Skip to main content
SpringerLink
Log in

Overexpression of the novel Zygophyllum xanthoxylum C2H2-type zinc finger gene ZxZF improves drought tolerance in transgenic Arabidopsis and poplar

  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Zygophyllum xanthoxylum (Bunge) is a perennial woody succulent xerophyte that is one of the most droughttolerant plant species identified to date. In this study, the gene encoding the novel C2H2-type zinc finger protein (ZFP) ZxZF was cloned from Z. Xanthoxylum and expressed in both Arabidopsis thaliana and poplar (Populus × euramericana cl. Bofeng 1) under the control of the drought-inducible promoter rd29A. Overexpression in Arabidopsis resulted in a higher survival rate and enhanced root growth compared with wild type (WT) plants under osmotic stress conditions induced by mannitol. Overexpression in poplar under stress conditions induced by PEG6000 improved photosynthetic function as evidenced by a higher maximum photochemical activity of photosystem II (PSII) (Fv/Fm) and elevated chlorophyll content. Furthermore, leaf tissue of transgenic poplar accumulated less malondialdehyde (MDA), and both superoxide dismutase (SOD) and peroxidase (POD) activities were elevated in transgenic plants. These results suggest that ZxZF overexpression played an essential role in drought tolerance in both Arabidopsis and poplar. Incorporating overexpression of ZxZF and other A1 subgroup C2H2 zinc finger proteins in plant breeding programs may result in enhanced drought tolerance.

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

Similar content being viewed by others

Abbreviations

ZFP:

zinc finger protein

WT:

wild type

PSII:

photosystem II

MDA:

malondialdehyde

SOD:

superoxide dismutase

POD:

peroxidase

C2H2:

Cys2/His2

rd29A:

RESPONSIVE TO DESSICATION 29A

TCA:

trichloroacetic acid

TBA:

thiobarbituric acid

References

  • An Y.Q., McDowell J.M., Huang S., McKinney E.C., Chambliss S. & Meagher R.B. 1996. Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 10: 107–121.

    Article  CAS  PubMed  Google Scholar 

  • Bailly C., Benamar A., Corbineau F. & Come D. 1996. Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol. Plant. 97: 104–110.

    Article  CAS  Google Scholar 

  • Bechtold N., Jolivet S., Voisin R. & Pelletier G. 2003. The endosperm and the embryo of Arabidopsis thaliana are independently transformed through infiltration by Agrobacterium tumefaciens. Transgenic Res. 12: 509–517.

    Article  CAS  PubMed  Google Scholar 

  • Chandra Rai. A., Singh M. & Shah K. 2012. Effect of water withdrawal on formation of free radical, proline accumulation and activities of antioxidant enzymes in ZAT12-transformed transgenic tomato plants. Plant Physiol. Biochem. 61: 108–114.

    Article  CAS  Google Scholar 

  • Ciftci-Yilmaz S. & Mittler R. 2008. The zinc finger network of plants. Cell Mol. Life Sci. 65: 1150–1160.

    Article  CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz S., Morsy M.R., Song L., Coutu A., Krizek B.A., Lewis M.W., Warren D., Cushman J., Connolly E.L. & Mittler R. 2007. The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J. Biol. Chem. 282: 9260–9268.

    Article  CAS  PubMed  Google Scholar 

  • Czechowski T., Stitt M., Altmann T., Udvardi M.K. & Scheible W-R. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidipsis. Plant Physiol. 139: 5–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dathan N., Zaccaro L., Esposito S., Isernia C., Omichinski J.G., Riccio A., Pedone C., Blasio B.D., Fattorusso R. & Pedone P.V. 2002. The Arabidopsis SUPERMAN protein is able to specifically bind DNA through its single Cys2-His2 zinc finger motif. Nucleic Acids Res. 30: 4945–4951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Englbrecht C.C., Schoof H. & Böhm S. 2014. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5(1): 39.

