini A, Basu D, Loake GJ (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant Microbe Interact 16:669–680

    Article  PubMed  CAS  Google Scholar 

  • Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Katagiri F, Thilmony R, He SY (2002) The Arabidopsis Thaliana–Pseudomonas Syringae interaction. The Arabidopsis Book 1:e0039. doi:10.1199/tab.0039

    PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    Article  PubMed  CAS  Google Scholar 

  • Kurkela S, Franck M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol Biol 15:137–144

    Article  PubMed  CAS  Google Scholar 

  • Lang V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20:951–962

    Article  PubMed  CAS  Google Scholar 

  • Lee K, Song EH, Kim HS, Yoo JH, Han HJ, Jung MS, Lee SM, Kim KE, Kim MC, Cho MJ, Chung WS (2008) Regulation of MAPK phosphatase 1 (AtMKP1) by calmodulin in Arabidopsis. J Biol Chem 283:23581–23588

    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 

  • Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci U S A 98:4782–4787

    Article  PubMed  CAS  Google Scholar 

  • Lu Y, Harrington HM (1994) Isolation of tobacco cDNA clones encoding calmodulin-binding proteins and characterization of a known calmodulin-binding domain. Plant Physiol Biochem 32:413–422

    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

    Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  PubMed  CAS  Google Scholar 

  • Nawrath C, Heck S, Parinthawong N, Metraux JP (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286

    Article  PubMed  CAS  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735

    Article  PubMed  CAS  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  PubMed  CAS  Google Scholar 

  • Ranty B, Aldon D, Galaud JP (2006) Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals. Plant Signal Behav 1:96–104

    Article  PubMed  Google Scholar 

  • Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160:381–404

    Article  PubMed  CAS  Google Scholar 

  • Reddy ASN, Takezawa D, Fromm H, Poovaiah BW (1993) Isolation and characterization of two cDNAs that encode for calmodulin-binding proteins from corn root tips. Plant Sci 94:109–117

    Article  CAS  Google Scholar 

  • Reddy ASN, Day IS, Narasimhulu SB, Safadi F, Reddy VS, Golovkin M, Harnly MJ (2002a) Isolation and characterization of a novel calmodulin-binding protein from potato. J Biol Chem 277:4206–4214

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Reddy ASN, Ali GS, Celesnik H, Day IS (2011a) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032

    Article  PubMed  CAS  Google Scholar 

  • Reddy ASN, Ben-Hur A, Day IS (2011b) Experimental and computational approaches for the study of calmodulin interactions. Phytochemistry 72:1007–1019

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, Zhang S (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105:5638–5643

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  PubMed  CAS  Google Scholar 

  • Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304

    Article  Google Scholar 

  • Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21:6483–6493

    Article  PubMed  CAS  Google Scholar 

  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

    PubMed  CAS  Google Scholar 

  • Verberne MC, Brouwer N, Delbianco F, Linthorst HJ, Bol JF, Verpoorte R (2002) Method for the extraction of the volatile compound salicylic acid from tobacco leaf material. Phytochem Anal 13:45–50

    Article  PubMed  CAS  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J (2009) Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5:e1000301

    Article  PubMed  Google Scholar 

  • Wang L, Tsuda K, Truman W, Sato M, Nguyen LV, Katagiri F, Glazebrook J (2011) CBP60g and SARD1 play partially redundant, critical roles in salicylic acid signaling. Plant J 67:1029–1041

    Article  PubMed  CAS  Google Scholar 

  • Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217

    Article  PubMed  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1:771–781

    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 

  • Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun DJ, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem 280:3697–3706

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Gao M, Xu F, Li Y, Zhu Z, Li X, Zhang Y (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci USA 107:18220–18225

    Article  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 

  • Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Yee-yung Charng and Dr. Hao Chen for critical reading of the manuscript, Dr. Jian-min Zhou and Dr. Yuelin Zhang for providing the P. syringae strain and the mutant sard1-1 cbp60g-1, respectively, the Arabidopsis Biological Resource Center for seed stocks, and Kathleen M. Buckley, M.S. for editing assistance. This work was supported by Chinese National Programs for High Technology Research and Development (No. 2011AA100203), National Natural Science Foundation of China (No. 30860030), the Program for New Century Excellent Talents of University (No. NCET-08-0871) from Ministry of Education (China), and the Innovative Research Group Fund (No. NDPYTD2010-3) from Inner Mongolia Agricultural University (China) to Guojing Li. The authors declare that they have no conflict of interest.

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  1. College of Life Sciences, Inner Mongolia Agricultural University, Hohhot, 010018, People’s Republic of China

    Dongli Wan, Ruili Li, Bo Zou, Xin Zhang, Jingyu Cong, Ruigang Wang & Guojing Li

  2. Department of Biology, Hong Kong Baptist University, Kowloon, Hong Kong

    Yiji Xia

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  1. Dongli Wan
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Correspondence to Guojing Li.

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Communicated by B. Li.

D. Wan, R. Li, and B. Zou contributed equally to this work.

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Wan, D., Li, R., Zou, B. et al. Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought tolerance in Arabidopsis . Plant Cell Rep 31, 1269–1281 (2012). https://doi.org/10.1007/s00299-012-1247-7

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