Advertisement

Amino Acids

, Volume 51, Issue 5, pp 839–853 | Cite as

Computational characterization of structural and functional roles of DREB1A, DREB1B and DREB1C in enhancing cold tolerance in rice plant

  • Ravindra Donde
  • Manoj Kumar Gupta
  • Gayatri Gouda
  • Jitendra Kumar
  • Ramakrishna Vadde
  • Khirod Kumar Sahoo
  • Sushanta Kumar Dash
  • Lambodar BeheraEmail author
Original Article
  • 210 Downloads

Abstract

Rice serves as the major food for almost half of the world population. Because of its origin in the tropical and subtropical area, rice is more sensitive towards cold stress. Three homologs of DREB1, namely DREB1A, DREB1B and DREB1C are induced Queryduring cold stress and after binding with GCC-box in the promoter region of the target gene, they enhance cold tolerance in rice plants. Though the majority of DREBs bind GCC-box, the degree of activation varies among DREBs. The protein encoded via these three transcription factors contains a common domain, namely AP2/ERF. In silico method was utilised to predict 3D structure of each AP2/ERF domain. The molecular dynamic analysis suggests, under the normal environmental condition, in each AP2/ERF domain, a positive correlation exists between β-strands and the movement of C-α is constrained. However, during cold stress, when AP2/ERF domain binds with GCC-box present in the promoter region of the target gene, mean pressure of each three AP2/ERF domain gets lowered and final potential energy increases. A positive correlation between β-strands gets disrupted and C-α experiences random movement suggesting enhanced activity of DREB1A, DREB1B and DREB1C during cold stress and enhancement of cold tolerance in plants. Further, MM/PBSA calculations for protein–DNA affinities reveal that, due to lack of α2 in DREB1C, the binding affinity of GCC-box with AP2/ERF domain of DREB1A > DREB1B > DREB1C. Thus, due to a better binding affinity with GCC-box, DREB1A and DREB1B can be utilised in near future for increasing cold tolerance of rice plant and increasing yield.

Keywords

DREB1 Protein–DNA interaction Molecular dynamics Simulation Cold stress 

Notes

Compliance with ethical standards

Conflict of interest

The authors of this manuscript declare no conflict of interest.

Ethical statement

This article involves only computational work and does not contain any studies with human participants or animals.

Supplementary material

726_2019_2727_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)

