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Licensed Unlicensed Requires Authentication Published by De Gruyter March 25, 2015

Identification of drought-induced transcription factors in Sorghum bicolor using GO term semantic similarity

  • Manoj Kumar Sekhwal , Ajit Kumar Swami , Vinay Sharma EMAIL logo and Renu Sarin

Abstract

Stress tolerance in plants is a coordinated action of multiple stress response genes that also cross talk with other components of the stress signal transduction pathways. The expression and regulation of stress-induced genes are largely regulated by specific transcription factors, families of which have been reported in several plant species, such as Arabidopsis, rice and Populus. In sorghum, the majority of such factors remain unexplored. We used 2DE refined with MALDI-TOF techniques to analyze drought stress-induced proteins in sorghum. A total of 176 transcription factors from the MYB, AUX_ARF, bZIP, AP2 and WRKY families of drought-induced proteins were identified. We developed a method based on semantic similarity of gene ontology terms (GO terms) to identify the transcription factors. A threshold value (≥ 90%) was applied to retrieve total 1,493 transcription factors with high semantic similarity from selected plant species. It could be concluded that the identified transcription factors regulate their target proteins with endogenous signals and environmental cues, such as light, temperature and drought stress. The regulatory network and cis-acting elements of the identified transcription factors in distinct families are involved in responsiveness to auxin, abscisic acid, defense, stress and light. These responses may be highly important in the modulation of plant growth and development.

References

1. Tuteja, N. Abscisic acid and abiotic stress signaling. Plant Signal Behav. 2 (2007) 135-138.Search in Google Scholar

2. Assefa, Y. and Staggenborg, S.A. Grain sorghum yield with hybrid advancement and change in agronomic practices from 1957 through 2008. Agron. J. 102 (2010) 703-706.Search in Google Scholar

3. Nakashima, K., Ito, Y. and Yamaguchi-Shinozaki, K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 49 (2009) 88-95.Search in Google Scholar

4. Hu, H., You, J., Fang, Y., Zhu, X., Qi, Z. and Xiong, L. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 67 (2008) 169-181.Search in Google Scholar

5. Ptashne, M. How eukaryotic transcriptional activators work. Nature 335 (1988) 683-689.Search in Google Scholar

6. Zhang, J.Z. Over-expression analysis of plant transcription factors. Curr. Opin. Plant Biol. 6 (2003) 1-11.Search in Google Scholar

7. Chen, L., Song, Y., Li, S., Zhang, L., Zou, C. and Yu, D. The role of WRKY transcription factors in plant abiotic stresses. Biochim. Biophys. Acta 1819 (2012) 120-128.Search in Google Scholar

8. Lee, C. and Huang, C.H. LASAGNA: a novel algorithm for transcription factor binding site alignment. BMC Bioinformatics 14 (2013) 108-120.Search in Google Scholar

9. Akhtar, M., Jaiswal, A., Taj, G., Jaiswal, J.P., Qureshi, M.I. and Singh, N.K. DREB1 /CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J. Genet. 91 (2012) 385-395.Search in Google Scholar

10. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K. and Shinozaki, K. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Biotechnol. 17 (2006) 113-122.Search in Google Scholar

11. He, K., Guo, A.Y., Gao, G., Zhu, Q.H., Liu, X.C., Zhang, H., Chen, X., Gu, X. and Luo, J. Computational identification of plant transcription factors and the construction of the PlantTFDB database. Methods Mol. Biol. 674 (2010) 351-368.Search in Google Scholar

12. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. Cluster analysis and display of genome-wide expression patterns. P. Natl. Acad. Sci. USA 96 (1999) 10943-10943.Search in Google Scholar

13. Tavazoie, S., Hughes, J.D., Campbell, M.J., Cho, R.J. and Church, G.M. Systematic determination of genetic network architecture. Nat. Genet. 22 (1999) 281-285.Search in Google Scholar

14. Cramer, G.R., Urano, K., Delrot, S., Pezzotti, M. and Shinozaki, K. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 11 (2011) 163-177.10.1186/1471-2229-11-163Search in Google Scholar PubMed PubMed Central

15. Todaka, D., Nakashima, K., Shinozaki, K. and Yamaguchi-Shinozaki, K. Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5 (2012) 6-15.Search in Google Scholar

