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Cloning and expression of a tau class glutathione S-transferase (ZjGSTU1) from Chinese jujube in response to phytoplasma infection

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Abstract

Phytoplasmas are associated with diseases of several hundred plant species. Jujube witches’ broom disease (JWB) is a destructive phytoplasma disease in Chinese jujube (Ziziphus jujuba Mill.). Ziziphus jujuba Mill. ‘J5’, an excellent strain with extremely high resistance to JWB, was selected by us. In our previous study, a GST (EC 2.5.1.18) fragment was sequenced from suppression subtractive hybridization library of ‘J5’ under JWB phytoplasma stress. Based on this result, a GST gene (ZjGSTU1, HM345954) was first isolated from jujube by homology cloning and RACE. ZjGSTU1 contains a complete open reading frame of 702 bp encoding a protein of 233 amino acid residues. Sequence alignment showed that ZjGSTU1 shared a typical conserved structure and high identity with tau GSTs from other plant species. Relative RT-PCR demonstrated that the expression of ZjGSTU1 mRNA in jujube leaves and branches could be triggered by JWB phytoplasma. Moreover, the expression of ZjGSTU1 mRNA in resistant strain ‘J5’ increased sooner and higher than that in sensitive strain ‘J9’ under JWB phytoplasma stress (‘J5’ and ‘J9’ are two strains from the same cultivar). Western blotting analyses showed that the expressions of ZjGSTU1 in ‘J5’ and ‘J9’ were dramatically up-regulated under JWB phytoplasma stress and its expression in ‘J5’ was also higher than that in ‘J9’ at protein level. Collectively, this paper highlights that ZjGSTU1 gene is responsive to phytoplasma infection. The possible roles of this gene were discussed in terms of regulatory process in resistance to phytoplasma infection.

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References

  • Agrawal GK, Jwa NS, Rakwal R (2002) A pathogen-induced novel rice (Oryza sativa L.) gene encodes a putative protein homologous to type II glutathione s-transferases. Plant Sci 163:1153–1160

    Article  CAS  Google Scholar 

  • Aliya S, Reddanna P, Thyagaraju K (2003) Does glutathione S-transferase Pi (GST-Pi) a marker protein for cancer? Mol Cell Biochem 253:319–327

    Article  PubMed  CAS  Google Scholar 

  • Benekos K, Kissoudis C, Nianiou IO, Labrou N, Madesis P, Kalamaki M, Makris A, Tsaftaris A (2010) Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotechnol 150:195–201

    Article  PubMed  CAS  Google Scholar 

  • David PD, Jonathan DS, Robert E (2011) The Arabidopsis phi class glutathione transferase AtGSTF2 binding and regulation by biologically active heterocyclic ligands. Biochem J 438:63–70

    Article  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2002) Comparison of relative RT-PCR and Northern Blot analyses to measure expression of β-1,3-Glucanase in Nicotiana benthamiana infected with colltotrichum destructivum. Plant Mol Biol Rep 20:347–356

    Article  CAS  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione s-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  PubMed  CAS  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:3004.1

    Article  Google Scholar 

  • Droog F (1997) Plant glutathione S-transferases, a tale of theta and tau. J Plant Growth Regul 16:95–107

    Article  CAS  Google Scholar 

  • Droog F, Hooykaas P, Zaal BJ (1995) 2,4-Dichlorophenoxyacetic acid and related chlorinated compounds inhibit two auxin-regulated type-III tobacco glutathione S-transferases. Plant Physiol 107:1139–1146

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dudler R, Hertig C, Rebman G, Bull J, Mauch F (1991) A pathogen-induced wheat gene encodes a protein homologous to glutathione S-transferases. Mol Plant-Microbe Interact 4:14–18

    Article  PubMed  CAS  Google Scholar 

  • Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624

    Article  PubMed  CAS  Google Scholar 

  • Gullner G, Komives T (2001) The role of glutathione and glutathione-related enzymes in plant-pathogen interactions. In: Grill D, Tausz M, Kok L (eds) Significance of glutathione in plant adaptation to the environment. Kluwer Academic Publishers, Dordrecht, pp 207–239

    Chapter  Google Scholar 

  • Hahn K, Strittmatter G (1994) Pathogen-defense gene prp1-1 from potato encodes an auxin-responsive glutathione S-transferase. Eur J Biochem 226:619–626

    Article  PubMed  CAS  Google Scholar 

  • Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832

    Article  PubMed  CAS  Google Scholar 

  • Jones AM, Thomas V, Truman B, Lilley K, Mansfield J, Grant M (2004) Specific changes in the Arabidopsis proteome in response to bacterial challenge: differentiating basal and R-gene mediated resistance. Phytochemistry 65:1805–1816

    Article  PubMed  CAS  Google Scholar 

  • Kilili KG, Atanassova N, Vardanyan A, Clatot N, Sabarna KA, Kanellopoulos PN, Makris AM, Kampranis SC (2004) Differential roles of tau class glutathione S-transferases in oxidative stress. J Biol Chem 279:24540–24551

