Skip to main content
SpringerLink
Log in

GhTZF1 regulates drought stress responses and delays leaf senescence by inhibiting reactive oxygen species accumulation in transgenic Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Redox homeostasis is important for plants to be able to maintain cellular metabolism, and disrupting cellular redox homeostasis will cause oxidative damage to cells and adversely affect plant growth. In this study, a cotton CCCH-type tandem zinc finger gene defined as GhTZF1, which was isolated from a cotton cell wall regeneration SSH library in our previous research, was characterized. GhTZF1 was predominantly expressed during early cell wall regeneration, and it was expressed in various vegetative and reproductive tissues. The expression of GhTZF1 was substantially up-regulated by a variety of abiotic stresses, such as PEG and salt. GhTZF1 also responds to methyl jasmonate (MeJA) and H2O2 treatment. Overexpression of GhTZF1 enhanced drought tolerance and delayed drought-induced leaf senescence in transgenic Arabidopsis. Subsequent experiments indicated that dark- and MeJA-induced leaf senescence was also attenuated in transgenic plants. The amount of H2O2 in transgenic plants was attenuated under both drought conditions and with MeJA-treatment. The activity of superoxide dismutase and peroxidase was higher in transgenic plants than in wild type plants under drought conditions. Quantitative real-time PCR analysis revealed that overexpression of GhTZF1 reduced the expression of oxidative-related senescence-associated genes (SAGs) under drought conditions. Overexpression of GhTZF1 also enhanced oxidative stress tolerance, which was determined by measuring the expression of a set of antioxidant genes and SAGs that were altered in transgenic plants during H2O2 treatment. Hence, we conclude that GhTZF1 may serve as a regulator in mediating drought stress tolerance and subsequent leaf senescence by modulating the reactive oxygen species homeostasis.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Attia H, Karray N, Msilini N, Lachaâl M (2011) Effect of salt stress on gene expression of superoxide dismutases and copper chaperone in Arabidopsis thaliana. Biol Plant 55:159–163

    Article  CAS  Google Scholar 

  • Blackshear P (2002) Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30:945

    Article  CAS  PubMed  Google Scholar 

  • Brossa R, López-Carbonell M, Jubany-Marí T, Alegre L (2011) Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient Arabidopsis plants. J Plant Growth Regul 30:322–333

    Article  CAS  Google Scholar 

  • Carrick DM, Lai WS, Blackshear PJ (2004) The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res Ther 6:248–264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen G, Liu C, Chen SG, Wang L (2012) Role of ARABIDOPSIS A-FIFTEEN in regulating leaf senescence involves response to reactive oxygen species and is dependent on ETHYLENE INSENSITIVE2. J Exp Bot 63:275–292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114

    Article  CAS  PubMed  Google Scholar 

  • Gao C, Wang Y, Liu G, Wang C, Jiang J, Yang C (2010) Cloning of ten peroxidase (POD) genes from Tamarix hispida and characterization of their responses to abiotic stress. Plant Mol Biol Rep 28:77–89

    Article  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Guo Y (2013) Towards systems biological understanding of leaf senescence. Plant Mol Biol 82:519–528

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Gan S (2005) Leaf senescence: signals, execution, and regulation. Curr Top Dev Biol 71:83–112

    Article  CAS  PubMed  Google Scholar 

  • He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang P, Chung M-S, Ju H-W, Na H-S, Lee D, Cheong H-S, Kim C (2011) Physiological characterization of the Arabidopsis thaliana oxidation-related zinc finger 1, a plasma membrane protein involved in oxidative stress. J Plant Res 124:699–705

    Article  CAS  PubMed  Google Scholar 

  • Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant 127:293–303

    Article  CAS  Google Scholar 

  • Irigoyen J, Emerich D, Sánchez-Díaz M (1992) Alfalfa leaf senescence induced by drought stress: photosynthesis, hydrogen peroxide metabolism, lipid peroxidation and ethylene evolution. Physiol Plant 84:67–72

    Article  CAS  Google Scholar 

  • Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161:1202–1216

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413

    Article  CAS  PubMed  Google Scholar 

  • Khanna-Chopra R (2012) Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249:469–481

    Article  CAS  PubMed  Google Scholar 

  • Khanna-Chopra R, Selote DS (2007) Acclimation to drought stress generates oxidative stress tolerance in drought-resistant than -susceptible wheat cultivar under field conditions. Environ Exp Bot 60:276–283

    Article  CAS  Google Scholar 

  • Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20:1260–1277

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141:1376–1388

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kurepa J, Smalle J, Va M, Montagu N, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764

    Article  CAS  PubMed  Google Scholar 

  • Lee S-J, Jung HJ, Kang H, Kim SY (2012a) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol 53:673–686

