Skip to main content
SpringerLink
Log in

Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Auxin is a key plant hormone that regulates various aspects of plant development. However, the mechanisms integrating auxin growth effects with stress responses are not fully understood. In this study, we investigated the possible role of calmodulin-binding transcription activator 1 (CAMTA1), an Arabidopsis thaliana calcium/calmodulin-binding transcription activator, in auxin signaling and its responses to different stresses. Plants harboring the AtCAMTA1 promoter fused to the GUS reporter gene revealed cell-specific expression patterns reminiscent of auxin responses. The responsiveness of CAMTA1 to auxin was further assessed by chemical disturbances in polar auxin transport, and by RT-PCR analysis of gene expression of dissected leaf sections from plants exposed to the auxin transport inhibitor NPA. Furthermore, the intensity and cell-specific expression patterns of CAMTA1 changed significantly and differentially on exposure to increasing salt concentrations and heat. Transcriptome analysis of a camta1 T-DNA insertion mutant revealed 63 up-regulated genes, of which 17 are associated with auxin signaling. Finally, analysis of hypocotyl elongation in the presence and absence of auxin revealed that camta1 T-DNA insertion mutants and CAMTA1-repressor lines are hyper-responsive to auxin compared to wild-type seedlings. Thus, CAMTA1 participates in auxin signaling and responds to abiotic stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Ca2+ :

Calcium

CaM:

Calmodulin

CAMTA:

Calmodulin-binding transcription activator

NPA:

Naphthylphthalamic acid

TF:

Transcription factor

References

  • Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–853

    PubMed  CAS  Google Scholar 

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328

    Article  PubMed  CAS  Google Scholar 

  • Benjamins R, Ampudia CS, Hooykaas PJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630

    Article  PubMed  CAS  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Bouché 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  Google Scholar 

  • Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  PubMed  CAS  Google Scholar 

  • Chung KM, Sano H (2007) Transactivation of wound-responsive genes containing the core sequence of the auxin-responsive element by a wound-induced protein kinase-activated transcription factor in tobacco plants. Plant Mol Biol 65:763–773

    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 

  • Dan H, Yang G, Zheng ZL (2007) A negative regulatory role for auxin in sulphate deficiency response in Arabidopsis thaliana. Plant Mol Biol 63:221–235

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Mészáros T, Miskolczi P, Oberschall A, Török K, Magyar Z, Dudits D, Deák M (2001) Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J Exp Bot 52:215–221

    Article  PubMed  CAS  Google Scholar 

  • Devlin PF, Yanovsky MJ, Kay SA (2003) A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133:1617–1629

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  PubMed  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 

  • Douglas CB, Adel MZ, Robert A, Amy JM, Neil EH, Keith RD, Jörn G (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fuchs I, Philippar K, Hedrich R (2006) Ion channels meet auxin action. Plant Biol 8:353–359

    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 

  • Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, Ogawa M, Yamauchi Y, Preston J, Aoki K, Kiba T, Takatsuto S, Fujioka S, Asami T, Nakano T, Kato H, Mizuno T, Sakakibara H, Yamaguchi S, Nambara E, Kamiya Y, Takahashi H, Hirai MY, Sakurai T, Shinozaki K, Saito K, Yoshida S, Shimada Y (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55:526–542

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  PubMed  CAS  Google Scholar 

  • Han J, Gong P, Reddig K, Mitra M, Guo P, Li HS (2006) The fly CAMTA transcription factor potentiates deactivation of rhodopsin, a G protein-coupled light receptor. Cell 127:847–858

    Article  PubMed  CAS  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49:1429–1450

    Article  PubMed  CAS  Google Scholar 

  • Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739

    Article  PubMed  CAS  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  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 

  • Jensen PJ, Hangarter RP, Estelle M (1998) Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol 116:455–462

    Article  PubMed  CAS  Google Scholar 

  • Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363

    Article  PubMed  CAS  Google Scholar 

  • Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, North KA, Kopriva S (2008) Complex signaling network in regulation of adenosine 5′-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol 146:1408–1420

    Article  PubMed  CAS  Google Scholar 

  • Kurepin LV, Emery RJ, Pharis RP, Reid DM (2007) Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: putative roles for plant hormones in leaf and internode growth. J Exp Bot 58:2145–2157

    Article  PubMed  CAS  Google Scholar 

  • Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792

    Article  PubMed  CAS  Google Scholar 

  • Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:60–61

    Article  Google Scholar 

  • Li L, Hou X, Tsuge T, Ding M, Aoyama T, Oka A, Gu H, Zhao Y, Qu LJ (2008) The possible action mechanisms of indole-3-acetic acid methyl ester in Arabidopsis. Plant Cell Rep 27:575–584

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 20:900–911

    Article  PubMed  CAS  Google Scholar 

  • López-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bögre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968