References

  1. Abraham MJ, Murtola T, Schulz R et al (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2:19–25.  https://doi.org/10.1016/j.softx.2015.06.001 CrossRefGoogle Scholar
  2. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274.  https://doi.org/10.1007/s00299-006-0204-8 CrossRefGoogle Scholar
  3. Aier I, Varadwaj PK, Raj U (2016) Structural insights into conformational stability of both wild-type and mutant EZH2 receptor. Sci Rep 6:34984.  https://doi.org/10.1038/srep34984 CrossRefGoogle Scholar
  4. Akhtar M, Jaiswal A, Taj G et al (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91:385–395CrossRefGoogle Scholar
  5. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410.  https://doi.org/10.1016/S0022-2836(05)80360-2 CrossRefGoogle Scholar
  6. Biovia DS (2017) Discovery studio visualizer. San DiegoGoogle Scholar
  7. Chakravarthy S, Tuori RP, D’Ascenzo MD et al (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050.  https://doi.org/10.1105/tpc.017574 CrossRefGoogle Scholar
  8. Chang T-T (1987) The impact of rice on human civilization and population expansion. Interdiscip Sci Rev 12:63–69.  https://doi.org/10.1179/isr.1987.12.1.63 CrossRefGoogle Scholar
  9. Chen R, Li L, Weng Z (2003) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52:80–87.  https://doi.org/10.1002/prot.10389 CrossRefGoogle Scholar
  10. Chen J-Q, Meng X-P, Zhang Y et al (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198.  https://doi.org/10.1007/s10529-008-9811-5 CrossRefGoogle Scholar
  11. Chen VB, Arendall WB, Headd JJ et al (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12–21.  https://doi.org/10.1107/S0907444909042073 CrossRefGoogle Scholar
  12. Chen L, Zheng Q-C, Zhang H-X (2015) Insights into the effects of mutations on Cren7-DNA binding using molecular dynamics simulations and free energy calculations. Phys Chem Chem Phys PCCP 17:5704–5711.  https://doi.org/10.1039/c4cp05413j CrossRefGoogle Scholar
  13. De Boer K, Tilleman S, Pauwels L et al (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J Cell Mol Biol 66:1053–1065.  https://doi.org/10.1111/j.1365-313X.2011.04566.x CrossRefGoogle Scholar
  14. de Castro E, Sigrist CJA, Gattiker A et al (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–W365.  https://doi.org/10.1093/nar/gkl124 CrossRefGoogle Scholar
  15. de Freitas GPM, Basu S, Ramegowda V et al (2016) Comparative analysis of gene expression in response to cold stress in diverse rice genotypes. Biochem Biophys Res Commun 471:253–259CrossRefGoogle Scholar
  16. Dossa K, Wei X, Li D et al (2016) Insight into the AP2/ERF transcription factor superfamily in sesame and expression profiling of DREB subfamily under drought stress. BMC Plant Biol 16:171.  https://doi.org/10.1186/s12870-016-0859-4 CrossRefGoogle Scholar
  17. Dubouzet JG, Sakuma Y, Ito Y et al (2003) OsDREB genes in rice, oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J Cell Mol Biol 33:751–763CrossRefGoogle Scholar
  18. Gasteiger E, Hoogland C, Gattiker A et al (2005) Protein identification and analysis tools on the ExPASy Server. In: The proteomics protocols handbook. Springer, pp 571–607Google Scholar
  19. Gupta MK, Vadde R (2018) In silico identification of natural product inhibitors for γ-secretase activating protein, a therapeutic target for Alzheimer’s disease. J Cell Biochem.  https://doi.org/10.1002/jcb.28316 Google Scholar
  20. Gupta MK, Vadde R (2019) Insights into the structure-function relationship of both wild and mutant Zinc transporter ZnT8 in human: a computational structural biology approach. J Biomol Struct Dyn.  https://doi.org/10.1080/07391102.2019.1567391 Google Scholar
  21. Gupta MK, Vadde R, Donde R et al (2018) Insights into the structure–function relationship of brown plant hopper resistance protein, Bph14 of rice plant: a computational structural biology approach. J Biomol Struct Dyn.  https://doi.org/10.1080/07391102.2018.1462737 Google Scholar
  22. Gupta MK, Vadde R, Gouda G et al (2019) Computational approach to understand molecular mechanism involved in BPH resistance in Bt- rice plant. J Mol Graph Model 88:209–220.  https://doi.org/10.1016/j.jmgm.2019.01.018 CrossRefGoogle Scholar
  23. Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861CrossRefGoogle Scholar
  24. Hong JC (2016) Chapter 3—General aspects of plant transcription factor families. In: Gonzalez DH (ed) Plant transcription factors. Academic Press, Boston, pp 35–56CrossRefGoogle Scholar
  25. Hulo N, Bairoch A, Bulliard V et al (2006) The PROSITE database. Nucleic Acids Res 34:D227–230.  https://doi.org/10.1093/nar/gkj063 CrossRefGoogle Scholar
  26. Ito Y, Katsura K, Maruyama K et al (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153.  https://doi.org/10.1093/pcp/pci230 CrossRefGoogle Scholar
  27. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225CrossRefGoogle Scholar
  28. Kandpal RP, Rao NA (1985) Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine coracana) seedlings during water stress and the effect of proline on protein biosynthesis. Plant Sci 40:73–79.  https://doi.org/10.1016/0168-9452(85)90044-5 CrossRefGoogle Scholar
  29. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291CrossRefGoogle Scholar
  30. Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748.  https://doi.org/10.1093/jxb/err210 CrossRefGoogle Scholar
  31. Li H, Wang Y, Wu M et al (2017) Genome-wide identification of AP2/ERF transcription factors in cauliflower and expression profiling of the ERF family under salt and drought stresses. Front Plant Sci.  https://doi.org/10.3389/fpls.2017.00946 Google Scholar