16. Dugas, D.V., Monaco, M.K., Olsen, A., Klein, R.R., Kumari, S., Ware, D. and Klein, P.E. Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genomics 12 (2011) 514-534.Search in Google Scholar

17. Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A.K., Chapman, J., Feltus, F.A., Gowik, U., Grigoriev, I.V., Lyons, E., Maher, C.A., Martis, M., Narechania, A., Otillar, R.P., Penning, B.W., Salamov, A.A., Wang, Y., Zhang, L., Carpita, N.C., Freeling, M., Gingle, A.R., Hash, C.T., Keller, B., Klein, P., Kresovich, S., McCann, M.C., Ming, R., Peterson, D.G., Mehboob-ur-Rahman, Ware, D., Westhoff, P., Mayer, K.F., Messing, J. and Rokhsar, D.S. The Sorghum bicolor genome and the diversification of grasses. Nature 457 (2009) 551-556.Search in Google Scholar

18. Hirayama, T. and Shinozaki, K. Research on plant abiotic stress responses in the post genome era: past, present and future. Plant J. 61 (2010) 1041-1052.Search in Google Scholar

19. Juncker, A.S., Jensen, L.J., Pierleoni, A., Bernsel, A., Tress, M.L., Bork, P., von Heijne, G., Valencia, A., Ouzounis, C.A., Casadio, R. and Brunak, S. Sequence-based feature prediction and annotation of proteins. Genome Biol. 10 (2009) 206-211.Search in Google Scholar

20. Cokus, S., Mizutani, S. and Pellegrini, M. An improved method for identifying functionally linked proteins using phylogenetic profiles. BMC Bioinformatics 8 (2007) S7-S18.10.1186/1471-2105-8-S4-S7Search in Google Scholar PubMed PubMed Central

21. Turanalp, M.E. and Can, T. Discovering functional interaction patterns in protein-protein interaction networks. BMC Bioinformatics 9 (2008) 276-293.Search in Google Scholar

22. Ulitsky, I. and Shamir, R. Identifying functional modules using expression profiles and confidence scored protein interactions. Bioinformatics 25 (2009) 1158-1164.Search in Google Scholar

23. Lee, D., Redfern, O. and Orengo, C. Predicting protein function from sequence and structure. Nat. Rev. Mol. Cell Biol. 8 (2007) 995-1005.Search in Google Scholar

24. Gomez, A., Cedano, J., Amela, I., Planas, P., Pinol, J. and Querol, E. Gene ontology function prediction in mollicutes using protein-protein association networks. BMC Syst. Biol. 5 (2011) 49-59.Search in Google Scholar

25. Harris, M.A., Clark, J., Ireland, A., Lomax, J., Ashburner, M., Foulger, R., Eilbeck, K., Lewis, S., Marshall, B., Mungall, C., Richter, J., Rubin, G.M., Blake, J.A., Bult, C., Dolan, M., Drabkin, H., Eppig, J.T., Hill, D.P., Ni, L., Ringwald, M., Balakrishnan, R., Cherry, J.M., Christie, K.R., Costanzo, M.C., Dwight, S.S., Engel, S., Fisk, D.G., Hirschman, J.E., Hong, E.L., Nash, R.S., Sethuraman, A., Theesfeld, C.L., Botstein, D., Dolinski, K., Feierbach, B., Berardini, T., Mundodi, S., Rhee, S.Y., Apweiler, R., Barrell, D., Camon, E., Dimmer, E., Lee, V., Chisholm, R., Gaudet, P., Kibbe, W., Kishore, R., Schwarz, E.M., Sternberg, P., Gwinn, M., Hannick, L., Wortman, J., Berriman, M., Wood, V., de la Cruz, N., Tonellato, P., Jaiswal, P., Seigfried, T., White, R. and Gene Ontology Consortium. The gene ontology (GO) database and informatics resource. Nucleic Acids Res. 32 (2004) D258-D261.Search in Google Scholar

26. Resnik, P. similarity in a taxonomy: an information based measure and its application to problems of ambiguity in natural language. J. Artif. Intell. Res. 11 (1999) 95-130.Search in Google Scholar

27. Wang, J.Z., Du, Z., Payattakool, R., Yu, P.S. and Chen, C.F. A new method to measure the semantic similarity of GO terms. Bioinformatics 23 (2007) 1274-1281.Search in Google Scholar

