Ukrainian Antarctic journal

No 15 (2016): Ukrainian Antarctic Journal
Articles

Bioinformatic prediction of genes of cold-induced transcription factors CBF/DREB1 and DREB4 in Deschampsia antarctica Desv.

О. M. Bublyk
Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv
I.O. Andreev
Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv
V. A. Kunakh
Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv
Published January 18, 2017
Keywords
  • abiotic stress,
  • antarctic plants,
  • in silico prediction,
  • tolerance,
  • transcription factors

Abstract

The work was aimed at the study of the mechanisms of stress-resistance in plants through the example of Antarctic hair grass (D. antarctica), in particular at the analysis of genes of transcription factors (TF) of CBF/DREB1 and DREB4 groups, responsible for the regulation of plant response to cold and other abiotic stresses. As a result of in silico analysis of the data of sequencing genomic DNA and mRNA of D. antarctica using identified genes from related species of grasses and some typical motives as reference sequences, 17 predicted genes of the studied groups were identified. Predicted genes DaCBF were described and classified by comparing with the sequences of previously described orthologous genes of other species, and the genes were named according to the nomenclature of CBF adopted for other grasses. The composition of gene clusters was analyzed along with their potential role in shaping the cold tolerance of the species. It was found that the sequences of the protein products of predicted genes contain conservative motives and DNA-binding domain AP2/ERF typical of these groups, and share significant homology with orthologous proteins of related species. Phylogenetic analysis showed that the structure of the group of predicted D. antarctica transcription factors is generally similar to that described for other cereals: small subgroups CBFI and CBFII are composed each of one TF, whereas larger groups CBFIII and CBFIV contain four and eight TF, respectively. DREB4 cluster consisted of three TF. Analysis of transcriptome sequences revealed the constitutive expression of TF of the groups CBFIIIc, CBF IV and DREB4. There were not found any specific distinctions in the size or composition of CBF/ DREB1 and DREB4 groups of predicted transcriptional factors, which could explain the increased cold-tolerance of D. antarctica.

