Skip to main content
Log in

Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Characterization of genes responsive to stress is important for efforts on improving stress tolerance of plants. To address components involved in stress tolerance of tomato (Solanum lycopersicum), a stress-responsive gene family encoding A20/AN1 zinc finger proteins was characterized. In the present study, 13 members of this gene family were cloned from tomato cultivar Pusa Ruby and named as Stress Associated Protein (SAP) genes. Out of 13 genes, 12 have been mapped on their respective chromosomes. Expression of these genes in response to cold, heat, salt, desiccation, wounding, abscisic acid, oxidative and submergence stresses was analysed. All tomato SAP genes were found to be responsive to one or other type of environmental stress. The phylogenetic analysis of these genes, along with their orthologs from Solanaceae species suggests the presence of a common set of SAP genes in the studied Solanaceae species. The present study characterizes a SAP gene family, which encodes A20/AN1 zinc finger containing proteins from tomato for the first time. Genes showing high expression in response to a particular stress can be exploited for improving stress tolerance of tomato and other Solanaceae members.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ExoSAP:

Exonuclease and shrimp alkaline phosphatase

IL:

Introgression line

MS:

Murashige and Skoog

SAP:

Stress-associated protein

TC:

Tentative consensus

References

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cooper B, Clarke JD, Budworth P, Kreps J, Hutchison D, Park S, Guimil S, Dunn M, Luginbuhl P, Ellero C, Goff SA, Glazebrook J (2003) A network of rice genes associated with stress response and seed development. Proc Natl Acad Sci USA 100:4945–4950

    Article  PubMed  CAS  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  PubMed  CAS  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version I. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Dixit VM, Green S, Sarma V, Holzman LB, Wolf FW, O’Rourke K, Ward PA, Prochownik EV, Marks RM (1990) Tumor necrosis factor-alpha induction of novel gene products in human endothelial cells including a macrophage-specific chemotaxin. J Biol Chem 265:2973–2978

    PubMed  CAS  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103:8281–8286

    Article  PubMed  CAS  Google Scholar 

  • Duan W, Sun B, Li TW, Tan BJ, Lee MK, Teo TS (2000) Cloning and characterization of AWP1, a novel protein that associates with serine/threonine kinase PRK1 in vivo. Gene 256:113–121

    Article  PubMed  CAS  Google Scholar 

  • Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162

    PubMed  CAS  Google Scholar 

  • Evans PC, Ovaa H, Hamon M, Kilshaw PJ, Hamm S, Bauer S, Ploegh HL, Smith TS (2004) Zinc-finger protein A20, a regulator of inflammation and cell survival, has de-ubiquitinating activity. Biochem J 378:727–734

    Article  PubMed  CAS  Google Scholar 

  • Hishiya A, Iemura S, Natsume T, Takayama S, Ikeda K, Watanabe K (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J 25:554–564

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Teng L, Li L, Liu T, Chen D, Xu LG, Zhai Z, Shu HB (2004) ZNF216 is an A20-like and IkappaB kinase gamma-interacting inhibitor of NFkappaB activation. J Biol Chem 279:16847–16853

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Wang MM, Jiang Y, Bao YM, Huang X, Sun H, Xu DQ, Lan HX, Zhang HS (2008) Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. Gene 420:135–144

    Article  PubMed  CAS  Google Scholar 

  • Jin Y, Wang M, Fu J, Xuan N, Zhu Y, Lian Y, Jia Z, Zheng J, Wang G (2007) Phylogenetic and expression analysis of ZnF-AN1 genes in plants. Genomics 90:265–275

    Article  PubMed  CAS  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462

    Article  PubMed  CAS  Google Scholar 

  • Klinkenberg M, Van Huffel S, Heyninck K, Beyaert R (2001) Functional redundancy of the zinc fingers of A20 for inhibition of NF-kappaB activation and protein–protein interactions. FEBS Lett 498:93–97

    Article  PubMed  CAS  Google Scholar 

  • Li L, Hailey DW, Soetandyo N, Li W, Lippincott-Schwartz J, Shu HB, Ye Y (2008) Localization of A20 to a lysosome-associated compartment and its role in NFkappaB signaling. Biochim Biophys Acta 1783:1140–1149

    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 

  • Opipari AW Jr, Boguski MS, Dixit VM (1990) The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J Biol Chem 265:14705–14708

    PubMed  CAS  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Rebagliati MR, Weeks DL, Harvey RP, Melton DA (1985) Identification and cloning of localized maternal RNA from Xenopus eggs. Cell 42:769–777

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiol Mol Biol Plants 14:69–79

    Article  CAS  Google Scholar 

  • Ströher E, Wang X-J, Roloff N, Klein P, Husemann A, Dietz K-J (2009) Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Mol Plant 2:357–367

    Article  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  PubMed  CAS  Google Scholar 

  • Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Mol Genet Genomics 276:565–575

    Article  PubMed  CAS  Google Scholar 

  • Vij S, Tyagi AK (2007) Emerging trends in the functional genomics of the abiotic stress response in crop plants. Plant Biotechnol J 5:361–380

    Article  PubMed  CAS  Google Scholar 

  • Vij S, Tyagi AK (2008) A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response. Funct Integr Genomics 8:301–307

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Chen T, Han C, He D, Liu H, An H, Cai Z, Cao X (2007) Lysosome-associated small Rab GTPase Rab7b negatively regulates TLR4 signaling in macrophages by promoting lysosomal degradation of TLR4. Blood 110:962–971

    Article  PubMed  CAS  Google Scholar 

  • Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett 582:1037–1043

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Thomashow MF (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39:905–919

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by grants received from the Department of Biotechnology and Defence Research and Development Organization, Government of India. A.U.S. acknowledges CSIR for the fellowship granted during his tenure as a research fellow. We also thank Dr. Dani Zamir for providing resources related to tomato I.L. population and Dr. Shailendra Vyas for critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arun Kumar Sharma.

Additional information

Communicated by K. Shirasu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 89 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Solanke, A.U., Sharma, M.K., Tyagi, A.K. et al. Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Mol Genet Genomics 282, 153–164 (2009). https://doi.org/10.1007/s00438-009-0455-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-009-0455-5

Keywords

Navigation