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

  • Xingen Zhang
  • Huilin Cai
  • Meng Lu
  • Qiye Wei
  • Lijuan Xu
  • Chen Bo
  • Qing Ma
  • Yang ZhaoEmail author
  • Beijiu ChengEmail author
Original Article

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.

Keywords

Drought-induced 19 family ZmDi19-1 Salt stress Transcriptome 

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

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

299_2019_2467_MOESM1_ESM.tif (7.3 mb)
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)
299_2019_2467_MOESM2_ESM.tif (4.7 mb)
Fig S2 Numbers of differentially expressed genes (TIFF 4836 kb)
299_2019_2467_MOESM3_ESM.tif (14.7 mb)
Fig S3 Expression levels of ABA-related genes in ZmDi19-1 transgenic Arabidopsis and WT after salt-stress treatments (TIFF 15050 kb)
299_2019_2467_MOESM4_ESM.docx (18 kb)
Table S1 Twenty-eight differentially expressed genes (DOCX 17 kb)
299_2019_2467_MOESM5_ESM.docx (18 kb)
Table S2 Primers used in this study (DOCX 17 kb)

References

  1. 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 9:1859–1868Google Scholar
  2. 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 19:1665–1681CrossRefGoogle Scholar
  3. Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510CrossRefGoogle Scholar
  4. 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 21:2253–2268CrossRefGoogle Scholar
  5. Bgre L, Meskiene I, Heberlebors E et al (2000) Stressing the role of MAP kinases in mitogenic stimulation. Plant Mol Biol 43(5):705–718CrossRefGoogle Scholar
  6. 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 246:1215–1231CrossRefGoogle Scholar
  7. 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 210:875–883CrossRefGoogle Scholar
  8. Choi HI, Hong JH, Ha JO, Kang JY, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730CrossRefGoogle Scholar
  9. Ciftciyilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160CrossRefGoogle Scholar
  10. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefGoogle Scholar
  11. 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 53:247–257CrossRefGoogle Scholar
  12. Dure L (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363–369CrossRefGoogle Scholar
  13. Englbrecht CC, Schoof H, Bohm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genom 5:39CrossRefGoogle Scholar
  14. 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 246:10–18CrossRefGoogle Scholar
  15. 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 17:822–835CrossRefGoogle Scholar
  16. 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 142:1559–1573CrossRefGoogle Scholar
  17. Klug A, Schwabe JW (1995) Protein motifs 5. Zinc fingers. Faseb J 9:597–604CrossRefGoogle Scholar
  18. 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 60:344–351CrossRefGoogle Scholar
  19. Latchman DS (1993) Transcription factors: an overview. Int J Exp Pathol 74:417–422Google Scholar
  20. 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 74:437–452CrossRefGoogle Scholar
  21. Li S, Xu C, Yang Y, Xia G (2010b) Functional analysis of TaDi19A, a salt-responsive gene in wheat. Plant Cell Environ 33(1):117–129Google Scholar
  22. 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 6:1487–1502CrossRefGoogle Scholar
  23. 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 85:49–61CrossRefGoogle Scholar
  24. 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 56:613–626CrossRefGoogle Scholar
  25. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefGoogle Scholar
  26. Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158CrossRefGoogle Scholar
  27. Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36:1405–1420Google Scholar
  28. 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 61:13–30CrossRefGoogle Scholar
  29. Miller J, Mclachlan AD, Klug A (1985) Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4:1609–1614CrossRefGoogle Scholar
  30. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plants Sci 7:405–410CrossRefGoogle Scholar
  31. 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 234:97–107CrossRefGoogle Scholar
  32. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  33. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95CrossRefGoogle Scholar
  34. 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–D872CrossRefGoogle Scholar
  35. 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 129:460–468CrossRefGoogle Scholar
  36. 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 21:11–13CrossRefGoogle Scholar
  37. 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 86:609–625CrossRefGoogle Scholar
  38. 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 6:20371CrossRefGoogle Scholar
  39. 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 99:8436–8441CrossRefGoogle Scholar
  40. 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 136:2734–2746CrossRefGoogle Scholar
  41. 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 3:217–223CrossRefGoogle Scholar
  42. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227CrossRefGoogle Scholar
  43. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417CrossRefGoogle Scholar
  44. Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596CrossRefGoogle Scholar
  45. Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078CrossRefGoogle Scholar
  46. 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 166:190–194CrossRefGoogle Scholar
  47. 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 17:113–122CrossRefGoogle Scholar
  48. 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 97:11632–11637CrossRefGoogle Scholar
  49. Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195CrossRefGoogle Scholar
  50. Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin in Biotechnol 16:123–132CrossRefGoogle Scholar
  51. 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 26:136–138CrossRefGoogle Scholar
  52. 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 33:2047–2062CrossRefGoogle Scholar
  53. 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 39:2740–2753CrossRefGoogle Scholar
  54. 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 109:199–208CrossRefGoogle Scholar
  55. Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297:249–260CrossRefGoogle Scholar
  56. Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183CrossRefGoogle Scholar
  57. 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 65:719–732CrossRefGoogle Scholar
  58. 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 66:5997–6008CrossRefGoogle Scholar
  59. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  60. 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 21:133–139CrossRefGoogle Scholar
  61. Young J (2006) Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9:654–663CrossRefGoogle Scholar
  62. Zarrinpar A, Bhattacharyya RP, Lim WA (2003) The structure and function of proline recognition domains. Sci STKE 179:RE8Google Scholar
  63. 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 55:1142–1156CrossRefGoogle Scholar
  64. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Xingen Zhang
    • 1
  • Huilin Cai
    • 1
  • Meng Lu
    • 1
  • Qiye Wei
    • 1
  • Lijuan Xu
    • 1
  • Chen Bo
    • 1
  • Qing Ma
    • 1
  • Yang Zhao
    • 1
    Email author
  • Beijiu Cheng
    • 1
    Email author
  1. 1.National Engineering Laboratory of Crop Stress Resistance Breeding, School of Life SciencesAnhui Agricultural UniversityHefeiChina

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