References

  1. Bublyk O. M., Andreev I. O., Kunakh V. A. In silico identification and analysis of stress-inducible DREB2 transcription factors genes in Deschampsia antarctica Desv. // Factors in experimental evolution of organisms. - 2016. - Vol. 19. - pp. 202-208. (In Ukrainian)
  2. Alberdi M., Bravo L. A., Gutierrez A., Gidekel M., Corcuera L. J. Ecophysiology of Antarctic vascular plants // Physiol. Plant. - 2002. - Vol. 115. - P. 479-486.
  3. Badawi M., Danyluk J., Boucho B., Houde M., Sarhan F. The CDF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs // Mol. Genet. Genomics. - 2007. - Vol. 277. - P. 533-554.
  4. Benedict C., Skinner J. S., Meng R., Chang Y., Bhalerao R., Huner N. P., Finn C. E., Chen T. H., Hurry V. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. // Plant Cell Environ. - 2006. - Vol. 29. - P. 1259-1272.
  5. Bräutigam M., Lindlöf A., Zakhrabekova S., Gharti-Chhetri G., Olsson B., Olsson O. Generation and analysis of 9792 EST sequences from cold acclimated oat, Avena sativa // BMC Plant Biol. - 2005. - 5:18.
  6. Byun M. Y., Lee J., Cui L. H., Kang Y., Oh T. K., Park H., Lee H., Kim W. T. Constitutive expression of DaCBF7, an Antarctic vascular plant Deschampsia antarctica CBF homolog, resulted in improved cold tolerance in transgenic rice plants // Plant Sci. - 2015. - Vol. 236. - P. 61-74.
  7. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T. L. BLAST+: architecture and applications // BMC Bioinformatics. - 2009. - Vol. 10. - P. 421.
  8. Campoli Ch., Matus-Cadis M. A., Pozniak C. J., Cattivelli L., Fowler D. B., Comparative expression of Cbf genes in the Triticieae under different acclimation induction temperatures // Mol. Genet. Genomics. - 2009. - Vol. 282. - P. 141.-152.
  9. Champ K. L., Febres V. J., Moore G. A. The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance // Mol. Genet. Genomics. - 2009. - Vol. 282. - P. 529-541.
  10. Dhillon T., Stockinger E. J. Cbf14 copy number variation in the A, B, and D genomes of diploid and polyploid wheat // Theor. Appl. Genet. - 2013. - Vol. 126, № 11. - P. 2777-2789.
  11. Dubouzet J. G., Sakuma Y., Ito Y., Kasuga M., Dubouzet E. G., Miura S., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression // Plant J. - 2003. - Vol. 33. - P. 751-763.
  12. Eulgem T. Regulation of the Arabidopsis defence transcriptome // Trends Plant Sci. - 2005. - Vol. 10, № 2. - P. 71-78.
  13. Fowler D. B., Carles R. J. Growth, development, and cold tolerance of fall-acclimated cereal grains // Crop Sci. - 1979. - Vol. 19. - P. 915-922.
  14. Fowler S., Thomashow M. F. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition in addition to the CBF cold response pathway // Plant Cell. - 2002. - Vol. 14, № 8. - P. 1675-1690.
  15. Francia E., Rizza F., Cattivelli L., Stanca A. M., Galiba G., Toth B., Hayes P. M., Skinner J. S., Pecchioni N. Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) x ‘Tremois” (spring) barley map // Theor. Appl. Genet. - 2004. - Vol. 108. - P. 670-680.
  16. Gao M. J., Allard G., Byass L., Flanagan A. M., Singh J. Regulation and characterization of four CBF transcription factors from Brassica napus // Plant Molecular Biology. - 2002. - Vol. 49. - P. 459-471.
  17. Gasteiger E., Hoogland C., Gattiker A., Duvaud, S. Wilkins M. R., Appel R. D., Bairoch A. Protein identification and analysis tools on the ExPASy server / Ed. by Walker J. M. The proteomics protocols handbook. - Totowa, N. J.: Humana Press, 2005. - P. 571-607.
  18. Gilmour S. J., Zarka D. G., Stockinger E. J., Salazar M. P., Houghton J. M., Thomashow M. F. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression // Plant J. - 1998. - Vol. 16. - P. 433-442.
  19. Haake V., Cook D., Riechmann J. L., Pineda O., Thomashow M. F., Zhang J. Z. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis // Plant Physiol. - 2002. - Vol. 130. - P. 639-648.
  20. Hannah M. A., Wiese D., Freund S., Fiehn O., Heyer A. G., Hincha D. K., Natural genetic variation of freezing tolerance in Arabidopsis // Plant Physiology. - 2006. - Vol. 142. - P. 98-112.
  21. Hussain S. S., Kayani M. A., Amjad M., Transcription factors as tools to engineer enhanced drought stress tolerance in plants // Biotechnol. Progr. - 2011. - Vol. 27, № 2. - P. 297-306.
  22. Jaglo K. R., Kle V. S., Amundsen K. L., Zhang X., Haake V., Zhang J. Z., Deits T., Thomashow M. F. Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species // Plant Physiol. - 2001. - Vol. 127. - P. 910-917.
  23. Jaglo-Ottosen K. R., Gilmour S. J., Zarka D. G., Schabenberger O., Thomashow M. F. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance // Science. - 1998. - Vol. 280. - P. 104-106.
