Overexpression of the novel Zygophyllum xanthoxylum C2H2-type zinc finger gene ZxZF improves drought tolerance in transgenic Arabidopsis and poplar
Abstract
Zygophyllum xanthoxylum (Bunge) is a perennial woody succulent xerophyte that is one of the most drought-tolerant 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.
Acknowledgements
This work was financially supported by the National High-Tech Research and Development Program (863 Program) from Ministry of Science and Technology of China (Grant No. 2013AA102703).
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: 107–121.10.1046/j.1365-313X.1996.10010107.xSuche in Google Scholar PubMed
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: 104–110.10.1111/j.1399-3054.1996.tb00485.xSuche in 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: 509–517.10.1023/A:1024272023966Suche in 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: 108–114.10.1016/j.plaphy.2012.09.010Suche in Google Scholar PubMed
Ciftci-Yilmaz S. & Mittler R. 2008. The zinc finger network of plants. Cell Mol. Life Sci. 65: 1150–1160.10.1007/s00018-007-7473-4Suche in Google Scholar PubMed
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: 9260–9268.10.1074/jbc.M611093200Suche in Google Scholar PubMed
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: 5–17.10.1104/pp.105.063743Suche in Google Scholar PubMed PubMed Central
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: 4945–4951.10.1093/nar/gkf613Suche in Google Scholar PubMed PubMed Central
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): 39.10.1186/1471-2164-5-39Suche in Google Scholar PubMed PubMed Central
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: 1772–1194.10.1105/tpc.111.085134Suche in Google Scholar PubMed PubMed Central
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: 1967–1990.10.1104/pp.113.225920Suche in Google Scholar PubMed PubMed Central
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: 220–227.10.1016/j.bbaexp.2007.02.006Suche in Google Scholar PubMed
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: 1805–1817.10.1101/gad.1812409Suche in Google Scholar PubMed PubMed Central
Inskeep W.P. & Bloom P.R. 1985. Extinction coefficients of chlorophyll a and b in N, N-dimethylformamide and 80% acetone. Plant Physiol. 77: 483–485.10.1104/pp.77.2.483Suche in Google Scholar PubMed PubMed Central
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–D1187.10.1093/nar/gkt1016Suche in Google Scholar PubMed PubMed Central
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: 287–291.10.1038/7036Suche in Google Scholar PubMed
Kiełbowicz-Matuk A. 2012. Involvement of plant C2H2-type zinc finger transcription factors in stress responses. Plant Sci. 185–186: 78–85.10.1016/j.plantsci.2011.11.015Suche in Google Scholar PubMed
Kodaira K.S., Qin F., Tran L.S., Maruyama K., Kidokoro S., Fujita Y., Shinozaki K. & Yamaguchi-Shinozaki K. 2011. Ara-bidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol. 157: 742–756.10.1104/pp.111.182683Suche in Google Scholar PubMed PubMed Central
Lazâr 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: 173–176.10.1007/s10895-005-0032-1Suche in Google Scholar PubMed
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: e0134753.10.1371/journal.pone.0134753Suche in Google Scholar PubMed PubMed Central
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: 1054–1059.10.1016/j.bbrc.2012.12.039Suche in Google Scholar PubMed
Livak K.J. & Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25: 402–408.10.1006/meth.2001.1262Suche in Google Scholar PubMed
Luo M., Bilodeau P., Koltunow A., Dennis E.S., Peacock W.J. & Chaudhury A.M. 1999. Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 96: 296–301.10.1073/pnas.96.1.296Suche in Google Scholar PubMed PubMed Central
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: 1141–1155.10.1007/s00425-011-1563-0Suche in Google Scholar PubMed
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: 1192–1202.10.1016/j.jplph.2012.03.019Suche in Google Scholar PubMed
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: 125–136.10.1093/treephys/tpn011Suche in Google Scholar PubMed
Mittler R., Vanderauwera S., Gollery M. & Breusegem F.V. 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9: 490–498.10.1016/j.tplants.2004.08.009Suche in Google Scholar PubMed
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: 669–681.10.1093/aob/mci219Suche in Google Scholar PubMed PubMed Central
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–S276.10.1105/tpc.010471Suche in Google Scholar PubMed PubMed Central
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: 170.10.3389/fpls.2014.00170Suche in Google Scholar PubMed PubMed Central
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.Suche in Google Scholar
Pennisi E. 2008. Getting to the root of drought responses. Science 320: 173.10.1126/science.320.5873.173Suche in Google Scholar PubMed
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: 44–50.10.1016/j.phytochem.2012.09.007Suche in Google Scholar PubMed
Roháček K. 2002. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40: 13–29.10.1023/A:1020125719386Suche in 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: 1367–1379.10.1104/pp.114.242404Suche in Google Scholar PubMed PubMed Central
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: 2807–2818.10.1093/jxb/erq120Suche in Google Scholar PubMed PubMed Central
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: 452–464.10.1046/j.1365-313X.2003.01819.xSuche in Google Scholar PubMed
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: 2731–2739.10.1093/molbev/msr121Suche in Google Scholar PubMed PubMed Central
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: 22–30.10.1016/j.plaphy.2013.06.024Suche in Google Scholar PubMed
Tang Q.Y. & Feng M.G. 2002. DPS data processing system for practical statistics. Beijing: Science Press.Suche in 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: 222–230.10.1016/j.jplph.2009.09.008Suche in Google Scholar PubMed
Weng J.H. & Lai M.F. 2005. Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. Photosynthetica 43: 439–444.10.1007/s11099-005-0070-6Suche in Google Scholar
Wolfe S.A., Nekludova L. & Pabo C.O. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29: 183–212.10.1146/annurev.biophys.29.1.183Suche in Google Scholar PubMed
Yamaguchi-Shinozaki K. & Shinozaki K. 1993. Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol. 101: 1119–1120.10.1104/pp.101.3.1119Suche in Google Scholar PubMed PubMed Central
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: 2038–2054.10.1105/tpc.114.124867Suche in Google Scholar PubMed PubMed Central
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: 500–510.10.1111/j.1744-7909.2012.01135.xSuche in Google Scholar PubMed
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.Suche in Google Scholar
- 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
©2016 Institute of Botany, Slovak Academy of Sciences
Artikel in diesem Heft
- Zoology
- Climate warming and invasive fish species: Will they replace native fish species in waters of temperate zones?
