Skip to main content
SpringerLink
Log in

Metal-responsive elements confer cadmium response in Arabidopsis

  • Short Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Molecular, biochemical, and genetic experiments demonstrate that metal-responsive elements (MREs), initially identified in animals, confer the cadmium transcriptional response in Arabidopsis, thus providing deep functional insights of MREs in plants.

Abstract

Cadmium (Cd) is highly toxic to all organisms including plants. Cd-responsive gene transcription is a fundamental aspect of the Cd response, in which Cd stress regulatory cis-acting elements are essential. However, little is known regarding such elements in plants. Metal-responsive elements (MREs, 5′-TGCRCNC-3′, R: A or G, N: any base) are essential for transcriptional induction of Cd in animals. MREs are also contained in the promoters of some Cd-regulated plant genes, but whether MREs confer Cd responses in plants is poorly defined. Herein, we used a previously identified MRE of the tobacco feedback-insensitive anthranilate synthase α-2 chain gene as a representative MRE (named as MREa, 5′-TGCACAC-3′) to explore the roles of MREs in the transcriptional response to Cd stress in Arabidopsis thaliana. First, we showed that MREa conferred Cd stress responsiveness on a minimal promoter in both concentration- and time-dependent manners, whereas the mutated MREa did not. Second, MREa specifically bound nuclear extracts, displaying a biochemical characteristic of cis-acting elements. We screened and identified four MREa-binding transcription factors, including ethylene response factor 13 (AtERF13). At last, MREa could mediate AtERF13 to activate the β-glucuronidase (GUS) reporter expression. Overall, these molecular, biochemical, and genetic data suggest that MREa is instrumental in the Cd response in Arabidopsis, thus providing deep functional insights of MREs in plants.

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

Data availability

All data supporting the findings of this study are available within the article and its supplementary information.

Abbreviations

EMSA:

Electrophoretic mobility shift assay

GST:

Glutathione S-transferase

GUS:

β-Glucuronidase

MREs:

Metal-responsive elements

References

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  PubMed  Google Scholar 

  • Culotta VC, Hamer DH (1989) Fine mapping of a mouse metallothionein gene metal response element. Mol Cell Biol 9:1376–1380

    CAS  PubMed  PubMed Central  Google Scholar 

  • DalCorso G, Farinati S, Furini A (2010) Regulatory networks of cadmium stress in plants. Plant Signal Behav 5:663–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng WG, Zhu Y, Montero A, Wu KK (2003) Quantitative analysis of binding of transcription factor complex to biotinylated DNA probe by a streptavidin-agarose pulldown assay. Anal Biochem 323:12–18

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong CJ, Wang Y, Yu SS, Liu JY (2010) Characterization of a novel rice metallothionein gene promoter: its tissue specificity and heavy metal responsiveness. J Integr Plant Biol 52:914–924

    Article  CAS  PubMed  Google Scholar 

  • Kang M, Abdelmageed H, Lee S, Reichert A, Mysore KS, Allen RD (2013) AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. Plant J 76:481–493

    Article  CAS  PubMed  Google Scholar 

  • Kusaba M, Takahashi Y, Nagata T (1996) A multiple-stimuli-responsive as-1-related element of parA gene confers responsiveness to cadmium but not to copper. Plant Physiol 111:1161–1167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Xu Y, Liu F, Zhao M, Sun Y, Ma Q (2018) Maize similar to RCD1 gene induced by salt enhances Arabidopsis thaliana abiotic stress resistance. Biochem Biophys Res Commun 503:2625–2632

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Sun N, Liu M, Liu J, Du B, Wang X, Qi X (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol 162:512–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lü S, Gu H, Yuan X, Wang X, Wu AM, Qu L, Liu JY (2007) The GUS reporter-aided analysis of the promoter activities of a rice metallothionein gene reveals different regulatory regions responsible for tissue-specific and inducible expression in transgenic Arabidopsis. Transgenic Res 16:177–191

