Skip to main content

Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human

Plant Molecular Biology volume 73, pages 449–465 (2010)Cite this article

Abstract

Helicases are motor proteins which can catalyze the unwinding of stable RNA or DNA duplex utilizing mainly ATP as source of energy. In this study we have identified complete sets of helicases from rice and Arabidopsis. The helicase gene family in rice and Arabidopsis contains 115 and 113 genes respectively. These helicases were validated based on their annotations and supported with organization of conserved helicase signature motifs. We have also identified homologs of 64 rice RNA and DNA helicases in Arabidopsis, yeast and human. We explored Arabidopsis oligonucleotide array data to gain functional insights into the transcriptome of helicase family members under ten different stress conditions. Our results revealed that expression of helicase genes is profoundly regulated under various stress conditions. The helicases identified in this study lay a foundation for the in depth characterization of each helicase type.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    Article  CAS  PubMed  Google Scholar 

  • Aubourg S, Kreis M, Lecharny A (1999) The DEAD-box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res 27:628–636

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen J (2002) The rice genome. Opening the door to comparative plant biology. Science 296:60–63

    Article  PubMed  Google Scholar 

  • Bernstein DA, Zittel MC, Keck JL (2003) High-resolution structure of the E. coli RecQ helicase catalytic core. EMBO J 22:4910–4921

    Article  CAS  PubMed  Google Scholar 

  • Boudet N, Aubourg S, Toffano-Nioche C, Kreis M, Lecharny A (2001) Evolution of intron/exon structure of DEAD helicase family genes in Arabidopsis, Caenorhabditis, and Drosophila. Genome Res 11:2101–2114

    Article  CAS  PubMed  Google Scholar 

  • Brewster AS, Wang G, Yu X, Greenleaf WB, Carazo JM, Tjajadia M, Klein MG, Chen XS (2008) Crystal structure of a near-full-length archaeal MCM: functional insights for an AAA+ hexameric helicase. Proc Natl Acad Sci USA 105:20191–20196

    Article  CAS  PubMed  Google Scholar 

  • Cho WK, Geimer S, Meurer J (2009) Cluster analysis and comparison of various chloroplast transcriptomes and genes in Arabidopsis thaliana. DNA Res 16:31–44

    Article  CAS  PubMed  Google Scholar 

  • Cordin O, Banroques J, Tanner NK, Linder P (2006) The DEAD-box protein family of RNA helicases. Gene 367:17–37

    Article  CAS  PubMed  Google Scholar 

  • Dalmay T, Horsefield R, Braunstein TH, Baulcombe DC (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20:2069–2077

    Article  CAS  PubMed  Google Scholar 

  • de la Cruz J, Kressler D, Linder P (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24:192–198

    Article  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  CAS  PubMed  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut JS, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu JK (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci USA 99:11507–11512

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD-box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267

    Article  CAS  PubMed  Google Scholar 

  • Gorbalenya AE, Koonin EV (1993) Helicases: amino acid sequence comparisons and structure-function relationship. Curr Opin Struct Biol 3:419–429

    Article  CAS  Google Scholar 

  • Hartung F, Plchova H, Puchta H (2000) Molecular characterization of RecQ homologues in Arabidopsis thaliana. Nucleic Acids Res 28:4275–4282

    Article  CAS  PubMed  Google Scholar 

  • Holding DR, Springer PS (2002) The Arabidopsis gene PROLIFERA is required for proper cytokinesis during seed development. Planta 214:373–382

    Article  CAS  PubMed  Google Scholar 

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 420747

  • Jankowsky E, Fairman ME (2007) RNA helicases–one fold for many functions. Curr Opin Struct Biol 17:316–324

    Article  CAS  PubMed  Google Scholar 

  • Kant P, Kant S, Gordon M, Shaked R, Barak S (2007) STRS1 and STRS2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stress. Plant Physiol 145:814–830

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Kim KA, Oh TR, Park CM, Kang H (2008) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 49:1563–1571

    Article  CAS  PubMed  Google Scholar 

  • Kobbe D, Blanck S, Demand K, Focke M, Puchta H (2008) AtRECQ2, a RecQ helicase homologue from Arabidopsis thaliana, is able to disrupt various recombinogenic DNA structures in vitro. Plant J 55:397–405

    Article  CAS  PubMed  Google Scholar 

  • Kobbe D, Blanck S, Focke M, Puchta H (2009) Biochemical characterization of AtRECQ3 reveals significant differences relative to other RecQ helicases. Plant Physiol 151:1658–1666

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  Google Scholar 

  • Linder P (2006) Dead-box proteins: a family affair—active and passive players in RNP-remodeling. Nucleic Acids Res 34:4168–4180

    Article  CAS  PubMed  Google Scholar 

  • Linder P, Owttrim GW (2009) Plant RNA helicases: linking aberrant and silencing RNA. Trends Plant Sci 14:344–352

    Article  CAS  PubMed  Google Scholar 

  • Liu HH, Liu J, Fan SL, Song MZ, Han XL, Liu F, Shen FF (2008) Molecular cloning and characterization of a salinity stress-induced gene encoding DEAD-box helicase from the halophyte Apocynum venetum. J Exp Bot 59:633–644

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Richards TA, Aves SJ (2009) Ancient diversification of eukaryotic MCM DNA replication proteins. MBC Evol Biol 9:60

    Article  CAS  Google Scholar 

  • Lorsch JR (2002) RNA chaperones exist and DEAD-box proteins get a life. Cell 109:797–800

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperon-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43

    CAS  PubMed  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  CAS  PubMed  Google Scholar 

  • Owttrim GW (2006) RNA helicases and abiotic stress. Nucleic Acids Res 34:3220–3230

    Article  CAS  PubMed  Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  CAS  PubMed  Google Scholar 