    Article  CAS  Google Scholar 

  • Feurtado J.A., Huang D.Q., Wicki-Stordeur L., Hemstock L.E., Potentier M.S., Tsang E.W. & Cutler A.J. 2011. The Arabidopsis C2H2 zinc finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. Plant Cell 23: 1772–1194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hichri I., Muhovski Y., Žižkova E., Dobrev P.I., Franco-Zorrilla J.M., Solano R., Lopez-Vidriero I., Motyka V. & Lutts S. 2014. The Solanum lycopersicum Zinc Finger2 cysteine-2/histidine-2 repressor-like transcription factor regulates development and tolerance to salinity in tomato and Arabidopsis. Plant Physiol. 164: 1967–1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J., Yang X., Wang M.M., Tang H.J., Ding L.Y., Shen Y. & Zhang H.S. 2007. A novel rice C2H2-type zinc finger protein lacking DLN-box/EAR-motif plays a role in salt tolerance. Biochim. Biophys. Acta 1769: 220–227.

    Article  CAS  PubMed  Google Scholar 

  • Huang X.Y., Chao D.Y., Gao J.P., Zhu M.Z., Shi M. & Lin H.X. 2009. A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev. 23: 1805–1817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inskeep W.P. & Bloom P.R. 1985. Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol. 77: 483–485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin J.P., Zhang H., Kong L., Gao G. & Luo J.C. 2014. Plant-TFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 42: D1182–D1187.

  • Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17: 287–291.

    Article  CAS  PubMed  Google Scholar 

  • Kiełbowicz-Matuk A. 2012. Involvement of plant C2H2-type zinc finger transcription factors in stress responses. Plant Sci. 185-186: 78–85.

    Article  PubMed  CAS  Google Scholar 

  • Kodaira K.S., Qin F., Tran L.S., Maruyama K., Kidokoro S., Fujita Y., Shinozaki K. & Yamaguchi-Shinozaki K. 2011. Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol. 157: 742–756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazár D., Sušila P. & Nauš J. 2006. Early detection of plant stress from changes in distributions of chlorophyll a fluorescence parameters measured with fluorescence imaging. J. Fluoresc. 16: 173–176.

    Article  PubMed  CAS  Google Scholar 

  • Liu Q.G., Wang Z.C., Xu X.M., Zhang H.Z. & Li C.H. 2015. Genome-wide analysis of C2H2 zinc-finger family transcription factors and their responses to abiotic stresses in poplar (Populus trichocarpa). PLoS ONE. 10: e0134753.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X.M., Nguyen X.C., Kim K.E., Han H.J., Yoo J., Lee K., Kim M.C., Yun D.J. & Chung W.S. 2013. Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochem. Biophys. Res. Com. 430: 1054–1059.

    Article  CAS  PubMed  Google Scholar 

  • Livak K.J. & Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25: 402–408.

    Article  CAS  PubMed  Google Scholar 

  • Luo M., Bilodeau P., Koltunow A., Dennis E.S., Peacock W.J. & Chaudhury A.M. 1999. Genes controlling fertilizationindependent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 96: 296–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo X., Bai X., Zhu D., Li Y., Ji W., Cai H., Wu J., Liu B.H. & Zhu Y.M. 2012a. GsZFP1, a new Cys2/His2-type zinc-finger protein, is a positive regulator of plant tolerance to cold and drought stress. Planta 235: 1141–1155.

    Article  CAS  PubMed  Google Scholar 

  • Luo X., Cui N., Zhu Y.M., Cao L., Zhai H., Cai H., Ji W., Wang X., Zhu D., Li Y. & Bai X. 2012b. Over-expression of GsZFP1, an ABA-responsive C2H2-type zinc finger protein lacking a QALGGH motif, reduces ABA sensitivity and decreases stomata size. J. Plant Physiol. 169: 1192–1202.

    Article  CAS  PubMed  Google Scholar 

  • Martin L., Leblanc-Fournier N., Azri W., Lenne C., Henry C., Coutand C. & Julien J-L. 2009. Characterization and expression analysis under bending and other abiotic factors of PtaZFP2, a poplar gene encoding a Cys2/His2 zinc finger protein. Tree Physiol. 29: 125–136.

    Article  CAS  PubMed  Google Scholar 

  • Mittler R., Vanderauwera S., Gollery M. & Breusegem F.V. 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9: 490–498.

    Article  CAS  PubMed  Google Scholar 

  • Mohanty B., Krishnan S.P.T., Swarup S. & Bajic V.B. 2005. Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Ann. Bot. 96: 669–681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakajima K. & Benfey P.N. 2002. Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14: S265–S276.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K., Yamaguchi-Shinozaki K. & Shinozaki K. 2014. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front. Plant Sci. 5: 170.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pei S.F., Fu H., Chen Y.M. & Li J.B. 2004. Influence of Z. xanthoxylum shrubs on soil fertility in enclosure and grazing conditions. J. Desert Res. 24: 763–767.