- Cellular and Molecular Biology
- Production of poly-3-hydroxybutyrate from mixed culture
- Cellular and Molecular Biology
- Molecular and immunological characterization of Lp1, the 34 kDa outer membrane lipoprotein of Pseudomonas aeruginosa
- Cellular and Molecular Biology
- Antibacterial activity of a microemulsion loaded with cephalosporin
- Cellular and Molecular Biology
- Isolation and characterization of Vibrio alginolyticus from cultured amphioxus Branchiostoma belcheri tsingtauense
- Cellular and Molecular Biology
- Somatic embryogenesis in Phlox paniculata – histological analysis
- Botany
- Overexpression of the novel Zygophyllum xanthoxylum C2H2-type zinc finger gene ZxZF improves drought tolerance in transgenic Arabidopsis and poplar
- Botany
- Vegetation diversity of the two Dinaric karstic rivers in Bosnia and Herzegovina
- Botany
- Diversity and spatial patterns of plant communities in volcanic temporary ponds of Sicily (Italy)
- Zoology
- Erythraeus (Erythraeus) pistacicus sp. n. (Trombidiformes: Erythraeidae) from southern Iran, and notes on other Erythraeus spp.
- Zoology
- Studies on eucrenal-hypocrenal zonation of springs along the river mainstream: A case study of a karst canyon in Bosnia and Herzegovina
- Zoology
- Different catching series from light and pheromone trapping of Helicoverpa armigera (Lepidoptera: Noctuidae)
- Zoology
- Newts in the nature reserve Dönche: Evaluation of diversity, breeding behaviour and threats due to a decline in habitat suitability
- Zoology
- Antioxidant status of rabbits after treatment with epicatechin and patulin
Artikel in diesem Heft
- Zoology
- Climate warming and invasive fish species: Will they replace native fish species in waters of temperate zones?
- Cellular and Molecular Biology
- Production of poly-3-hydroxybutyrate from mixed culture
- Cellular and Molecular Biology
- Molecular and immunological characterization of Lp1, the 34 kDa outer membrane lipoprotein of Pseudomonas aeruginosa
- Cellular and Molecular Biology
- Antibacterial activity of a microemulsion loaded with cephalosporin
- Cellular and Molecular Biology
- Isolation and characterization of Vibrio alginolyticus from cultured amphioxus Branchiostoma belcheri tsingtauense
- Cellular and Molecular Biology
- Somatic embryogenesis in Phlox paniculata – histological analysis
- Botany
- Overexpression of the novel Zygophyllum xanthoxylum C2H2-type zinc finger gene ZxZF improves drought tolerance in transgenic Arabidopsis and poplar
- Botany
- Vegetation diversity of the two Dinaric karstic rivers in Bosnia and Herzegovina
- Botany
- Diversity and spatial patterns of plant communities in volcanic temporary ponds of Sicily (Italy)
- Zoology
- Erythraeus (Erythraeus) pistacicus sp. n. (Trombidiformes: Erythraeidae) from southern Iran, and notes on other Erythraeus spp.
- Zoology
- Studies on eucrenal-hypocrenal zonation of springs along the river mainstream: A case study of a karst canyon in Bosnia and Herzegovina
- Zoology
- Different catching series from light and pheromone trapping of Helicoverpa armigera (Lepidoptera: Noctuidae)
- Zoology
- Newts in the nature reserve Dönche: Evaluation of diversity, breeding behaviour and threats due to a decline in habitat suitability
- Zoology
- Antioxidant status of rabbits after treatment with epicatechin and patulin