  • Pause A, Methot N, Sonenberg N (1993) The HRIGRXXR region of the DEAD box RNA helicase eukaryotic translation initiation factor 4A is required for RNA binding and ATP hydrolysis. Mol Cell Biol 13:6789–6798

    CAS  PubMed  Google Scholar 

  • Pennacchio LA (2003) Insights from human/mouse genome comparisons. Mamm Genome 14:429–436

    Article  CAS  PubMed  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Pike ACW, Shrestha B, Popuri V, Burgess-Brown Muzzolini L, Costantini S, Vindigni A, Gileadi O (2009) Structure of the human RECQ1 helicase reveals a putative strand-separation pin. Proc Natl Acad Sci USA 106:1039–1044

    Article  CAS  PubMed  Google Scholar 

  • Poole RL (2007) The TAIR database. Methods Mol Biol 406:179–212

    Article  CAS  PubMed  Google Scholar 

  • Sabelli PA, Burgess SR, Kush AK, Young MR, Shewry PR (1996) cDNA cloning and characterization of a maize homologue of the MCM proteins required for the initiation of DNA replication. Mol Gen Genet 252:125–136

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sanan-Mishra N, Pham XH, Sopory SK, Tuteja N (2005) Pea DNA helicase 45 over expression in tobacco confers high salinity tolerance without affecting yield. Proc Natl Acad Sci USA 102:509–514

    Article  CAS  PubMed  Google Scholar 

  • Schmid SR, Linder P (1992) D-E-A-D protein family of putative RNA helicases. Mol Microbiol 6:283–291

    Article  CAS  PubMed  Google Scholar 

  • Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100

    Article  CAS  PubMed  Google Scholar 

  • Schuster-Böckler B, Schultz J, Rahmann S (2004) HMM Logos for visualization of protein families. BMC Bioinformatics 5:7

    Article  PubMed  Google Scholar 

  • Shultz RW, Lee T-J, Allen GC, Thompson WF, Hanley-Bowdoin L (2009) Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants. Plant Physiol 150:658–669

    Article  CAS  PubMed  Google Scholar 

  • Soukas A, Cohen P, Socci ND, Friedman JM (2000) Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev 15:963–980

    Google Scholar 

  • Springer PS, McCombie WR, Sundaresan V, Martienssen RA (1995) Gene trap tagging of PROLIFERA an essential MCM2–3-5-like gene in Arabidopsis. Science 268:877–880

    Article  CAS  PubMed  Google Scholar 

  • Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA (2000) The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127:1815–1822

    CAS  PubMed  Google Scholar 

  • Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208

    Article  CAS  PubMed  Google Scholar 

  • Tanner NK, Linder P (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8:251–262

    Article  CAS  PubMed  Google Scholar 

  • Tuteja N (2003) Plant DNA helicases, the long unwinding road. J Exp Bot 54:2201–2214

    Article  CAS  PubMed  Google Scholar 

  • Tuteja R (2010) Genome wide identification of Plasmodium falciparum helicases: a comparison with human host. Cell Cycle 9:104–120

    PubMed  Google Scholar 

  • Tuteja N, Tuteja R (2004a) Prokaryotic and eukaryotic DNA helicases. Essential molecular motor proteins for cellular machinery. Eur J Biochem 271:1835–1848

    Article  CAS  PubMed  Google Scholar 

  • Tuteja N, Tuteja R (2004b) Unravelling DNA helicases. Motif, structure, mechanism and function. Eur J Biochem 271:1849–1863

    Article  CAS  PubMed  Google Scholar 

  • Ursic D, Himmel KL, Gurley KA, Webb F, Culbertson MR (1997) The yeast SEN1 gene is required for the processing of diverse RNA classes. Nucleic Acids Res 25:4778–4785

    Article  CAS  PubMed  Google Scholar 

  • Vashisht AA, Tuteja N (2005) Cold stress-induced pea DNA helicase 47 is homologous to eIF4A and inhibited by DNA-interacting ligands. Arch Biochem Biophys 440:79–90

    Article  CAS  PubMed  Google Scholar 

  • Vashisht AA, Tuteja N (2006) Stress responsive DEAD-box helicases, a new pathway to engineer plant stress tolerance. J Photochem Photobiol B 84:150–160

    Article  CAS  PubMed  Google Scholar 

  • Vashisht AA, Pradhan A, Tuteja R, Tuteja N (2005) Cold and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J 44:76–87

    Article  CAS  PubMed  Google Scholar 

  • Vincentz M, Cara FA, Okura VK, da Silva FR, Pedrosa GL et al (2004) Evaluation of monocot and eudicot divergence using the sugarcane transcriptome. Plant Physiol 134:951–959

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H et al (2005) The genomes of Oryza sativa. A history of duplications. PLoS Biol 3:266–281

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Work on helicases and plant stress tolerance in N.T.’s laboratory is supported partially by the Department of Science and Technology (DST), Government of India and Department of Biotechnology (DBT), Government of India.

Author information

Affiliations

  1. Plant Molecular Biology Group, International Centre for Genetic Engineering and Biotechnology (ICGEB), Aruna Asaf Ali Marg, New Delhi, 110067, India

    Pavan Umate, Renu Tuteja & Narendra Tuteja

Authors
  1. Pavan Umate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Renu Tuteja
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Narendra Tuteja
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Narendra Tuteja.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 269 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Umate, P., Tuteja, R. & Tuteja, N. Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human. Plant Mol Biol 73, 449–465 (2010). https://doi.org/10.1007/s11103-010-9632-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9632-5

Keywords

  • Abiotic stress
  • DEAD-box proteins
  • Helicase motifs
  • Protein alignment
  • Sequence LOGO
  • Transcriptomics