    Google Scholar 

  • Pennisi E. 2008. Getting to the root of drought responses. Science 320: 173.

    Article  PubMed  Google Scholar 

  • Rai A.C., Singh M. & Shah K. 2013. Engineering drought tolerant tomato plants over-expressing BcZAT12 gene encoding a C2H2 zinc finger transcription factor. Phytochemistry 85: 44–50.

    Article  CAS  PubMed  Google Scholar 

  • Roháček K. 2002. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40: 13–29.

    Article  Google Scholar 

  • Shi H.T., Wang X., Ye T.T., Chen F.F., Deng J., Yang P.F., Zhang Y.S. & Chan Z.L. 2014. The Cysteine2/Histidine2-type transcription factor ZINC FINGER OF ARABIDOPSIS THALIANA6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and CREPEAT-BINDING FACTOR genes in Arabidopsis. Plant Physiol. 165: 1367–1379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun S.J., Guo S.Q., Yang X., Bao Y.M., Tang H.J., Sun H., Huang J. & Zhang H.S. 2010. Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J. Exp. Bot. 61: 2807–2818.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R., Bartels D. & Kirch H.H. 2003. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J. 35: 452–464.

    Article  CAS  PubMed  Google Scholar 

  • Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang L.L., Cai H., Ji W., Luo X., Wang Z.Y., Wu J., Wang X.D., Cui L., Wang Y., Zhu Y.M. & Bai X. 2013. Overexpression of GsZFP1 enhances salt and drought tolerance in transgenic alfalfa (Medicago sativa L.). Plant Physiol. Biochem. 71: 22–30.

    Article  CAS  PubMed  Google Scholar 

  • Tang Q.Y. & Feng M.G. 2002. DPS data processing system for practical statistics. Beijing: Science Press.

    Google Scholar 

  • Wang Y.C., Gao C.Q., Liang Y.N., Wang C., Yang C.P. & Liu G.F. 2010. A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J. Plant Physiol. 167: 222–230.

    Article  CAS  PubMed  Google Scholar 

  • Weng J.H. & Lai M.F. 2005. Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. Photosynthetica 43: 439–444.

    Article  CAS  Google Scholar 

  • Wolfe S.A., Nekludova L. & Pabo C.O. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29: 183–212.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K. & Shinozaki K. 1993. Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol. 101: 1119–1120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y.J., Ma C., Xu Y.J., Wei Q., Imtiaz M., Lan H.B., Gao S., Cheng L.N., Wang M.Y., Fei Z.J., Hong B. & Gao J.P. 2014. A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis. Plant Cell 26: 2038–2054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H., Ni L., Liu Y.P., Wang Y.F., Zhang A.Y., Tan M.P. & Jiang M.Y. 2012. The C2H2-type zinc finger protein ZFP182 is involved in abscisic acid-induced antioxidant defense in rice. J. Integr. Plant Biol. 54: 500–510.

    Article  CAS  PubMed  Google Scholar 

  • Zhang W.X., Liu B.Y., Ding C.J., Zhang B.Y., Huang Q.J., Chu Y.G. & Su XH. 2014. Transformation of zinc finger protein transcription factor gene (ZxZF) and preliminary evaluation of drought tolerance in Populus × euramericana. Sci. Sil. Sin. 50: 31–37.

    Google Scholar 

Download references

Author information

Author notes

  1. Yanguang Chu and Weixi Zhang contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry; Key Laboratory of Tree Breeding and Cultivation, State Forestry Administration, WanShouShan, Beijing, 100091, People’s Republic of China

    Yanguang Chu, Qinjun Huang, Bingyu Zhang & Xiaohua Su

  2. Institute of Crop Science, Chinese Academy of Agricultural Sciences, No. 12, Zhongguancun South Street, Beijing, 100081, People’s Republic of China

    Weixi Zhang & Bin Wu

Authors
  1. Yanguang Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weixi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinjun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bingyu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaohua Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaohua Su.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chu, Y., Zhang, W., Wu, B. et al. Overexpression of the novel Zygophyllum xanthoxylum C2H2-type zinc finger gene ZxZF improves drought tolerance in transgenic Arabidopsis and poplar. Biologia 71, 769–776 (2016). https://doi.org/10.1515/biolog-2016-0093

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/biolog-2016-0093

Key words

Search

Navigation