  24. Jia Y., Ding Y., Shi Y., Zhang X., Gong Zh., Yang Sh. The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis // New Phytologists. - 2016. - Vol. 212, № 2. - P. 345-353.
  25. Jiang F., Wang F., Wu Z., Li Y., Shi G., Hu J., Hou X. Components of the Arabidopsis CBF cold-response pathway are conserved in non-heading chinese cabbage // Plant Mol. Biol. Rep. - 2011. - Vol. 29. - P. 525-532.
  26. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress inducible transcription factor // Nat. Biotechnol. - 1999. - Vol. 17. - P. 287-291.
  27. Knox A. K., Dhillon T., Cheng H., Tondelli A., Pecchioni N., Stockinger E. J. CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals // Theor. Appl. Genet. - 2010. - P. 121, № 1. - P. 21-35.
  28. Knox A. K., Li Ch., Vágújfalvi A., Galiba G., Stockinger E. J., Dubcovsky J. Identification of candidate CBF genes for the frost tolerance locus Fr-Am2 in Triticum monococcum // Plant Mol. Biol. - 2008. - Vol. 67. - P. 257-270.
  29. Lata Ch., Prasad M., Role of DREBs in regulation of abiotic stress responses in plants // J. Exp. Bot. - 2011. - Vol. 62, №. 14. - P. 4731-4748.
  30. Lee J., Kang. Y., Shin S. C., Park H., Lee H. Combined analysis of the chloroplast genome and transcriptome of the Antarctic vascular plant Deschampsia antarctica Desv. // PLOS ONE. - 2014. - Vol. 9, № 3. - e92501.
  31. Lee J., Noh E. K., Choi H.-S., Shin S., Park H., Lee H. Transcriptome sequencing of the Antarctic vascular plant Deschampsia antarctica Desv. under abiotic stress // Planta. - 2013. - Vol. 237. - P. 823-836.
  32. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression, respectively, in Arabidopsis // Plant Cell. - 1998. - Vol. 10. - P. 1391-1406.
  33. Miller A. K., Galiba G., Dubcovsky J. A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am2 in Triticum monococcum // Mol. Genet. Genomics. - 2006. - Vol. 275. - P. 193-203.
  34. Mohseni S., Che H., Djilalli Z., Dumont E., Nankeu J., Danyluk J. Wheat CBF gene family: identification of polymorphisms in the CBF coding sequence // Genome . - 2012. - Vol. 55, № 12. - P. 865-881.
  35. Moore R. C., Purugganan M. D. The evolutionary dynamics of plant duplicate genes // Curr. Opin. Plant. Biol. - 2005. - Vol. 8. - P. 122-128.
  36. Nakano M., Suzuki K., Fujimura T., Shinshi H., Genome-wide analysis of the ERF gene family in Arabidopsis and rice // Plant Physiol. - 2006. - Vol. 140. - P. 411-432.
  37. Nakashima K., Yamaguchi-Shinozaki K. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants // Physiol. Plant. - 2006. Vol. 126. - P. 62-71.
  38. Navarro M., Marque G., Ayax C., Keller G., Borges J. P., Marque C., Teulières C. Complementary regulatory of four Eucalyptus CBF genes under various cold conditions // J Exp. Bot. - 2009. - Vol. 60, № 9. - P. 2713-2724.
  39. Nicholas K. B., Nicholas H. B. J., Deerfield D. W. GeneDoc: analysis and visualization of genetic variation // EMBNEW News. - 1997. - Vol. 4. - P. 14.
  40. Novillo F., Alonso J. M., Ecker J. R., Salinas J. CBF2/DREB1C is a negative regulator of CBF1/DREB1A expression and plays a central role in stress tolerance in Arabidopsis // Proc. Natl. Acad. Sci. USA. - 2004. - Vol. 101. - P. 3985-3990.
  41. Novillo F., Medina J., Salinas J., Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon // Proc. Natl. Acad. Sci. USA. - 2007. - Vol. 104. - P. 21002-21007.
  42. Okonechnikov K., Golosova O., Fursov M., the UGENE team. Unipro UGENE: a unified bioinformatics toolkit // Bioinformatics. - 2012. - Vol. 28. - P. 1166-1167.
  43. Park S., Lee Ch.-M., Doherty C. J., Gilmour S. J., Kimand Y. S., Thomashow M. F. Regulation of Arabidopsis CBF regulon by a complex low-temperature regulatory network // Plant J. - 2015. - Vol. 82. - P. 193-207.
  44. Parnikoza I., Kozeretska I., Kunakh V. Vascular plants of the Maritime Antarctic: Origin and adaptation // Am. J. Plant Sci. - 2011. - Vol. 2, № 3. - P. 381-395.
  45. Pennycooke J. C., Cheng H., Roberts S. M., Yang Q., Rhee S. Y., Stockinger E. J. The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements // Plant Mol. Biol. - 2008. - Vol. 67. - P. 483-497.
  46. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees // Mol. Biol. Evol. - 1987. - Vol. 4, № 4. - P. 406-425.
  47. Sakuma Y., Liu Q., Dubouzet J. G., Abe H., Shinozaki K., Yamaguchi-Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression // Biochem. Biophys. Res. Commun. - 2002. - Vol. 290, № 3. - P. 998-1009.
  48. Semple C., Wolfe K. H., Gene duplication and gene conversion in the Caenorhabditis elegans genome //J Mol Evol. - 1999. - Vol. 48. - P. 555-564.
