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Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis

Abstract

MYB family of transcription factors (TF) comprises one of the largest transcription factors in plants and is represented in all eukaryotes. They include highly conserved MYB repeats (1R, R2R3, 3R, and 4R) in the N-terminus. In addition to this, they have diverse C-terminal sequences which help the protein gain wide distinct functions, such as controlling development, secondary metabolism, hormonal regulation and response to biotic and abiotic stress. Stress-responsive roles of the MYB TFs were reported for drought, salt, wounding, cold, freezing, dehydration and osmotic stresses. This study describes the identification of barley R2R3-MYB TFs including their expression analysis in tissues under control and Boron (B) toxic conditions. Conserved motifs for MYB proteins were searched into barley full-transcriptome RNA-seq data and a total of 320 protein sequences were filtered as MYB TFs in which 51 of them corresponded to R2R3 MYB TFs. Using various bioinformatics tools, their conserved domain structures, chromosomal distributions, gene duplications, comparative functional analysis, as well as phylogenetic relations with Arabidopsis thaliana, were conducted. Beside the RNA-seq data-based expression pattern analysis of 51 R2R3 MYB TFs, quantitative analysis of selected R2R3 MYB TF genes was assessed in control and B-stressed root and leaf tissues. Critical B-induced R2R3 MYB TFs were identified. It was concluded that the results would be useful for functional characterizations of R2R3-type MYB transcription factors that are possibly involved in both B stress and divergent regulation mechanisms in plants.

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Abbreviations

AMV:

Myeloblastosis virus

DBD:

DNA-binding domain

Gb:

Gigabase

IBSC:

International Barley Genome Sequencing Consortium

RPKM:

Reads per kilobase per million mapped reads

RT-qPCR:

Reverse transcriptase quantitative PCR

TAD:

Trans-acting domain

TF:

Transcription factors

References

  1. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  3. Apweiler R, Attwood TK, Bairoch A et al (2001) The interpro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 29:37–40

  4. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

  5. Bailey TL, Boden M, Buske FA, Frith M, Grant CE et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–208

  6. Camacho-Cristobal JJ, Rexach J, Gonzalez-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255

  7. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200

  8. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

  9. Dai X, Wang Y, Yang A, Zhang WH (2012) OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiol 159:169–183

  10. Ding Z, Li S, An X, Liu X, Qin H, Wang D (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 36:17–29

  11. Du H, Zhang L, Liu L, Tang XF, Yang WJ, Wu YM, Huang YB, Tang YX (2009) Biochemical and molecular characterization of plant MYB transcription factor family. Biochem 74:1–11

  12. Du H, Feng B, Yang S, Huang Y, Tang Y (2012a) The R2R3-MYB transcription factor gene family in maize. PLoS One 7(6):e37463

  13. Du H, Yang S, Liang Z, Feng B, Liu L, Huang Y, Tang Y (2012b) Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol 12:106

  14. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

  15. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116

  16. Ganesan G, Sankararamasubramanian HM, Harikrishnan M, Ashwin G, Parida A (2012) A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. J Exp Bot 63(12):4549–4561

  17. Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

  18. Hegvold AB, Gabrielsen OS (1996) The importance of the linker connecting the repeats of the c-Myb oncoprotein may be due to a positioning function. Nucleic Acids Res 24:3990–3995

  19. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

  20. Jia L, Clegg MT, Jiang T (2004) Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol 134:575–585

  21. Kanei-Ishii C, Sarai A, Sawazaki T, Nakagoshi H, He DN, Ogata K, Nishimura Y, Ishii S (1990) The tryptophan cluster: a hypothetic structure of the DNA-binding domain of the MYB protooncogene product. J Biol Chem 265:19990–19995

  22. Kasajima I, Ide Y, Yokota Hirai M, Fujiwara T (2010) WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plantarum 139:80–92

  23. Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V, Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13:544

  24. Kekec G, Tombuloglu H, Unver T, Sakcali MS (2013) Transcriptome profiling and analysis of boron tolerant barley (Hordeum vulgare L.) following toxic boron treatment. (Unpublished)

