Skip to main content
SpringerLink
Log in

The amino acid region from 448-517 of CAMTA3 transcription factor containing a part of the TIG domain represses the N-terminal repression module function

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

CAMTA3, a Ca2+-regulated transcription factor, is a repressor of plant immune responses. A truncated version of CAMTA3; CAMTA3334 called N-terminal repression module (NRM), and its extended version (CAMTA447), which include the DNA binding domain, were previously reported to complement the camta3/2 mutant phenotype. Here, we generated a series of CAMTA3 truncated versions [the N-terminus (aa 1-517), C-terminus (aa 517-1032), R1 (aa 1-173), R2 (aa 174-345), R3 (aa 346–517), R4 (aa 517-689), R5 (aa 690-861) and R6 (aa 862-1032)], expressed in camta3 mutant and analyzed the phenotypes of the transgenic lines. Interestingly, unlike CAMTA447, extending the N-terminal region to 517 aa did not complement the camta3 phenotype, suggesting that the amino acid region from 448-517 (70 aa), which includes a part of the TIG domain suppresses the NRM activity. The C-terminus and other truncated versions (R1–R6) also failed to complement the camta3 mutant. Expressing the full length or NRM of CAMTA3 in camta3 plants suppressed the activation of immune-responsive genes and increased the expression of cold-induced genes. In contrast, the transgenic lines expressing the N- or C-terminus or R1–R6 of CAMTA3 showed expression patterns like those of the camta3 with enhanced expression of the defense genes and suppressed expression of the cold response genes. Furthermore, like camta3, the transgenic lines expressing the N- or C-terminus, or R1–R6 of CAMTA3 exhibited higher levels of H2O2 and increased resistance to a Pst DC3000 as compared to WT, NRM, or FL-CAMTA3 transgenic plants. Our studies identified a novel regulatory region in CAMTA3 that suppresses the NRM activity.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abdel-Hameed AA, Prasad KV, Jiang Q, Reddy AS (2020) Salt-induced stability of SR1/CAMTA3 mRNA is mediated by reactive oxygen species and requires the 3’end of its open reading frame. Plant Cell Physiol 61:748–760

    Article  CAS  PubMed  Google Scholar 

  • Aravind L, Koonin EV (1999) Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J Mol Biol 287:1023–1040

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Chao L, Kim Y, Gilmour SJ, Thomashow MF (2022) Temperature modulation of CAMTA3 gene induction activity is mediated through the DNA binding domain. Plant J 112:235–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X (2009) Ethylene Insensitive3 and Ethylene Insensitive3-Like1 repress salicylic acid induction Deficient2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527–2540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung J-S, Koo SC, Jin BJ, Baek D, Yeom S-I, Chun HJ, Choi MS, Cho HM, Lee SH, Jung W-H (2020) Rice CaM-binding transcription factor (OsCBT) mediates defense signaling via transcriptional reprogramming. Plant Biotechnol Rep 14:e15358

    Article  Google Scholar 

  • Cui H, Gobbato E, Kracher B, Qiu J, Bautor J, Parker JE (2017) A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytol 213:1802–1817

    Article  CAS  PubMed  Google Scholar 

  • Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in arabidopsis leaves. Bio Protoc 2:e263

    Article  PubMed  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  CAS  PubMed  PubMed Central  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Fromm H, Finkler A (2015) Repression and de-repression of gene expression in the plant immune response: the complexity of modulation by Ca2+ and calmodulin. Mol Plant 8:671–673

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Hoehenwarter W, Scheel D, Lee J (2020) Phosphorylation of the CAMTA3 transcription factor triggers its destabilization and nuclear export. Plant Physiol 184:1056–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jing B, Xu S, Xu M, Li Y, Li S, Ding J, Zhang Y (2011) Brush and spray: a high-throughput systemic acquired resistance assay suitable for large-scale genetic screening. Plant Physiol 157:973–980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidokoro S, Yoneda K, Takasaki H, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K (2017) Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. Plant Cell 29:760–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, An C, Park S, Gilmour SJ, Wang L, Renna L, Brandizzi F, Grumet R, Thomashow M (2017) CAMTA-mediated regulation of salicylic acid immunity pathway genes in Arabidopsis exposed to low temperature and pathogen infection. The Plant Cell TPC 00865:02016

    Google Scholar 

  • Kim Y, Gilmour SJ, Chao L, Park S, Thomashow MF (2020) Arabidopsis CAMTA transcription factors regulate pipecolic acid biosynthesis and priming of immunity genes. Mol Plant 13:157–168

    Article  CAS  PubMed  Google Scholar 

  • Koo SC, Choi MS, Chun HJ, Shin DB, Park BS, Kim YH, Park HM, Seo HS, Song JT, Kang KY, Yun DJ, Chung WS, Cho MJ, Kim MC (2009) The calmodulin-binding transcription factor OsCBT suppresses defense responses to pathogens in rice. Mol Cells 27:563–570

    Article  CAS  PubMed  Google Scholar 

  • Laluk K, Prasad KV, Savchenko T, Celesnik H, Dehesh K, Levy M, Mitchell-Olds T, Reddy AS (2012) The calmodulin-binding transcription factor SIGNAL RESPONSIVE1 is a novel regulator of glucosinolate metabolism and herbivory tolerance in Arabidopsis. Plant Cell Physiol 53:2008–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Whalley HJ, Knight MR (2015) Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmodulin-binding transcription activators (CAMTAs) to produce specific gene expression responses. New Phytol 208:174-187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389

