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Cross talk between energy cost and expression of Methyl Jasmonate-regulated genes: from DNA to protein

  • Ehsan Sadeghnezhad
  • Mohsen Sharifi
  • Hassan Zare-maivan
  • Babak Khorsand
  • Javad Zahiri
Original Article
  • 12 Downloads

Abstract

Plant cell balances energy consumption for its different biological processes under oxidative circumstances. The aim of the present study is to deepen our knowledge of the regulation of Methyl Jasmonate (MeJA) responsive genes, especially the discussion on energy index from DNA to protein. The cis- and trans-responsive elements, the translation efficiency and accuracy, the codon adaptation, the amount of entropy in the codon usage of a sequence and finally, co-expression patterns of up-regulated genes by MeJA in shoot and root of Arabidopsis plant under 8 different abiotic stresses (UV, cold, drought, heat, wounding, osmotic, oxidative, and salinity) were analyzed. We designed an R package, namely SADEG (https://cran.r-project.org/web/packages/SADEG/) to estimate the relative stability of the DNA sequence. Cost of amino acids biosynthesis was weakly correlated with the energy consumption for each triplet-triplet binding related to each amino acid during the translation process. Our results also demonstrated that natural selection, gene length, gene expression levels, and influence of GC3s on the codon bias could affect the codon usage patterns of MeJA-responsive genes in Arabidopsis.

Keywords

Abiotic stress Energy cost Methyl Jasmonate-responsive genes SADEG package Stacking energy 

Abbreviation

AFE

Average free energy

BAR

Bio-analytic resource database

CAI

Codon adaptation index

CUB

Codon usage bias

DRGM

Down-regulated genes by MeJA

E-CAI

Expect- codon adaptation index

ENC

Effective number of codons

GCP

Genes co-expression percentage

GO

Gene ontology

URGM

Up-regulated genes by MeJA

Notes

Acknowledgements

The authors greatly appreciate Tarbiat Modares University for supporting this research.

Author contribution statement

ES, M.S, and H.Z.M designed the research and collected the experimental data. B.K, E.S, and J.Z created SADEG package and performed the computational analysis. E.S wrote the original manuscript and all co-authors edited the manuscript and package manual.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13562_2018_480_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1309 kb)
13562_2018_480_MOESM2_ESM.xlsx (438 kb)
Supplementary material 2 (XLSX 438 kb)
13562_2018_480_MOESM3_ESM.xlsx (320 kb)
Supplementary material 3 (XLSX 320 kb)

