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Identification and Expression Pattern of a ZPR1 Gene in Wild Tomato (Solanum Pennellii)

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Abstract

The mammalian zinc finger protein ZPR1 is known to be essential in cell cycle progression, but its homolog in plants remains to be identified. Here, we isolated SpZPR1 from the wild tomato species Solanum pennellii LA0716 and found that its protein sequence shares homology with ZPR1 genes from other organisms. SpZPR1 mRNA was found to accumulate in tomato apical meristem in response to ABA (abscisic acid) treatment and heat stress. A transactivation activity assay in yeast revealed that SpZPR1 functions as a transcriptional activator, while the results of our gel electrophoresis mobility shift assay showed that SpZPR1 was able to bind the ABRE (ABA-responsive element) sequence in vitro. Our study is the first to provide evidence that SpZPR1 is involved in the ABA signaling network and plays a potential role in plant cell development and abiotic stress response.

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References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  PubMed  CAS  Google Scholar 

  • Antoni R, Rodriguez L, Gonzalez-Guzman M, Pizzio GA, Rodriguez PL (2011) News on ABA transport, protein degradation, and ABFs/WRKYs in ABA signaling. Curr Opin Plant Biol 14:547–553

    Article  PubMed  CAS  Google Scholar 

  • Barrero JM, Piqueras P, Gonzalez-Guzman M, Serrano R, Rodriguez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56:2071–2083

    Article  PubMed  CAS  Google Scholar 

  • Cuartero J, Bolarin MC, Asins MJ, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57:1045–1058

    Article  PubMed  CAS  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  PubMed  CAS  Google Scholar 

  • Dewey C, Wu JQ, Cawley S, Alexandersson M, Gibbs R, Pachter L (2004) Accurate identification of novel human genes through simultaneous gene prediction in human, mouse, and rat. Genome Res 14:661–664

    Article  PubMed  CAS  Google Scholar 

  • Doran B, Gherbesi N, Hendricks G, Flavell RA, Davis RJ, Gangwani L (2006) Deficiency of the zinc finger protein ZPR1 causes neurodegeneration. Proc Natl Acad Sci USA 103:7471–7475

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132

    Article  PubMed  CAS  Google Scholar 

  • Galcheva-Gargova Z, Konstantinov KN, Wu IH, Klier FG, Barrett T, Davis RJ (1996) Binding of zinc finger protein ZPR1 to the epidermal growth factor receptor. Science 272:1797–1802

    Article  PubMed  CAS  Google Scholar 

  • Galcheva-Gargova Z, Gangwani L, Konstantinov KN, Mikrut M, Theroux SJ, Enoch T, Davis RJ (1998) The cytoplasmic zinc finger protein ZPR1 accumulates in the nucleolus of proliferating cells. Mol Biol Cell 9:2963–2971

    PubMed  CAS  Google Scholar 

  • Gangwani L (2006) Deficiency of the zinc finger protein ZPR1 causes defects in transcription and cell cycle progression. J Biol Chem 281:40330–40340

    Article  PubMed  CAS  Google Scholar 

  • Gangwani L, Mikrut M, Galcheva-Gargova Z, Davis RJ (1998) Interaction of ZPR1 with translation elongation factor-1alpha in proliferating cells. J Cell Biol 143:1471–1484

    Article  PubMed  CAS  Google Scholar 

  • Gangwani L, Mikrut M, Theroux S, Sharma M, Davis RJ (2001) Spinal muscular atrophy disrupts the interaction of ZPR1 with the SMN protein. Nat Cell Biol 3:376–383

    Article  PubMed  CAS  Google Scholar 

  • Gangwani L, Flavell RA, Davis RJ (2005) ZPR1 is essential for survival and is required for localization of the survival motor neurons (SMN) protein to Cajal bodies. Mol Cell Biol 25:2744–2756

    Article  PubMed  CAS  Google Scholar 

  • Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355

    Article  PubMed  CAS  Google Scholar 

  • Martin B, Thorstenson YR (1988) Stable carbon isotope composition (deltaC), water use efficiency, and biomass productivity of lycopersicon esculentum, lycopersicon pennellii, and the F(1) hybrid. Plant Physiol 88:213–217

    Article  PubMed  CAS  Google Scholar 

  • Mishra AK, Gangwani L, Davis RJ, Lambright DG (2007) Structural insights into the interaction of the evolutionarily conserved ZPR1 domain tandem with eukaryotic EF1A, receptors, and SMN complexes. Proc Natl Acad Sci USA 104:13930–13935

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  PubMed  CAS  Google Scholar 

  • Nogusa Y, Yanaka N, Sumiyoshi N, Takeda K, Kato N (2006) Expression of zinc finger protein ZPR1 mRNA in brain is up-regulated in mice fed a high-fat diet. Int J Mol Med 17:491–496

    PubMed  CAS  Google Scholar 

  • Peng S, Zhu Z, Zhao K, Shi J, Yang Y, He M, Wang Y (2012) A novel heat shock transcription factor, VpHsf1, from Chinese wild Vitis pseudoreticulata is involved in biotic and abiotic stresses. Plant Mol Biol Rep: 1–8

  • Qu G-Z, Zang L, Xilin H, Gao C, Zheng T, Li K-L (2012) Co-transfer of LEA and bZip genes from Tamarix confers additive salt and osmotic stress tolerance in transgenic tobacco. Plant Mol Biol Rep 30:512–518

    Article  CAS  Google Scholar 

  • Ross EJ, Stone JM, Elowsky CG, Arredondo-Peter R, Klucas RV, Sarath G (2004) Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1. J Exp Bot 55:1721–1731

    Article  PubMed  CAS  Google Scholar 

  • Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270

    Article  PubMed  CAS  Google Scholar 

  • Sonnhammer EL, Koonin EV (2002) Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 18:619–620

    Article  PubMed  CAS  Google Scholar 

  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

    PubMed  CAS  Google Scholar 

  • Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  PubMed  CAS  Google Scholar 

  • Wu F, Mueller LA, Crouzillat D, Petiard V, Tanksley SD (2006) Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174:1407–1420

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Guo X, Lei C, Cheng Z, Lin Q, Wang J, Wu F, Wang J, Wan J (2011) Overexpression of SlCZFP1, a novel TFIIIA-type zinc finger protein from tomato, confers enhanced dold tolerance in transgenic Arabidopsis and rice. Plant Mol Biol Rep 29:185–196

    Article  Google Scholar 

  • Zhang Y, Feng F, He C (2012) Downregulation of OsPK1 contributes to oxidative stress and the variations in ABA/GA balance in rice. Plant Mol Biol Rep 30:1006–1013

    Article  CAS  Google Scholar 

  • Ziaf K, Loukehaich R, Gong P, Liu L, Han Q, Wang T, Li H, Ye Z (2011) A multiple stress responsive gene ERD15 from Solanum pennellii confers stress tolerance in tobacco. Plant Cell Physiol 52:1055–1067

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Khurram Ziaf for critical reviews of this manuscript. This work was supported by grants from Project 973 (NO. 2009CB119002), the National High Technology R&D Program of China (2012AA100104) and the National Natural Science Foundation of China (30871712).

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Correspondence to Hanxia Li.

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Supplementary Fig. S1

Full-length cDNA sequence of the SpZPR1 gene and the deduced amino acid sequence. (DOC 26 kb)

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Li, J., Sima, W., Ouyang, B. et al. Identification and Expression Pattern of a ZPR1 Gene in Wild Tomato (Solanum Pennellii). Plant Mol Biol Rep 31, 409–417 (2013). https://doi.org/10.1007/s11105-012-0509-4

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