  32. Liu Q, Kasuga M, Sakuma Y et al (1998) 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 10:1391–1406CrossRefGoogle Scholar
  33. Liu X, Wei X, Sheng Z et al (2016) Polycomb protein OsFIE2 affects plant height and grain yield in rice. PLOS One 11:e0164748.  https://doi.org/10.1371/journal.pone.0164748 CrossRefGoogle Scholar
  34. Luscombe NM, Laskowski RA, Thornton JM (1997) NUCPLOT: a program to generate schematic diagrams of protein-nucleic acid interactions. Nucleic Acids Res 25:4940–4945CrossRefGoogle Scholar
  35. Nakashima K, Tran L-SP, Van Nguyen D et al (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J Cell Mol Biol 51:617–630.  https://doi.org/10.1111/j.1365-313X.2007.03168.x CrossRefGoogle Scholar
  36. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182.  https://doi.org/10.1105/tpc.7.2.173 CrossRefGoogle Scholar
  37. Pandey B, Sharma P, Tyagi C et al (2016) Structural modeling and molecular simulation analysis of HvAP2/EREBP from barley. J Biomol Struct Dyn 34:1159–1175.  https://doi.org/10.1080/07391102.2015.1073630 CrossRefGoogle Scholar
  38. Pandey B, Grover A, Sharma P (2018) Molecular dynamics simulations revealed structural differences among WRKY domain-DNA interaction in barley (Hordeum vulgare). BMC Genom 19:1.  https://doi.org/10.1186/s12864-018-4506-3 CrossRefGoogle Scholar
  39. Patra MC, Rath SN, Pradhan SK et al (2014) Molecular dynamics simulation of human serum paraoxonase 1 in DPPC bilayer reveals a critical role of transmembrane helix H1 for HDL association. Eur Biophys J 43:35–51.  https://doi.org/10.1007/s00249-013-0937-6 CrossRefGoogle Scholar
  40. Pirrello J, Prasad BN, Zhang W et al (2012) Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol 12:190.  https://doi.org/10.1186/1471-2229-12-190 CrossRefGoogle Scholar
  41. Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLOS One 8:e66428.  https://doi.org/10.1371/journal.pone.0066428 CrossRefGoogle Scholar
  42. Sasaki K, Mitsuhara I, Seo S et al (2007) Two novel AP2/ERF domain proteins interact with cis-element VWRE for wound-induced expression of the Tobacco tpoxN1 gene. Plant J Cell Mol Biol 50:1079–1092.  https://doi.org/10.1111/j.1365-313X.2007.03111.x CrossRefGoogle Scholar
  43. Seck PA, Diagne A, Mohanty S, Wopereis MC (2012) Crops that feed the world 7: rice. Food Secur 4:7–24CrossRefGoogle Scholar
  44. Taiz L (2013) Agriculture, plant physiology, and human population growth: past, present, and future. Theor Exp Plant Physiol 25:167–181.  https://doi.org/10.1590/S2197-00252013000300001 Google Scholar
  45. Turner PJ (2005) XMGRACE, Version 5.1. 19. Cent Coast Land-Margin Res Or Grad Inst Sci Technol Beaverton ORGoogle Scholar
  46. Wang Y, Wan L, Zhang L et al (2012) An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol Biol 78:275–288.  https://doi.org/10.1007/s11103-011-9861-2 CrossRefGoogle Scholar
  47. Wang J, Xu H, Li N et al (2015) Artificial selection of Gn1a plays an important role in improving rice yields across different ecological regions. Rice 8:37.  https://doi.org/10.1186/s12284-015-0071-4 CrossRefGoogle Scholar
  48. Wang C, Greene D, Xiao L et al (2017) Recent developments and applications of the MMPBSA method. Front Mol Biosci.  https://doi.org/10.3389/fmolb.2017.00087 Google Scholar
  49. Wei B, Jing R, Wang C et al (2009) Dreb1 genes in wheat (Triticum aestivum L.): development of functional markers and gene mapping based on SNPs. Mol Breed 23:13–22.  https://doi.org/10.1007/s11032-008-9209-z CrossRefGoogle Scholar
  50. Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407–W410.  https://doi.org/10.1093/nar/gkm290 CrossRefGoogle Scholar
  51. Wu L, Zhang Z, Zhang H et al (2008) Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol 148:1953–1963.  https://doi.org/10.1104/pp.108.126813 CrossRefGoogle Scholar
  52. Xie G, Kato H, Imai R (2012) Biochemical identification of the OsMKK6–OsMPK3 signalling pathway for chilling stress tolerance in rice. Biochem J 443:95–102.  https://doi.org/10.1042/BJ20111792 CrossRefGoogle Scholar
  53. Yang J, Zhang Y (2015) I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Res 43:W174–W181.  https://doi.org/10.1093/nar/gkv342 CrossRefGoogle Scholar
  54. Yasuda H (2017) Cross-tolerance to thermal stresses and its application to the development of cold tolerant rice. Jpn Agric Res Q JARQ 51:99–105.  https://doi.org/10.6090/jarq.51.99 CrossRefGoogle Scholar
  55. Zhang Y, Chen C, Jin X-F et al (2009) Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Rep 42:486–492CrossRefGoogle Scholar
  56. Zhang X, Tang Y, Ma Q et al (2013) OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean. PLOS One 8:e83011.  https://doi.org/10.1371/journal.pone.0083011 CrossRefGoogle Scholar
  57. Zhang Q, Chen Q, Wang S et al (2014) Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice 7:24.  https://doi.org/10.1186/s12284-014-0024-3 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Ravindra Donde
    • 1
  • Manoj Kumar Gupta
    • 2
  • Gayatri Gouda
    • 1
  • Jitendra Kumar
    • 1
  • Ramakrishna Vadde
    • 2
  • Khirod Kumar Sahoo
    • 3
  • Sushanta Kumar Dash
    • 1
  • Lambodar Behera
    • 1
    Email author
  1. 1.ICAR-National Rice Research InstituteCuttackIndia
  2. 2.Department of Biotechnology and BioinformaticsYogi Vemana UniversityKadapaIndia
  3. 3.Department of BiotechnologyRavenshaw UniversityCuttackIndia

Personalised recommendations