COMMON BEAN (Phaseolus vulgaris L.) DOF TRANSCRIPTION FACTORS DIFFERENTIALLY EXPRESSED UNDER SALT STRESS

Abstract

DNA-binding with one finger (DOF) transcription factor family has found to be playing important roles for seed germination, photosynthesis, plant development and stress responses in several plant species. Hence, this study aimed to characterize the DOF genes in common bean at the genome-scale level. The various bioinformatics tools were used and the results were confirmed through bench-work studies. Expression levels of putative PvDOF genes were analyzed using publicly available RNA-seq data and the expression levels of five selected PvDOF genes were further analyzed through qPCR in tolerant cv. ‘Yakutiye’ and sensitive cv. ‘Zulbiye’ subjected to salt stress. As a result, 42 candidate PvDOF genes were defined. The length of PvDOF proteins ranged from 181 (PvDOF-41) to 503 (PvDOF-35) amino acids (aa). pIs of PvDOF proteins were between 5.03 (PvDOF-21) and 8.92 (PvDOF-6) ranging from acidic to alkaline, and the molecular weight of PvDOFs were between 21944.3 Da (PvDOF-14) and 54786.5 Da (PvDOF-35). While the highest number of PvDOFs was found on chromosome 2 (eight genes), the lowest number of PvDOF genes was identified on chromosomes 4 and 7 (one gene). Two segmentally duplicated gene couple were detected. A total of 21 PvDOF genes were targeted by miRNAs of 20 plant species. According to the normalized RPKM (Read Per Kilobase Million) values which were obtained from the RNAseq analysis, PvDOF-6, 8, 9, 17, 27, 28, 30, 35 and 39 genes were found up- or down-regulated after salt stress treatment in the leaf and root tissues of common bean. Additionally, the most of the qPCR data were found to be consistent with the RNAseq data and the PvDOF17 gene was found as being the most expressional divergent gene between cv. ‘Zulbiye and cv. ‘Yakutiye’. In conclusion, the results of this study might help understanding the biological roles of PvDOF TF family under salt stress and can be used for the improving of common bean through biotechnological approaches.

Keywords

• Bioinformatics,DOF,RNAseq,qPCR,Phaseolus vulgaris,salinity

References

1. W.J. Broughton, G. Hernández, M. Blair, S. Beebe, P. Gepts, J. Vanderleyden, Beans (Phaseolus spp.) - model food legumes, Plant and Soil, 252(1), (2003) 55-128.
2. P.N. Miklas, J.D. Kelly, S.E. Beebe, M.W. Blair, Common bean breeding for resistance against biotic and abiotic stresses: From classical to MAS breeding, Euphytica, 147(1-2), (2006) 105-131.
3. W. Liu, C.N. Stewart Jr, Plant synthetic promoters and transcription factors (vol 37, pg 36, 2016), Current Opinion in Biotechnology, 38, (2016) 203-203.
4. I. Buyuk, B. Inal, E. Ilhan, M. Tanriseven, S. Aras, M. Erayman, Genome-wide identification of salinity responsive HSP70s in common bean, Molecular Biology Reports, 43(11), (2016) 1251-1266.
5. I. Buyuk, S. Aras, Genome-wide in silico identification, characterization and transcriptional analysis of the family of growth-regulating factors in common bean (Phaseolus vulgaris L.) subjected to polyethylene glycol-induced drought stress, Archives of Biological Sciences, 69(1), (2017) 5-14.
6. B. Inal, I. Buyuk, E. Ilhan, S. Aras, Genome-wide analysis of Phaseolus vulgaris C2C2-YABBY transcription factors under salt stress conditions, 3Biotech, 7, (2017) 302.
7. E. Ilhan, I. Buyuk, B. Inal, Transcriptome–Scale characterization of salt responsive bean TCP transcription factors, Gene, 642, (2018) 64-73.
8. S. Yanagisawa, Dof domain proteins: Plant-specific transcription factors associated with diverse phenomena unique to plants, Plant and Cell Physiology, 45(4), (2004) 386-391.

