Skip to main content
SpringerLink
Log in

A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

ZmDi19-1 can be induced by various abiotic stresses and enhance the salt tolerance of transgenic Arabidopsis thaliana.

Abstract

Drought-induced protein 19 (Di19) is an essential zinc finger family member that plays vital roles in regulating multiple stress responses. Here, the Di19 family gene in maize (Zea mays) ZmDi19-1 was characterized. We determined that ZmDi19-1 is constitutively expressed in root, stem, leaf and other maize tissues under normal conditions. In addition, ZmDi19-1 expression was induced by PEG and NaCl stresses. The subcellular localization revealed that ZmDi19-1 is a nuclear membrane protein. In yeast cells, ZmDi19-1 displayed transcriptional activity and could bind to the TACA(A/G)T sequence, which was corroborated using the dual luciferase reporter assay system. The overexpression of ZmDi19-1 in Arabidopsis thaliana enhanced the plants’ tolerance to salt stress. Compared with wild-type, the Arabidopsis ZmDi19-1-overexpressing lines had higher relative water and proline contents, and lower malondialdehyde contents, in leaves under salt-stress conditions. The transcriptome analysis revealed 1414 upregulated and 776 downregulated genes, and an RNA-seq analysis identified some differentially expressed genes, which may be downstream of ZmDi19-1, involved in salt-stress responses. The data demonstrated that ZmDi19-1 responds to salt stress and may impact the expression of stress-related genes in Arabidopsis.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 10

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

GFP:

Green fluorescent protein

MDA:

Malondialdehyde

REL:

Relative electrical leakage

ORF:

Open reading frame

qRT-PCR:

Quantitative real-time polymerase chain reaction

References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Adie BAT, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA et al (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510

    Article  CAS  PubMed  Google Scholar 

  • Belin C, Megies C, Hauserova E, Lopez-Molina L (2009) Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21:2253–2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bgre L, Meskiene I, Heberlebors E et al (2000) Stressing the role of MAP kinases in mitogenic stimulation. Plant Mol Biol 43(5):705–718

    Article  Google Scholar 

  • Cai R, Dai W, Zhang C, Wang Y, Wu M, Zhao Y et al (2017) The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 246:1215–1231

    Article  CAS  PubMed  Google Scholar 

  • Chak RK, Thomas TL, Quatrano RS, Rock CD (2000) The genes ABI1 and ABI2 are involved in abscisic acid- and drought-inducible expression of the Daucus carota L. Dc3 promoter in guard cells of transgenic Arabidopsis thaliana (L.) Heynh. Planta 210:875–883

    Article  CAS  PubMed  Google Scholar 

  • Choi HI, Hong JH, Ha JO, Kang JY, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Ciftciyilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160

    Article  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • Demiral T, Turkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  • Dure L (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363–369

    Article  CAS  PubMed  Google Scholar 

  • Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genom 5:39

    Article  CAS  Google Scholar 

  • Gosti F, Bertauche N, Vartaninan N, Giraudat J (1995) Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet 246:10–18

    Article  CAS  PubMed  Google Scholar 

  • Kang X, Chong J, Ni M (2005) Hypersensitive to Red and Blue 1, a ZZ-type zinc finger protein, regulates phytochrome B-mediated red and cryptochrome-mediated blue light responses. Plant Cell 17:822–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kariola T, Brader G, Helenius E, Li J, Heino P, Palva ET (2006) Early responsive to dehydration 15, a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiol 142:1559–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klug A, Schwabe JW (1995) Protein motifs 5. Zinc fingers. Faseb J 9:597–604

    Article  CAS  PubMed  Google Scholar 

  • Koca H, Bor M, Ozdemir F, Turkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351

    Article  CAS  Google Scholar 

  • Latchman DS (1993) Transcription factors: an overview. Int J Exp Pathol 74:417–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li G, Tai FJ, Zheng Y, Luo J, Gong SY, Zhang ZT et al (2010a) Two cotton Cys2/His2-type zinc-finger proteins, GhDi19-1 and GhDi19-2, are involved in plant response to salt/drought stress and abscisic acid signaling. Plant Mol Biol 74:437–452

    Article  CAS  PubMed  Google Scholar 

  • Li S, Xu C, Yang Y, Xia G (2010b) Functional analysis of TaDi19A, a salt-responsive gene in wheat. Plant Cell Environ 33(1):117–129

    PubMed  Google Scholar 

  • Liu WX, Zhang FC, Zhang WZ, Song LF, Wu WH, Chen YF (2013) Arabidopsis Di19 functions as a transcription factor and modulates PR1, PR2, and PR5 expression in response to drought stress. Mol Plant 6:1487–1502

    Article  CAS  PubMed  Google Scholar 

  • Ma F, Wang L, Li J, Samma M, Xie Y, Wang R et al (2014) Interaction between HY1 and HO in auxin-induced lateral root formation in Arabidopsis. Plant Mol Biol 85:49–61

    Article  CAS  PubMed  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, Ga2ox7, under high-salinity stress in Arabidopsis. The Plant J 56:613–626