    Article  PubMed  Google Scholar 

  • Oñate-Sánchez L, Singh KB (2002) Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol 128:1313–1322

    Article  PubMed  PubMed Central  Google Scholar 

  • Qi X, Zhang Y, Chai T (2007) Characterization of a novel plant promoter specifically induced by heavy metal and identification of the promoter regions conferring heavy metal responsiveness. Plant Physiol 143:50–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radtke F, Heuchel R, Georgiev O, Hergersberg M, Gariglio M, Dembic Z, Schaffner W (1993) Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J 12:1355–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198

    Article  CAS  PubMed  Google Scholar 

  • Stuart GW, Searle PF, Chen HY, Brinster RL, Palmiter RD (1984) A 12-base-pair DNA motif that is repeated several times in metallothionein gene promoters confers metal regulation to a heterologous gene. Proc Natl Acad Sci USA 81:7318–7322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuart GW, Searle PF, Palmiter RD (1985) Identification of multiple metal regulatory elements in mouse metallothionein-I promoter by assaying synthetic sequences. Nature 317:828–831

    Article  CAS  PubMed  Google Scholar 

  • Sun N, Liu M, Zhang W, Yang W, Bei X, Ma H, Qiao F, Qi X (2015) Bean metal-responsive element-binding transcription factor confers cadmium resistance in tobacco. Plant Physiol 167:1136–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomoto M, Tada Y, Yamamoto YY, Koyama H (2015) SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and other transcription factors are involved in ALUMINUM-ACTIVATED MALATE TRANSPORTER1 expression. Plant Physiol 167:991–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Lin T, Wang M, Qi X (2020) An AC-rich bean element serves as an ethylene-responsive element in Arabidopsis. Plants 9:1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Qiao F, Wang M, Wang Y, Xu Y, Qi X (2023) PvERF104 confers cadmium tolerance in Arabidopsis: evidence for metal-responsive element-binding transcription factors. Environ Exp Bot 206:105167

    Article  CAS  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Yu Q, Jobe TO, Pham A, Ge C, Guo Q, Liu J, Liu H, Zhang H, Zhao Y, Xue S, Hauser F, Schroeder JI (2021) An amiRNA screen uncovers redundant CBF and ERF34/35 transcription factors that differentially regulate arsenite and cadmium responses. Plant Cell Environ 44:1692–1706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Wang P, Bai Z, Herde M, Ma Y, Li N, Liu S, Huang CF, Cui R, Ma H, Zhang M, Wang H, Wei T, Quan T, Zhang W, Liu C, Zhang T, Yang ZB (2022) Calmodulin-like protein CML24 interacts with CAMTA2 and WRKY46 to regulate ALMT1-dependent Al resistance in Arabidopsis thaliana. New Phytol 233:2471–2487

    Article  CAS  PubMed  Google Scholar 

  • Zou T, Lin R, Pu L, Mei Q, Wang Z, Jian S, Zhang M (2021) Genome-wide identification, structure characterization, expression pattern profiling, and substrate specificity of the metal tolerance protein family in Canavalia rosea (Sw.) DC. Plants 10:1340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Prof. Jing Li (Capital Normal University, China) for critical reading and valuable suggestions. This work was supported by the National Natural Science Foundation of China (grant nos. 31771361 and 32070546 to X.Q.).

Author information

Author notes

  1. Chunying Wang and Ziqiang Gao have contributed equally to the article.

Authors and Affiliations

  1. College of Life Sciences, Capital Normal University, Beijing, 100048, China

    Chunying Wang, Ziqiang Gao, Yang Shi & Xiaoting Qi

Authors
  1. Chunying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ziqiang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoting Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaoting Qi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest with the contents of this article.

Additional information

Communicated by Dorothea Bartels.

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 file1 (PDF 463 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Gao, Z., Shi, Y. et al. Metal-responsive elements confer cadmium response in Arabidopsis. Planta 257, 53 (2023). https://doi.org/10.1007/s00425-023-04093-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04093-4

Keywords

Search

Navigation