  49. Sharoni A. M., Nuruzzaman M., Satoh K., Shimizu T., Kondoh H., Sasaya T., Choi I. R., Omura T., Kikuchi S. Gene Structures, classification and expression models of the AP2/EREBP transcription factor family in rice // Plant Cell Physiol. - 2011. - Vol. 52, № 2. - P. 344-360.
  50. Skinner J. S., von Zitzewitz J., Szucs P., Marquez-Cedillo L., Filichkin T., Amundsen K., Stockinger E. J., Thomashow M. F., Chen T. H., Hayes P. M. Structural, functional, and phylogenetic characterization of a large CBF gene family in barley // Plant Mol. Biol. - 2005. - Vol. 59. - P. 533-551.
  51. Stockinger E. J., Gilmour S. J., Thomashow M. F. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit // Proc. Natl. Acad. Sci. USA. - 1997. - Vol. 94. - P. 1035-1040.
  52. Sun S., Yu. J. P., Chen F., Zhao T. J., Fang X. H., Li Y. Q., Sui S. F. TINY, a dehydration responsive element (DRE)-binding protein-like transcription factor connecting the DRE and ethylene-responsive element-mediated signaling pathways in Arabidopsis // J. Biol Chem. - 2008. - Vol. 283, № 10. - P. 6261-6271.
  53. Tamura K., Yamada T. A perennial ryegrass CBF gene cluster is located in a region predicted by conserved synteny between Poaceae species // Theor. Appl. Genet. - 2007. - Vol. 114, № 2. - P. 273-283.
  54. Tang H., Bowers J. E., Wang X., Ming R., Alam M., Paterson A. H. Synteny and collinearity in plant genomes // Science. - 2008. - Vol. 320. - P. 486-488.
  55. Thomashow M. F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms // Annu. Rev. Plant Physiol. Plant. Mol. Biol. - 1999. - Vol. 50. - P. 571-599.
  56. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice // Nucleic Acids Res. - 1994. - Vol. 22. - P. 4673-4680.
  57. Tian X.-H., Li X.-P., Zhou H.-L., Zhang J.-S., Gong Zh.-Zh., Chen Sh.-Y. OsDREB4 genes in rice encode AP2-containing proteins that bind specifically to the dehydration-responsive element // J. Integr. Plant Biol. - 2005. - Vol. 47, № 4. - P. 467-476.
  58. Todorovska E. G., Kolev S., Christov N. K., Balint A., Kocsy G., Vágújfalvi A., Galiba G. The expression of CBF genes at Fr-2 locus is associated with the level of frost tolerance in Bulgarian winter wheat cultivars // Biotechnol. Biotechnol. Equip. - 2014. - Vol. 28, № 3. - P. 392-401.
  59. Tondelli A., Francia E., Barabaschi D., Pasquariello M., Pecchioni N. Inside the CBF locus in Poaceae // Plant Sci. - 2011. - Vol. 180. - P. 39-45.
  60. Vogel J. T., Zarka D. G., Van Buskirk H. A.., Fowler S. G., Thomashow M. F. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis // Plant J. - 2005. - Vol. 41. - P. 195-211.
  61. Wang Q., Guan Y., Wu Y., Chen H., Chen F., Chu C. Over-expression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice // Plant Mol. Biol. - 2008. - Vol. 67. - P. 589-602.
  62. Wang Q. J.., Xu K. Y., Tong Z. G., Wang S. H., Gao Z. H., Zhang J. Y., Zong Ch.-W., Qiao Y.-Sh., Zhang Zh. Characterization of a new dehydration responsive element binding factor in central arctic cowberry // Plant Cell Tiss. Organ Cult. - 2010. - Vol. 101. - P. 211-219.
  63. Wei G., Pan Y., Lei J., Zhu Y.-X. Molecular cloning, phylogenetic analysis, expressional profiling and in vitro studies of TINY2 from Arabidopsis thaliana // J. Biochem. Mol. Biol. 2005. - Vol. 38. - P. 440-446.
  64. Xiao H., Tattersall E. A., Siddiqua M. K., Cramer G. R., Nassuth A. CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia // Plant Cell Environ. - 2008. - Vol. 31. - P. 1-10.
  65. Xiao H., Siddiqua M., Braybook S., Nassuth A. Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid // Plant Cell Environ. - 2006. - Vol. 29, № 7. - P. 1410-1421.
  66. Xue G.-P. Characterization of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the analysis of the DNA binding activity // Nucleic Acids Res. - 2002. - Vol. 30, № 15. - P. 77.
  67. Xue G.-P. The DNA-binding activity of an AP2 transcriptional actvator HvCBF2 involved in regulation of low temperature responsive genes in barley is modulated by temperature // Plant J. - 2003. - Vol. 33, № 2. - P. 373-383.
  68. Yamaguchi-Shinozaki K., Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses // Annu. Rev. Plant Biol. - 2006. - Vol. 57. - P. 781-803.
  69. Yang W., Liu X. D., Chi X. J., Wu C. A., Li Y. Z., Song L. L., Liu X. M., Wang Y. F., Wang F. W., Zhang C., Liu Y., Zong J. M., Li H. Y. Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways // Planta. - 2011. - Vol. 233. - P. 219-229.
  70. Zhang X., Fowler S. G., Cheng H., Lou Y., Rhee S. Y., Stockinger E. J., Thomashow M. F. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis // Plant J. - 2004. - Vol. 39. - P. 905-919.
  71. Zhao C., Zhang Z., Xie S., Si T., Li Y., Zhu J.-K. Mutational evidence for the critical role of CBF genes in cold acclimation in Arabidopsis // Plant Physiol. - 2016. - Vol. 171. - P. 2744-2759.