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158

    Article  CAS  PubMed  Google Scholar 

  • Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36:1405–1420

    CAS  PubMed  Google Scholar 

  • Milla MAR, Townsend J, Chang IF, Cushman JC (2006) The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant Mol Biol 61:13–30

    Article  CAS  PubMed  Google Scholar 

  • Miller J, Mclachlan AD, Klug A (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4:1609–1614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plants Sci 7:405–410

    Article  CAS  Google Scholar 

  • Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkinson H, Kapushesky M, Kolesnikov N, Rustici G, Shojatalab M, Abeygunawardena N, Holloway E et al (2009) Array express update-from an archive of functional genomics experiments to the atlas of gene expression. Nucleic Acids Res 37:D868–D872

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponting CP, Blake DJ, Davies KE, Kendrick-Jones J, Winder SJ (1996) ZZ and TAZ: new putative zinc fingers in dystrophin and other proteins. Trends Biochem Sci 21:11–13

    Article  CAS  PubMed  Google Scholar 

  • Qin LX, Li Y, Li DD, Xu WL, Zheng Y, Li XB (2014) Arabidopsis drought-induced protein Di19-3 participates in plant response to drought and high salinity stresses. Plant Mol Biol 86:609–625

    Article  CAS  PubMed  Google Scholar 

  • Qin LX, Nie XY, Hu R, Li G, Xu WL, Li XB (2016) Phosphorylation of serine residue modulates cotton Di19-1 and Di19-2 activities for responding to high salinity stress and abscisic acid signaling. Sci Rep 6:20371

    Article  CAS  PubMed  PubMed Central  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 99:8436–8441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K et al (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596

    Article  CAS  PubMed  Google Scholar 

  • Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078

    Article  CAS  PubMed  Google Scholar 

  • Thalhammer A, Bryant G, Sulpice R, Hincha DK (2014) Disordered cold regulated 15 proteins protect chloroplast membranes during freezing through binding and folding, but do not stabilize chloroplast enzymes in Vivo. Plant Phyol 166:190–194

    Article  CAS  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin in Biotechnol 17:113–122

    Article  CAS  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195

    Article  CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin in Biotechnol 16:123–132

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Yu C, Chen C, He C, Zhu Y, Huang W (2014) Identification of rice Di19 family reveals OSDi19-4 involved in drought resistance. Plant Cell Rep 33:2047–2062

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Yu C, Xu S, Zhu Y, Huang W (2016a) Osdi19-4 acts downstream of OSCDPK14 to positively regulate aba response in rice. Plant Cell Environ 39:2740–2753

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Su G, Li M, Ke Q, Kim SY, Li H et al (2016b) Overexpressing Arabidopsis ABF3 increases tolerance to multiple abiotic stresses and reduces leaf size in alfalfa. Plant Physiol Biochem 109:199–208

    Article  CAS  PubMed  Google Scholar 

  • Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297:249–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  CAS  Google Scholar 

  • Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC et al (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Wang Y, Zheng H, Lu W, Zheng C (2015) Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. J Exp Bot 66:5997–6008

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    Article  CAS  PubMed  Google Scholar 

  • Young J (2006) Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9:654–663

    Article  PubMed  Google Scholar 

  • Zarrinpar A, Bhattacharyya RP, Lim WA (2003) The structure and function of proline recognition domains. Sci STKE 179:RE8

  • Zhao Y, Ma Q, Jin X, Peng X, Liu J, Deng L et al (2014) A novel maize Homeodomain-Leucine Zipper (hd-zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis. Plant Cell Physiol 55:1142–1156

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31871627, 31701436) and the Science and Technology Major Project of Anhui Province (18030701180).

Author information

Author notes

  1. Xingen Zhang and Huilin Cai contributed equally to this work.

Authors and Affiliations

  1. National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life Sciences, Anhui Agricultural University, Hefei, 230036, China

    Xingen Zhang, Huilin Cai, Meng Lu, Qiye Wei, Lijuan Xu, Chen Bo, Qing Ma, Yang Zhao & Beijiu Cheng

Authors
  1. Xingen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huilin Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiye Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lijuan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chen Bo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qing Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Beijiu Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yang Zhao or Beijiu Cheng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Leandro Peña.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2019_2467_MOESM1_ESM.tif

Fig S1 Validation of transgenic Arabidopsis overexpressing ZmDi19-1. a PCR analysis of transgenic Arabidopsis thaliana using ZmDi19-1 gene primers. b GUS staining of ZmDi19-1 transgenic Arabidopsis thaliana (TIFF 7511 kb)

Fig S2 Numbers of differentially expressed genes (TIFF 4836 kb)

299_2019_2467_MOESM3_ESM.tif

Fig S3 Expression levels of ABA-related genes in ZmDi19-1 transgenic Arabidopsis and WT after salt-stress treatments (TIFF 15050 kb)

Table S1 Twenty-eight differentially expressed genes (DOCX 17 kb)

Table S2 Primers used in this study (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Cai, H., Lu, M. et al. A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis. Plant Cell Rep 38, 1563–1578 (2019). https://doi.org/10.1007/s00299-019-02467-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-019-02467-1

Keywords

Search

Navigation