9. S. Yanagisawa, The Dof family of plant transcription factors. Trends in Plant Science, 7(12), (2002) 555-560.
10. J. Ma, M-Y. Li, F. Wang, J. Tang and A-S. Xiong, Genome-wide analysis of Dof family transcription factors and their responses to abiotic stresses in Chinese cabbage, BMC Genomics, 16(1), (2015) 1.
11. K. Shinozaki, K. Yamaguchi-Shinozaki, M. Seki, Regulatory network of gene expression in the drought and cold stress responses, Current opinion in plant biology, 6(5), (2003) 410-417.
12. K. Nakashima, Y. Ito, K. Yamaguchi-Shinozaki, Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses, Plant physiology, 149(1), (2009) 88-95.
13. D.M. Goodstein, S. Shu, R. Howson, R. Neupane, R.D. Hayes, J. Fazo, T. Mitros, W. Dirks, U. Hellsten, N. Putnam, D.S. Rokhsar, Phytozome: a comparative platform for green plant genomics, Nucleic Acids Research, 40(D1), (2012) D1178-D1186.
14. A.Y. Guo, Q.H. Zhu, X. Chen, J.C. Luo, [GSDS: a gene structure display server], Yi Chuan, 29(8), (2007) 1023-1026.
15. R.E. Voorrips, MapChart: software for the graphical presentation of linkage maps and QTLs, J Hered, 93(1), (2002) 77-78.
16. Z. Yang, S. Gu, X. Wang, W. Li, Z. Tang, C. Xu, Molecular evolution of the CPP-like gene family in plants: Insights from comparative genomics of Arabidopsis and rice, Journal of Molecular Evolution, 67(3), (2008) 266-277.
17. T.L. Bailey, N. Williams, C. Misleh, W.W. Li, MEME: discovering and analyzing DNA and protein sequence motifs, Nucleic Acids Res, 34 (Web Server issue), (2006) W369-373.
18. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar, MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods, Molecular Biology and Evolution, 28(10), (2011) 2731-2739
19. I. Letunic, P. Bork, Interactive Tree of Life v2: online annotation and display of phylogenetic trees made easy, Nucleic Acids Research, 39, (2011) W475-W478
20. P. Horton, K.J. Park, T. Obayashi, N. Fujita, H. Harada, C.J. Adams-Collier, K. Nakai, WoLF PSORT: protein localization predictor. Nucleic Acids Res, 35 (Web Server issue), (2007) W585-587.
21. O. Emanuelsson, S. Brunak, G. von Heijne, H. Nielsen, Locating proteins in the cell using TargetP, SignalP and related tools, Nature Protocols, 2(4), (2007) 953-971.
22. Y.J. Zhang, miRU: an automated plant miRNA target prediction server, Nucleic Acids Research, 33, (2005) W701-W704.
23. M. Suyama, D. Torrents, P. Bork, PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments, Nucleic Acids Res, 34 (Web Server issue), (2006) W609-612.
24. M. Lynch, J.S. Conery, The evolutionary demography of duplicate genes, J Struct Funct Genomics, 3(1-4), (2003) 35-44.
25. Z. Yang, R. Nielsen, Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol, 17(1), (2000) 32-43.
26. M.C. Hiz, B. Canher, H. Niron, M. Turet, Transcriptome Analysis of Salt Tolerant Common Bean (Phaseolus vulgaris L.) under Saline Conditions, Plos One, 9(3), (2014) e9259810.
27. G. Caraux, S. Pinloche, PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order Bioinformatics, 21(7), (2005) 1280-1281.
28. N.S. Guler, A. Saglam, M. Demiralay, A. Kadioglu, Apoplastic and symplastic solute concentrations contribute to osmotic adjustment in bean genotypes during drought stress, Turkish Journal of Biology, 36(2), (2012) 151-160.
29. T. Barac, S. Taghavi, B. Borremans, A. Provoost, L. Oeyen, J.V. Colpaert, J. Vangronsveld, D. van der Lelie, Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants, Nature biotechnology, 22(5), (2004) 583-588.
30. K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method, Methods, 25(4), (2001) 402-408.
31. Y. Guo, L.J. Qiu, Genome-wide analysis of the Dof transcription factor gene family reveals soybean-specific duplicable and functional characteristics, PLoS One, 8(9), (2013) e76809.
32. N.I. Park, P.A. Tuan, H. Xu, S.U. Park, Isolation and characterization of the PgDOF transcription factor in Platycodon grandiflorum, Plant Omics, 4(3) (2011) 149-153.