  25. Klempnauer K, Gonda T, Bishop J (1982) Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell 31:453–463

  26. Latchman DS (1997) Transcription factors: an overview. Int J Biochem Cell B 29:1305–1312

  27. Letunic I, Doerks T, Bork P (2012) SMART7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:302–305

  28. Lippold F, Sanchez DH, Musialak M, Schlereth A, Scheible WR, Hincha DK, Udvardi MK (2009) AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiol 149:1761–1772

  29. Lipsick JS (1996) One billion years of MYB. Oncogene 13:223–235

  30. Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grapeMYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83

  31. Mayer KF, Martis M, Hedley PE et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263

  32. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by rna-seq. Nat Methods 5:621–628

  33. Nozawa A, Miwa K, Kobayashi M, Fujiwara T (2006) Isolation of Arabidopsis thaliana cDNAs that confer yeast boric acid tolerance. Biosci Biotech Bioch 70:1724–1730

  34. Ochiai K, Shimizu A, Okumoto Y, Fujiwara T, Matoh T (2011) Suppression of a NAC-like transcription factor gene improves boron-toxicity tolerance in rice. Plant Physiol 156:1457–1463

  35. Ogata K, Kanei-Ishii C, Sasaki M, Hatanaka H (1996) The cavity in the hydrophobic core of Myb DNA-binding domain is reserved for DNA recognition and trans-activation. Nat Struct Biol 3:178–187

  36. Pabo CO, Sauer RT (1992) Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem 61:1053–1095

  37. Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6:3553–3558

  38. Raffaele S, Vailleau F, Leger A, Joubes J, Miersch O, Huard C, Blee E, Mongrand S, Domergue F, Roby D (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20:752–767

  39. Reid R (2007) Update on boron toxicity and tolerance in plants. In: Xu F, Goldbach HE, Brown PH, Bell RW, Fujiwara T, Hunt CD, Goldberg S, Shi L (eds) Advances in plant and animal boron nutrition. Springer, Dordrecht, pp 83–90

  40. Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

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

  42. Schreiber AW, Shi BJ, Huang CY, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics 12:129

  43. Schulte D, Close TJ, Graner A et al (2009) The International Barley Sequencing Consortium (IBSC) at the threshold of efficient access to the barley genome. Plant Physiol 149:142–147

  44. Shin D, Moon S, Han S et al (2011) Expression of StMYB1R-1, a novel potato single MYB-like domain transcription factor, increases drought tolerance. Plant Physiol 155:421–432

  45. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4(5):447–456

  46. Sutton T, Baumann U, Hayes J et al (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449

  47. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

  48. The International Barley Genome Sequencing Consortium (IBSC) (2012) A physical, genetical, and functional sequence assembly of the barley genome. Nature 491:711–717

  49. Tombuloglu H, Semizoglu N, Sakcali S, Kekec G (2012) Boron induced expression of some stress-related genes in tomato. Chemosphere 86:433–438

  50. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

  51. Williams CE, Grotewold E (1997) Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. J Biol Chem 272:563–571

  52. Yang A, Dai XY, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556

  53. Yanhui C, Xiaoyuan Y, Kun H, Meihua L et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

  54. Yau SK, Ryan J (2008) Boron toxicity tolerance in crops: a viable alternative to soil amelioration. Crop Sci 48:854–865

  55. Zhang H, Jin JP, Tang L, Zhao Y, Gu XC, Gao G, Luo JC (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117

  56. Zhang L, Zhao G, Jia J, Liu X, Kong X (2012) Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. J Exp Bot 63:203–214

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Acknowledgments

This study is supported by TUBITAK (Scientific and Technological Research Council of Turkey) (grant no.: 111T015) and the Scientific Research Fund of Fatih University under the project number of P50031105_G(1941). Also, we would like to thank Miss. Berçem Yeman for the manuscript proofreading.

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Correspondence to Huseyin Tombuloglu.

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Communicated by S. Hohmann.

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Tombuloglu, H., Kekec, G., Sakcali, M.S. et al. Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genomics 288, 141–155 (2013). https://doi.org/10.1007/s00438-013-0740-1

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Keywords

  • R2R3-MYB transcription factors
  • Transcriptome
  • Boron toxicity
  • Barley
  • Phylogenetics