28. Li, M., Wu, X., Pan, Y. and Wang, J. hF-measure: A new measurement for evaluating clusters in protein-protein interaction networks. Proteomics 13 (2013) 291-300.Search in Google Scholar

29. Sharma, V., Sekhwal, M.K., Swami, A.K. and Sarin, R. Identification of drought responsive proteins using gene ontology hierarchy. Bioinformation 8 (2012) 595-599.Search in Google Scholar

30. Sekhwal, M.K., Sharma, V. and Sarin, R. Identification of MFS proteins in sorghum using semantic similarity. Theory Biosci. 132 (2013), 105-113.Search in Google Scholar

31. Sekhwal, M.K., Sharma, V. and Sarin, R. Annotation of glycoside hydrolases in Sorghum bicolor using proteins interaction approach. J. Proteome Sci. Comput. Biol. 2 (2013) 2.Search in Google Scholar

32. Sekhwal, M.K., Swami, A.K., Sarin, R. and Sharma, V. Identification of salt treated proteins in sorghum using gene ontology linkage. Physiol. Mol. Biol. Plants 18 (2012) 209-16.Search in Google Scholar

33. Damerval, C., Vienne, D.D., Zivy, M. and Thiellement, H. Technical improvements in two-imensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7 (1986) 52-54.Search in Google Scholar

34. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254.Search in Google Scholar

35. Blackshear, P.J. Systems for polyacrylamide gel electrophoresis. Methods Enzymol. 104 (1984) 237-255.Search in Google Scholar

36. Shameer, K., Ambika, S., Varghese, S.M., Karaba, N., Udayakumar, M. and Sowdhamini, R. STIFDB-Arabidopsis stress responsive transcription factor DataBase. Int. J. Plant Genomics 2009 (2009) 583429-583436.Search in Google Scholar

37. Riano-Pachon, D.M., Ruzicic, S., Dreyer, I. and Mueller-Roeber, B. PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8 (2007) 42-51.Search in Google Scholar

38. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402.Search in Google Scholar

39. UniProt Consortium. The Universal Protein Resource (UniProt). Nucleic Acids Res. 35 (2007) D193-D197.10.1093/nar/gkl929Search in Google Scholar PubMed PubMed Central

40. Bateman, A., Coin, L., Durbin, R., Finn, R.D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E.L., Studholme, D.J., Yeats, C. and Eddy, S.R. The Pfam protein families database. Nucleic Acids Res. 32 (2004) D138-D141.10.1093/nar/gkh121Search in Google Scholar PubMed PubMed Central

41. Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouze, P. and Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30 (2002) 325-327.Search in Google Scholar

42. Ostlund, G., Schmitt, T., Forslund, K., Kostler, T., Messina, D.N., Roopra, S., Frings, O. and Sonnhammer, E.L. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38 (2010) D196-203.10.1093/nar/gkp931Search in Google Scholar PubMed PubMed Central

43. Yilmaz, A., Mejia-Guerra, M.K., Kurz, K., Liang, X., Welch, L. and Grotewold, E. AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res. 39 (2011) D1118-1122.10.1093/nar/gkq1120Search in Google Scholar PubMed PubMed Central

44. Rhee, S.Y., Beavis, W., Berardini, T.Z., Chen, G., Dixon, D., Doyle, A., Garcia-Hernandez, M. and Huala, E. The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31 (2003) 224-228.Search in Google Scholar

45. Hunter, S., Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Binns, D., Bork, P., Das, U., Daugherty, L., Duquenne, L., Finn, R.D., Gough, J., Haft, D., Hulo, N., Kahn, D., Kelly, E., Laugraud, A., Letunic, I., Lonsdale, D., Lopez, R., Madera, M., Maslen, J., McAnulla, C., McDowall, J., Mistry, J., Mitchell, A., Mulder, N., Natale, D., Orengo, C., Quinn, A.F., Selengut, J.D., Sigrist, C.J., Thimma, M., Thomas, P.D., Valentin, F., Wilson, D., Wu, C.H. and Yeats, C. InterPro: the integrative protein signature database. Nucleic Acids Res. 37 (2009) D211-215.10.1093/nar/gkn785Search in Google Scholar PubMed PubMed Central