References

  1. Almlöf M, Andér M, Åqvist J (2007) Energetics of codon—anticodon recognition on the small ribosomal subunit. Biochemistry 46:200–209CrossRefPubMedGoogle Scholar
  2. Aravind L, Landsman D (1998) AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res 26:4413–4421CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350CrossRefPubMedGoogle Scholar
  4. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(suppl_2):W202–W208CrossRefPubMedPubMedCentralGoogle Scholar
  5. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bowman JL (2000) The YABBY gene family and abaxial cell fate. Curr Opin Plant Biol 3:17–22CrossRefPubMedGoogle Scholar
  7. Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907PubMedPubMedCentralGoogle Scholar
  8. Chen Y, Xu Q, Tan C, Li X, Chi X, Cai B, Chen JL (2017) Genomic analysis of codon usage shows influence of mutation pressure, natural selection, and host features on Senecavirus A evolution. Microb Pathog 112:313–319CrossRefPubMedGoogle Scholar
  9. Clarke SM, Cristescu SM, Miersch O, Harren FJ, Wasternack C, Mur LA (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187CrossRefPubMedGoogle Scholar
  10. Claverie P (1971) Calculation of interaction energy between triplets in the RNA 11 configuration. J Mol Biol 56:75–82CrossRefPubMedGoogle Scholar
  11. Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Biol 48:355–381CrossRefGoogle Scholar
  12. De Domenico S et al (2012) Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress. Plant Physiol Biochem 61:115–122CrossRefPubMedGoogle Scholar
  13. Duret L, Mouchiroud D (1999) Expression pattern and surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci 96:4482–4487CrossRefPubMedGoogle Scholar
  14. Fernández-Calvo P et al (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715CrossRefPubMedPubMedCentralGoogle Scholar
  15. Feys BJ, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gigliotti E (2007) Discovering statistics using SPSS. J Adv Nurs 58:303CrossRefGoogle Scholar
  17. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499CrossRefGoogle Scholar
  18. Hershberg R, Petrov DA (2008) Selection on codon bias. Annu Rev Genet 42:287–299CrossRefPubMedGoogle Scholar
  19. Hooper SD, Berg OG (2000) Gradients in nucleotide and codon usage along Escherichia coli genes. Nucleic Acids Res 28:3517–3523CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jakab G, Ton J, Flors V, Zimmerli L, Métraux J-P, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jumali SS, Said IM, Ismail I, Zainal Z (2011) Genes induced by high concentration of salicylic acid in Mitragyna speciosa. Aust J Crop Sci 5:296Google Scholar
  22. Lamesch P, Dreher K, Swarbreck D, Sasidharan R, Reiser L, Huala E (2010) Using the Arabidopsis information resource (TAIR) to find information about Arabidopsis genes. Curr Protoc Bioinform 30(1):1–11Google Scholar
  23. Lee T-M, Lur H-S, Chu C (1997) Role of abscisic acid in chilling tolerance of rice (Oryza sativa L.) seedlings.: II. Modulation of free polyamine levels. Plant Sci 126:1–10CrossRefGoogle Scholar
  24. Murata K, Sugita Y, Okamoto Y (2004) Free energy calculations for DNA base stacking by replica-exchange umbrella sampling. Chem Phys Lett 385:1–7CrossRefGoogle Scholar
  25. Nejad ES, Askari H, Soltani S (2012) Regulatory TGACG-motif may elicit the secondary metabolite production through inhibition of active cyclin-dependent kinase/cyclin complex. Plant Omics 5:553Google Scholar
  26. Pauwels L et al (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci 105:1380–1385CrossRefPubMedGoogle Scholar
  27. Pedranzani H et al (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Reg 41:149–158CrossRefGoogle Scholar
  28. Puigbò P, Bravo IG, Garcia-Vallvé S (2008) E-CAI: a novel server to estimate an expected value of codon adaptation index (eCAI). BMC Bioinform 9:65CrossRefGoogle Scholar
  29. Sadeghnezhad E, Sharifi M, Zare-Maivan H (2016) Profiling of acidic (amino and phenolic acids) and phenylpropanoids production in response to methyl jasmonate-induced oxidative stress in Scrophularia striata. Planta 244:75–85CrossRefPubMedGoogle Scholar
  30. Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep 32:1085–1098CrossRefPubMedGoogle Scholar
  31. Sayyari M, Babalar M, Kalantari S, Martínez-Romero D, Guillén F, Serrano M, Valero D (2011) Vapour treatments with methyl salicylate or methyl jasmonate alleviated chilling injury and enhanced antioxidant potential during postharvest storage of pomegranates. Food Chem 124:964–970CrossRefGoogle Scholar
  32. Seshasayee ASN, Sivaraman K, Luscombe NM (2011) An overview of prokaryotic transcription factors. In: A handbook of transcription factors. Springer, Dordrecht, pp 7–23Google Scholar
  33. Sharp PM, Li W-H (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295CrossRefPubMedPubMedCentralGoogle Scholar
  34. Soltani S, Askari H, Ejlali N, Aghdam R (2014) The structural properties of DNA regulate gene expression. Mol BioSyst 10:273–280CrossRefPubMedGoogle Scholar
  35. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677CrossRefPubMedPubMedCentralGoogle Scholar
  36. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163CrossRefPubMedGoogle Scholar
  37. van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297CrossRefPubMedGoogle Scholar
  38. Vassilenko KS, Alekhina OM, Dmitriev SE, Shatsky IN, Spirin AS (2011) Unidirectional constant rate motion of the ribosomal scanning particle during eukaryotic translation initiation. Nucleic Acids Res 39:5555–5567CrossRefPubMedPubMedCentralGoogle Scholar
  39. Vicario S, Moriyama EN, Powell JR (2007) Codon usage in twelve species of Drosophila. BMC Evol Biol 7:226CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365–1374CrossRefPubMedGoogle Scholar
  41. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol Adv 32:31–39CrossRefPubMedGoogle Scholar
  43. Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87:23–29CrossRefPubMedGoogle Scholar
  44. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37:W652–W660CrossRefPubMedPubMedCentralGoogle Scholar
  45. Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391CrossRefPubMedGoogle Scholar
  46. Zhao IL, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2012) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51CrossRefPubMedGoogle Scholar

Copyright information

© Society for Plant Biochemistry and Biotechnology 2018

Authors and Affiliations

  • Ehsan Sadeghnezhad
    • 1
  • Mohsen Sharifi
    • 1
  • Hassan Zare-maivan
    • 1
  • Babak Khorsand
    • 2
  • Javad Zahiri
    • 3
  1. 1.Department of Plant Biology, Faculty of Biological SciencesTarbiat Modares UniversityTehranIran
  2. 2.Department of Computer Engineering, Faculty of EngineeringFerdowsi University of MashhadMashhadIran
  3. 3.Bioinformatics and Computational Omics. Lab (BioCOOL), Department of Biophysics, Faculty of Biological SciencesTarbiat Modares UniversityTehranIran

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