    Article  PubMed  Google Scholar 

  • Mitsuda N, Isono T, Sato MH (2003) Arabidopsis CAMTA family proteins enhance V-PPase expression in pollen. Plant Cell Physiol 44:975–981

    Article  PubMed  CAS  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    Article  PubMed  CAS  Google Scholar 

  • Nag R, Maity MK, Dasgupta M (2005) Dual DNA binding property of ABA insensitive 3 like factors targeted to promoters responsive to ABA and auxin. Plant Mol Biol 59:821–838

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Aviñó JP, Bennett AB (2005) Role of a Ca2+-ATPase induced by ABA and IAA in the generation of specific Ca2+ signals. Biochem Biophys Res Commun 329:406–415

    Article  PubMed  Google Scholar 

  • Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Scrase-Field SA, Knight MR (2003) Calcium: just a chemical switch? Curr Opin Plant Biol 6:500–506

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453

    Article  PubMed  CAS  Google Scholar 

  • Shishova M, Lindberg S (2004) Auxin induces an increase of Ca2+ concentration in the cytosol of wheat leaf protoplasts. J Plant Physiol 161:937–945

    Article  PubMed  CAS  Google Scholar 

  • Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123

    Article  PubMed  CAS  Google Scholar 

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121:1179–1190

    Article  PubMed  CAS  Google Scholar 

  • Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57:4059–4070

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Kaplan B, Bouché N, Arazi T, Dolev D, Talke IN, Maathuis FJM, Sanders D, Bouchez D, Fromm H (2000) Expression of a truncated tobacco NtCBP4 channel in transgenic plants, and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance. Plant J 24:533–542

    Article  PubMed  CAS  Google Scholar 

  • Timpte C, Wilson AK, Estelle M (1994) The axr2-1 mutation of Arabidopsis thaliana is a gain-of-function mutation that disrupts an early step in auxin response. Genetics 138:1239–1249

    PubMed  CAS  Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Mopper S, Hasenstein KH (2001) Effects of salinity on endogenous ABA, IAA, JA, AND SA in Iris hexagona. J Chem Ecol 27:327–342

    Article  PubMed  CAS  Google Scholar 

  • Xu N, Hagen G, Guilfoyle T (1997) Multiple auxin response modules in the soybean SAUR 15A promoter. Plant Sci 126:193–201

    Article  CAS  Google Scholar 

  • Yang T, Poovaiah BW (2000) Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J Biol Chem 275:3137–3143

    Article  PubMed  CAS  Google Scholar 

  • Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signalling pathways in plants. J Biol Chem 277:45049–45058

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Masa H. Sato (Kyoto University, Japan) for his kind gift of the DNA construct of CAMTA1::GUS and Dr. Aliza Finkler (Tel Aviv University, Israel) for critically reading the manuscript. We also thank Prof. Robert Fluhr and Ms. Dina Volodarsky (Weizmann Institute of Science, Israel) for assistance with the “Plant Hormone” Web tool. The research was supported by a grant from the Israel Science Foundation (ISF) to H. F., by a grant from the Biotechnology and Biological Sciences Research Council (BBSRC), UK to M. R. K., and by an ERA-NET Plant Genomics grant to M. R. K and H. F., funded by the Biotechnological and Biological Sciences Research Council (BBSRC), UK and the Ministry of Agriculture and Rural Development (MOARD), Israel.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, Faculty of Life Sciences, Tel Aviv University, 69978, Tel Aviv, Israel

    Yael Galon, Roni Aloni, Dikla Nachmias, Orli Snir & Hillel Fromm

  2. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK

    Sarah Scrase-Field, Joy M. Boyce & Marc R. Knight

  3. Plant Stress Signalling Lab, Institute of Plant and Microbial Sciences, School of Biological and Biomedical Sciences, Durham University, South Road, Durham, H1 3LE, UK

    Marc R. Knight

  4. Bioinformatics Unit, Department of Biological Services, Weizmann Institute of Science, PO Box 26, 76100, Rehovot, Israel

    Ester Feldmesser

  5. INRA, Institut Jean Pierre Bourgin, Station De Génétique et d’Amélioration des Plantes, UR254, 78026, Versailles, France

    Nicolas Bouché

Authors
  1. Yael Galon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roni Aloni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dikla Nachmias
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Orli Snir
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ester Feldmesser
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sarah Scrase-Field
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joy M. Boyce
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nicolas Bouché
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marc R. Knight
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hillel Fromm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hillel Fromm.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 368 kb)

Supplementary material 2 (PDF 651 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galon, Y., Aloni, R., Nachmias, D. et al. Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis. Planta 232, 165–178 (2010). https://doi.org/10.1007/s00425-010-1153-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1153-6

Keywords

Search

Navigation