46. Jiang, J.J. and Conrath, D.W. Semantic similarity based on corpus statistics and lexical taxonomy. Proc. ROCLING X. Taiwan (1997) 19-33.Search in Google Scholar

47. Ding, X., Richter, T., Chen, M., Fujii, H., Seo, Y.S., Xie, M., Zheng, X., Kanrar, S., Stevenson, R.A., Dardick, C., Li, Y., Jiang, H., Zhang, Y., Yu, F., Bartley, L.E., Chern, M., Bart, R., Chen, X., Zhu, L., Farmerie, W.G., Gribskov, M., Zhu, J.K., Fromm, M.E., Ronald, P.C. and Song, W.Y. A rice kinase-protein interaction map. Plant Physiol. 149 (2009) 1478-1492.Search in Google Scholar

48. Wippel, K. and Sauer, N. Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter. J. Exp. Bot. 63 (2012) 669-679.Search in Google Scholar

49. Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M. and Guo, Y. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19 (2007) 1415-1431.Search in Google Scholar

50. Anjum, S.A., Xie, X., Wang, L., Saleem, M. F., Man, C. and Lei W. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res. 6 (2011) 2026-2032. Search in Google Scholar

51. Krasensky, J. and Jonak, C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63 (2012) 1593-608.Search in Google Scholar

52. Nakashima K. and Yamaguchi-Shinozaki, K. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol. Plant 126 (2006) 62-71.Search in Google Scholar

53. Sazegari, S. and Niazi, A. Isolation and molecular characterization of wheat (Triticum aestivum) dehydration responsive element binding factor (DREB) isoforms. Aust. J. Crop Sci. 6 (2012) 1037-1044.Search in Google Scholar

54. Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K. and Yamaguchi- Shinozaki, K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and coldinducible gene expression. Biochem. Biophys. Res. Commun. 290 (2002) 998-1009.10.1006/bbrc.2001.6299Search in Google Scholar PubMed

55. Sharoni, A.M., Nuruzzaman, M., Satoh, K., Moumeni, A., Attia, K., Venuprasad, R., Serraj, R., Kumar, A., Leung, H., Islam, A.K. and Kikuchi, S. Comparative transcriptome analysis of AP2/EREBP gene family under normal and hormone treatments, and under two drought stresses in NILs setup by Aday selection and IR64. Mol. Genet. Genomics 287 (2012) 1-19.Search in Google Scholar

56. Zhao, L., Hu, Y., Chong, K. and Wang, T. ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance of rice. Ann. Bot. 105 (2010) 401-409.Search in Google Scholar

57. Mundy, J. and Chua, N.H. Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J. 7 (1988) 2279-2286.Search in Google Scholar

58. Kizis, D., Lumbreras, V. and Pages, M. Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett. 498 (2001) 187-189.Search in Google Scholar

59. Abe, H., Yamaguchi-Shinozaki, K., Urao, T., Iwasaki, T. and Shinozaki, K. Role of MYC and MYB homologs in drought and abscisic acid regulated gene expression. Plant Cell 9 (1997) 1859-1868.Search in Google Scholar

60. Ma, H.S., Liang, D., Shuai, P., Xia, X.L. and Yin, W.L. The salt and drought inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J. Exp. Bot. 61 (2010) 4011-4019.Search in Google Scholar

61. Shirsat, A., Wilford, N., Croy, R. and Boulter, D. Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol. Gen. Genet. 215 (1989) 326-331.Search in Google Scholar

62. Dunn, M.A., White, A.J., Vural, S. and Hughes, M.A. Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeum vulgare L.). Plant Mol. Biol. 38 (1998) 551-564.Search in Google Scholar

63. Blecken, J., Weisshaar, B. and Herzfeld, F. Two distinct cis-acting elements are involved in light-dependent activation of the pea elip promoter. Mol. Gen. Genet. 245 (1994) 371-379.Search in Google Scholar

64. Lopez-Ochoa, L, Acevedo-Hernandez, G, Martinez-Hernandez, A., Arguello-Astorga, G. and Herrera-Estrella, L. Structural relationships between diverse cis-acting elements are critical for the functional properties of a rbcS minimal light regulatory unit. J. Exp. Bot. 58 (2007) 4397-4406.Search in Google Scholar