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Seo PJ, Lee H-J, Park C-M (2012b) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Woo HR, Nam HG (2003) Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci 8:272–278

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Lin P-C, Pomeranz MC, Jikumaru Y, Kang SG, Hah C, Fujioka S, Kamiya Y, Jang J-C (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J 65:253–268

    Article  CAS  PubMed  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  CAS  Google Scholar 

  • Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B (2012) Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot 63:1315–1328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Munné-Bosch S, Jubany-Marí T, Alegre L (2001) Drought—induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant, Cell Environ 24:1319–1327

    Article  Google Scholar 

  • Navabpour S, Morris K, Allen R, Harrison E, Soheila A, Buchanan-Wollaston V (2003) Expression of senescence—enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292

    Article  CAS  PubMed  Google Scholar 

  • Pastori G, Río L (1994) An activated-oxygen-mediated role for peroxisomes in the mechanism of senescence of Pisum sativum L. leaves. Planta 193:385–391

    Article  CAS  Google Scholar 

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium(IV). Anal Biochem 139:487–492

    Article  CAS  PubMed  Google Scholar 

  • Pomeranz MC, Hah C, Lin PC, Kang SG, Finer JJ, Blackshear PJ, Jang JC (2010) The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol 152:151–165

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pomeranz M, Finer J, Jang J-C (2011) Putative molecular mechanisms underlying tandem CCCH zinc finger protein mediated plant growth, stress, and gene expression responses. Plant Signal Behav 6:647–651

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    Article  CAS  Google Scholar 

  • Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci 104:19631–19636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Scalet M, Federico R, Guido MC, Manes F (1995) Peroxidase activity and polyamine changes in response to ozone and simulated acid rain in Aleppo pine needles. Environ Exp Bot 35:417–425

    Article  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139

    Article  CAS  Google Scholar 

  • Stumpo DJ, Byrd NA, Phillips RS, Ghosh S, Maronpot RR, Castranio T, Meyers EN, Mishina Y, Blackshear PJ (2004) Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the tristetraprolin family. Mol Cell Biol 24:6445–6455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun J, Jiang H, Xu Y, Li H, Wu X, Xie Q, Li C (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valente MAS, Faria JAQA, Soares-Ramos JRL, Reis PAB, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MAO, Fietto LG, Loureiro ME, Aragao FJL, Fontes EPB (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J Exp Bot 60:533–546

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genom 9:44

    Article  Google Scholar 

  • Weaver L, Gan S, Quirino B, Amasino R (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469

    Article  CAS  PubMed  Google Scholar 

  • Wi S, Jang S, Park K (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30:37–49

    Article  CAS  PubMed  Google Scholar 

  • Woo HR, Kim JH, Nam HG, Lim PO (2004) The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. Plant Cell Physiol 45:923–932

    Article  CAS  PubMed  Google Scholar 

  • Yan J, He C, Wang J, Mao Z, Holaday SA, Allen RD, Zhang H (2004) Overexpression of the Arabidopsis 14-3-3 protein GF14λ in cotton leads to a “stay-green” phenotype and improves stress tolerance under moderate drought conditions. Plant Cell Physiol 45:1007–1014

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Tu L, Zhu L, Fu L, Min L, Zhang X (2008) Expression profile analysis of genes involved in cell wall regeneration during protoplast culture in cotton by suppression subtractive hybridization and macroarray. J Exp Bot 59:3661–3674

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Young TE, Meeley RB, Gallie DR (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J 40:813–825

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Wang W, Zhang G, Kaminek M, Dobrev P, Xu J, Gruissem W (2010) Senescence-inducible expression of isopentenyl transferase extends leaf life, increases drought stress resistance and alters cytokinin metabolism in cassava. J Integr Plant Biol 59:653–669

    Google Scholar 

  • Zhu L, Tu L, Zhu F, Liu D, Zhang X (2005) An improved simple protocol for isolation of high quality RNA from Gossypium spp. suitable for cDNA library construction. Acta Agronomica Sinica 31:1657–1659

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the funding of the National Natural Science Foundation of China (Nos. 31101185, 31371675) and the National High-tech R&D Program of China (863 Program) (No. 2013AA102601-4).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Ting Zhou, Xiyan Yang, Lichen Wang, Jiao Xu & Xianlong Zhang

Authors
  1. Ting Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiyan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lichen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xianlong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiyan Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, T., Yang, X., Wang, L. et al. GhTZF1 regulates drought stress responses and delays leaf senescence by inhibiting reactive oxygen species accumulation in transgenic Arabidopsis . Plant Mol Biol 85, 163–177 (2014). https://doi.org/10.1007/s11103-014-0175-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-014-0175-z

Keywords

Search

Navigation