    Article  PubMed  CAS  Google Scholar 

  • Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu MJ, Zhao J, Zhou JY (2010) Jujube witches’ broom. China Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • Liu YQ, Peng L, Ning Q, Zhao J, Liu MJ (2012) Effect of jujube witches’ broom (JWB) phytoplasma on the chlorophyll and several protective enzymes in jujube trees. Acta Agriculturae Boreali-Sinica 27(2):213–217 (in Chinese)

    Google Scholar 

  • Liu YJ, Han XM, Ren LL, Yang H, Zeng QY (2013) Functional divergence of the GST supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol 161:773–786

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Margaria P, Abbà S, Palmano S (2013) Novel aspects of grapevine response to phytoplasma infection investigated by a proteomic and phospho-proteomic approach with data integration into functional networks. BMC Genom 14:38

    Article  CAS  Google Scholar 

  • Matz M, Shagin D, Bogdanova E, Britanova O, Lukyanov S, Diatchenko L, Chenchik A (1999) Amplification of cDNA ends based on template-switching effect and step-out PCR. Nucleic Acids Res 27:1558–1560

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Perl-Treves R, Foley RC, Chen W, Singh KB (2004) Early induction of the Arabidopsis GSTF8 promoter by specific strains of the fungal pathogen Rhizoctonia solani. Mol Plant Microbe Interact 17:70–80

    Article  PubMed  CAS  Google Scholar 

  • Qiao Y, Zhao J, Wu TY, Yang YR, Liu MJ (2009) Genetic diversity of twenty three strains of Ziziphus jujuba Mill. cv. Junzao with different levels of resistance to jujube witches’ broom disease. Acta Hort. 840:391–397

    Google Scholar 

  • Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68

    Article  PubMed  CAS  Google Scholar 

  • Shi HY, Li ZH, Zhang YX, Chen L, Xiang DY, Zhang YF (2014) Two pear glutathione s-transferases genes are regulated during fruit development and involved in response to salicylic acid, auxin, and glucose signaling. PLoS ONE 9(2):e89926. doi:10.1371/journal.pone.0089926

    Article  PubMed  PubMed Central  Google Scholar 

  • Soranzo N, Gorla MS, Mizzi L, Toma GD, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271:511–521

    Article  PubMed  CAS  Google Scholar 

  • Strauss E (2009) Phytoplasma research begins to bloom. Science 325:388–390

    Article  PubMed  CAS  Google Scholar 

  • Sun HF, Meng YP, Cui GM, Cao QF, Li J, Liang AH (2009) Selection of house keeping genes for gene expression studies on the development of fruit bearing shoots in Chinese jujube (Ziziphus jujuba Mill.). Mol Biol Rep 36:2183–2190

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Nagata T (1992) ParB: an auxin regulated gene encoding glutathione S-transferase. PNAS 89:56–59

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Y (2012) Construction of SSH-cDNA library of Chinese jujube infected with phytoplasma and its ESTs analysis. Agricultural University of Hebei, Master’s degree thesis (in Chinese)

  • Zhao J, Liu ZC, Dai L, Liu MJ (2005) Isolation of total RNA for different organs and tissues of Ziziphus jujuba Mill. J Plant Genet Res 10:111–117 (in Chinese)

    Google Scholar 

  • Zhao MR, Han YY, Feng YN, Li F, Wang W (2012) Expansions are involved in cell growth mediated by abscisic acid and indole-3-acetic acid under drought stress in wheat. Plant Cell Rep 31:671–685

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by grants from the Natural Science Foundation of Hebei Province (C2010000679, C2009000534), and the Provincial Key Technology R&D Program of Hebei, China (11230606D-6). The authors are grateful to Dr. Fang Xu, Dr. Haiyan Shi and Dr. Oliver Dong for critical reading of the manuscript.

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Authors and Affiliations

  1. College of Life Science, Agricultural University of Hebei, Baoding, 071000, China

    Long Peng, Yanlin Zhao & Jin Zhao

  2. Research Center of Chinese Jujube, Agricultural University of Hebei, Baoding, 071000, China

    Zhihui Zhao & Mengjun Liu

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  1. Long Peng
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  2. Yanlin Zhao
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  3. Zhihui Zhao
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  4. Jin Zhao
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  5. Mengjun Liu
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Corresponding authors

Correspondence to Jin Zhao or Mengjun Liu.

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Communicated by E. Kuzniak-Gebarowska.

L. Peng and Y. Zhao equally contributed to this research work.

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Peng, L., Zhao, Y., Zhao, Z. et al. Cloning and expression of a tau class glutathione S-transferase (ZjGSTU1) from Chinese jujube in response to phytoplasma infection. Acta Physiol Plant 36, 2905–2913 (2014). https://doi.org/10.1007/s11738-014-1660-3

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  • DOI: https://doi.org/10.1007/s11738-014-1660-3

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