33. W. Huang, Y. Huang, M.Y. Li, F. Wang, Z.S. Xu, A.S. Xiong, Dof transcription factors in carrot: genome-wide analysis and their response to abiotic stress, Biotechnol Lett, 38(1), (2016) 145-155.
34. Y.J. Shu, L.L. Song, J. Zhang, Y. Liu, C.H. Guo, Genome-wide identification and characterization of the Dof gene family in Medicago truncatula, Genetics and Molecular Research, 14(3), (2015) 10645-10657
35. X. Yang, G.A. Tuskan, M.Z. Cheng, Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication, Plant Physiol, 142(3), (2006) 820-830.
36. N. Malviya, S. Gupta, V.K. Singh, M.K. Yadav, N.C. Bisht, B.K. Sarangi, D. Yadav, Genome wide in silico characterization of Dof gene families of pigeonpea (Cajanus cajan (L) Millsp.), Mol Biol Rep, 42(2), (2015) 535-552.
37. J.L. Riechmann, J. Heard, G. Martin, L. Reuber, C.Z. Jiang, J. Keddie, L. Adam, O. Pineda, O.J. Ratcliffe, R.R. Samaha, R. Creelman, M. Pilgrim, P. Broun, J.Z. Zhang, D. Ghandehari, B.K. Sherman, C.L. Yu, Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes, Science, 290(5499), (2000) 2105-2110
38. C.L. Wen, Q. Cheng, L. Zhao, A. Mao, J. Yang, S. Yu, Y. Weng, Y. Xu, Identification and characterisation of Dof transcription factors in the cucumber genome, Scientific Reports, 6, (2016) 23072.
39. J. Venkatesh, S.W. Park, Genome-wide analysis and expression profiling of DNA-binding with one zinc finger (Dof) transcription factor family in potato, Plant Physiol Biochem, 94, (2015):73-85.
40. X. Cai, Y. Zhang, C. Zhang, T. Zhang, T. Hu, J. Ye, J. Zhang, T. Wang, H. Li, Z. Ye, Genome-wide analysis of plant-specific Dof transcription factor family in tomato, J Integr Plant Biol, 55(6), (2013) 552-566.
41. Z. Wu, J. Cheng, J. Cui, X. Xu, G. Liang, X. Luo, X. Chen, X. Tang, K. Hu, C. Qin, Genome-Wide Identification and Expression Profile of Dof Transcription Factor Gene Family in Pepper (Capsicum annuum L.), Front Plant Sci, 7, (2016):574.
42. D. Lijavetzky, P. Carbonero, J. Vicente-Carbajosa, Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol, 3, (2003) 17.
43. L.E. Flagel, J.F. Wendel, Gene duplication and evolutionary novelty in plants, New Phytol, 183(3), (2009) 557-564.
44. S. Gupta, N. Malviya, H. Kushwaha, J. Nasim, N.C. Bisht, V.K. Singh, D. Yadav, Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor, Planta, 241(3), (2015) 549-562.
45. H. Kushwaha, S. Gupta, V.K. Singh, S. Rastogi, D. Yadav, Genome wide identification of Dof transcription factor gene family in sorghum and its comparative phylogenetic analysis with rice and Arabidopsis, Mol Biol Rep, 38(8), (2011) 5037-5053.
46. M. Martinez, I. Rubio-Somoza, R. Fuentes, P. Lara, P. Carbonero, I. Diaz, The barley cystatin gene (Icy) is regulated by DOF transcription factors in aleurone cells upon germination, Journal of Experimental Botany, 56(412), (2005) 547-556.
47. A. Song, T. Gao, P. Li, S. Chen, Z. Guan, D. Wu, J. Xin, Q. Fan, K. Zhao, F. Chen, Transcriptome-wide identification and expression profiling of the DOF transcription factor gene family in Chrysanthemum morifolium. Frontiers in plant science, 7, (2016).
48. G. Liang, D. Yu, Reciprocal regulation among miR395, APS and SULTR2;1 in Arabidopsis thaliana, Plant Signal Behav, 5(10), (2010) 1257-1259.
49. H.H. Liu, X. Tian, Y.J. Li, C.A. Wu, C.C. Zheng, Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana, Rna-a Publication of the Rna Society, 14(5), (2008) 836-843.
50. L. Zhou, Y. Liu, Z. Liu, D. Kong, M. Duan, L. Luo, Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa, J Exp Bot, 61(15), (2010) 4157-4168.
51. H. Eren, M. Pekmezci, S. Okay, M. Turktas, B. Inal, E. Ilhan, M. Atak, M. Erayman, T. Unver, Hexaploid wheat (Triticum aestivum) root miRNome analysis in response to salt stress, Annals of Applied Biology, 167(2), (2015) 208-216.
52. M. Etehadnia, D.R. Waterer, K.K. Tanino, The method of ABA application affects salt stress responses in resistant and sensitive potato lines, Journal of plant growth regulation, 27(4), (2008) 331-341.