    Article  CAS  PubMed  Google Scholar 

  • Müller CW, Rey FA, Sodeoka M, Verdine GL, Harrison SC (1995) Structure of the NF-κB p50 homodimer bound to DNA. Nature 373:311–317

    Article  PubMed  Google Scholar 

  • Nie H, Zhao C, Wu G, Wu Y, Chen Y, Tang D (2012) SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN3. Plant Physiol 158:1847–1859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nimchuk Z, Eulgem T, Holt Iii BF, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579–609

    Article  CAS  PubMed  Google Scholar 

  • Prasad KVSK, Abdel-Hameed AAE, Xing D, Reddy ASN (2016) Global gene expression analysis using RNA-seq uncovered a new role for SR1/CAMTA3 transcription factor in salt stress. Sci Rep 6:27021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad K, Abdel-Hameed AAE, Jiang Q, Reddy ASN (2023) DNA-binding activity of CAMTA3 is essential for its function: identification of critical amino acids for its transcriptional activity. Cells 12:1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu YJ, Xi J, Du LQ, Suttle JC, Poovaiah BW (2012) Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol Biol 79:89–99

    Article  CAS  PubMed  Google Scholar 

  • Rahman H, Yang J, Xu YP, Munyampundu JP, Cai XZ (2016) Phylogeny of Plant CAMTAs and Role of AtCAMTAs in Nonhost Resistance to Xanthomonas oryzae pv. oryzae. Front Plant Sci 7:177

    Article  PubMed  PubMed Central  Google Scholar 

  • Rubtsov AM, Lopina OD (2000) Ankyrins. FEBS Lett 482:1–5

    Article  CAS  PubMed  Google Scholar 

  • Truman W, Sreekanta S, Lu Y, Bethke G, Tsuda K, Katagiri F, Glazebrook J (2013) The CALMODULIN-BINDING PROTEIN60 family includes both negative and positive regulators of plant immunity. Plant Physiol 163:1741–1751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Wang Z-Y (2014) At the intersection of plant growth and immunity. Cell Host Microbe 15:400–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Gong Q, Wu Y, Huang F, Ismayil A, Zhang D, Li H, Gu H, Ludman M, Fatyol K, Qi Y, Yoshioka K, Hanley-Bowdoin L, Hong Y, Liu Y (2021) A calmodulin-binding transcription factor links calcium signaling to antiviral RNAi defense in plants. Cell Host Microbe 29(1393–1406):e1397

    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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yao J, Withers J, He SY (2013) Pseudomonas syringae infection assays in Arabidopsis. Methods Mol Biol 1011:63–81

    Article  CAS  PubMed  Google Scholar 

  • Yuan P, Jewell JB, Behera S, Tanaka K, Poovaiah B (2020) Distinct molecular pattern-induced calcium signatures lead to different downstream transcriptional regulations via AtSR1/CAMTA3. Int J Mol Sci 21:8163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan P, Tanaka K, Poovaiah B (2021) Calmodulin-binding transcription activator AtSR1/CAMTA3 fine-tunes plant immune response by transcriptional regulation of the salicylate receptor NPR1. Plant Cell Environ 44:3140–3154

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Du LQ, Shen CJ, Yang YJ, Poovaiah BW (2014) Regulation of plant immunity through ubiquitin-mediated modulation of Ca2+-calmodulin-AtSR1/CAMTA3 signaling. Plant J 78:269–281

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Agriculture and Food Research Initiative competitive grant (2019-67013-29239) of the USDA NIFA and the NSF (MCB # 5333470) to A.S.N.R; A.A.E.A. was supported by the Egyptian Cultural and Educational Bureau.

Funding

Funding was provided by the Directorate for Biological Sciences (NSF) and the NIFA (USDA).

Author information

Author notes

  1. Amira A. E. Abdel-Hameed

    Present address: Department of Botany and Microbiology, Faculty of Science, Zagazig University, Zagazig, 44519, Egypt

Authors and Affiliations

  1. Department of Biology and Program in Cell and Molecular Biology, Colorado State University, Fort Collins, CO, 80523-1878, USA

    Amira A. E. Abdel-Hameed, Kasavajhala V. S. K. Prasad & Anireddy S. N. Reddy

Authors
  1. Amira A. E. Abdel-Hameed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kasavajhala V. S. K. Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anireddy S. N. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.S.N.R. conceived the project. A.A.E.A. made gene constructs, generated lines expressing different versions of CAMTA3, and performed transcript quantification of marker genes. K.V.S.K.P. performed immunoblots, disease resistance assays, and in situ staining for H2O2. All authors were involved in data analysis and writing the manuscript.

Corresponding author

Correspondence to Anireddy S. N. Reddy.

Ethics declarations

Conflict of interest

No conflict of interest is declared by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Table 1

Primer sequences of all the primers used in the current investigation (DOCX 46 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Hameed, A.A.E., Prasad, K.V.S.K. & Reddy, A.S.N. The amino acid region from 448-517 of CAMTA3 transcription factor containing a part of the TIG domain represses the N-terminal repression module function. Physiol Mol Biol Plants 29, 1813–1824 (2023). https://doi.org/10.1007/s12298-023-01401-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-023-01401-w

Keywords

Search

Navigation