65. Katiyar, A., Smita, S., Lenka, S.K., Rajwanshi, R., Chinnusamy, V. and Bansal, K.C. Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13 (2012) 544-562.Search in Google Scholar

66. Yang, A., Dai, X. and Zhang, W.H. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J. Exp. Bot. 63 (2012) 2541-2556.10.1093/jxb/err431Search in Google Scholar PubMed PubMed Central

67. Seo, P.J., Xiang, F., Qiao, M., Park, J.Y., Lee, Y.N., Kim, S.G., Lee, Y.H., Park, W.J. and Park, C.M. The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 151 (2009) 275-289.Search in Google Scholar

68. Dai, X., Xu, Y., Ma, Q., Xu, W., Wang, T., Xue, Y. and Chong. K. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol. 143 (2007) 1739-1751.10.1104/pp.106.094532Search in Google Scholar PubMed PubMed Central

69. Reyes, J.C., Muro-Pastor, M.I. and Florencio, F.J. The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol. 134 (2004) 1718-1732.10.1104/pp.103.037788Search in Google Scholar PubMed PubMed Central

70. Sun, T.P. Gibberellin metabolism, perception and signaling pathways in Arabidopsis. Arabidopsis Book 6 (2008) e0103-0131.10.1199/tab.0103Search in Google Scholar PubMed PubMed Central

71. Toh, S., Imamura, A., Watanabe, A., Nakabayashi, K., Okamoto, M., Jikumaru, Y., Hanada, A., Aso, Y., Ishiyama, K., Tamura, N., Iuchi, S., Kobayashi, M., Yamaguchi, S., Kamiya, Y., Nambara, E., and Kawakami N. High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellins action in Arabidopsis seeds. Plant Physiol. 146 (2008) 1368-1385.Search in Google Scholar

72. Hagen, G. and Guilfoyle, T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol. Biol. 49 (2002) 373-385.10.1023/A:1015207114117Search in Google Scholar

73. Xing, H., Pudake, R.N., Guo, G., Xing, G., Hu, Z., Zhang, Y., Sun, Q. and Ni, Z. Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12 (2011) 178-190.Search in Google Scholar

74. Reed, J.W. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6 (2001) 420-425.Search in Google Scholar

75. Tian, Q., Uhlir, N.J. and Reed, J.W. Arabidopsis SHY2/IAA3 inhibits auxinregulated gene expression. Plant Cell 14 (2002) 301-319.Search in Google Scholar

76. Ying, S., Zhang, D.F., Fu, J., Shi, Y.S., Song, Y.C., Wang, T.Y. and Li, Y. Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235 (2012) 253-266.Search in Google Scholar

77. Huang, X.S., Liu, J.H. and Chen, X.J. Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol. 10 (2010) 230-247.Search in Google Scholar

78. Zhao, J.P., Jiang, X.L., Zhang, B.Y. and Su, X.H. Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7 (2012) e44968-44980.10.1371/journal.pone.0044968Search in Google Scholar PubMed PubMed Central

79. Lu, X., Jiang, W., Zhang, L., Zhang, F., Zhang, F., Shen, Q., Wang, G. and Tang, K. AaERF1 positively regulates the resistance to Botrytis cinerea in Artemisia annua. PLoS One 8 (2013) e57657-57668.10.1371/journal.pone.0057657Search in Google Scholar PubMed PubMed Central

80. Luo, X., Bai, X., Sun, X., Zhu, D., Liu, B., Ji, W., Cai, H., Cao, L., Wu, J., Hu, M., Liu, X., Tang, L. and Zhu Y. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J. Exp. Bot. 64 (2013) 2155-2169.Search in Google Scholar

81. Fujiwara, T. and Beachy, R.N. Tissue-specific and temporal regulation of a beta-conglycinin gene: roles of the RY repeat and other cis-acting elements. Plant Mol. Biol. 24 (1994) 261-272.Search in Google Scholar

82. Fauteux, F. and Stromvik, M.V. Seed storage protein gene promoters contain conserved DNA motifs in Brassicaceae, Fabaceae and Poaceae. BMC Plant Biol. 9 (2009) 126-136. 10.1186/1471-2229-9-126Search in Google Scholar PubMed PubMed Central

Received: 2014-5-19
Accepted: 2014-12-1
Published Online: 2015-3-25
Published in Print: 2015-3-1

© 2015 University of Wrocław, Poland

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