Skip to main content
SpringerLink
Log in

Excited states and energy transfer among DNA bases in double helices

  • Perspective
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The study of excited states and energy transfer in DNA double helices has recently gained new interest connected to the development of computational techniques and that of femtosecond spectroscopy. The present article points out contentious questions regarding the nature of the excited states and the occurrence of energy transfer and shows how they are currently approached. Using as example the polymer poly(dA)·poly(dT), composed of about 2000 adenine—thymine pairs, a model is proposed on the basis of time-resolved measurements (fluorescence decays, fluorescence anisotropy decays and fluorescence spectra, obtained with femtosecond resolution), associated to steady-state spectra. According to this qualitative model, excitation at 267 nm populates excited states that are delocalized over a few bases (excitons). Ultrafast internal conversion directs the excited state population to the lower part of the exciton band giving rise to fluorescence. Questions needing further investigations, both theoretical and experimental, are underlined with particular emphasis on delicate points related to the complexity and the plasticity of these systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. D. Markovitsi, D. Onidas, T. Gustavsson, F. Talbot and E. Lazzarotto, Collective behavior of Franck–Condon excited states and energy transfer in double helices, J. Am. Chem. Soc., 2005, 127, 17130–31.

    Article  CAS  PubMed  Google Scholar 

  2. I. Tinoco, Jr., Hypochromism in polynucleotides, J. Am. Chem. Soc., 1960, 82, 4785–90.

    Article  CAS  Google Scholar 

  3. W. Rhodes, Hypochromism and other spectral properties of helical polynucleotides, J. Am. Chem. Soc., 1961, 83, 3609–17.

    Article  CAS  Google Scholar 

  4. T. Miyata and S. Yomosa, Exciton states in synthetic polynucleotides, J. Phys. Soc. Jpn., 1969, 27, 727–35.

    Article  CAS  Google Scholar 

  5. J. Eisinger and R. G. Shulman, Excited electronic states of DNA, Science, 1968, 161, 1311–19.

    Article  CAS  PubMed  Google Scholar 

  6. B. Bouvier, J. P. Dognon, R. Lavery, D. Markovitsi, P. Millié, D. Onidas and K. Zakrzewska, Influence of conformational dynamics on the exciton states of DNA oligomers, J. Phys. Chem. B, 2003, 107, 13512–22.

    Article  CAS  Google Scholar 

  7. B. Bouvier, T. Gustavsson, D. Markovitsi, P. Millié, Dipolar coupling between electronic transitions of the DNA bases and its relevance to exciton states in double helices, Chem. Phys., 2002, 275, 75–92.

    Article  CAS  Google Scholar 

  8. E. Emanuele, D. Markovitsi, P. Millié and K. Zakrzewska, UV spectra and excitation delocalisation in DNA: influence of the spectral width, ChemPhysChem, 2005, 6, 1387–92.

    Article  CAS  PubMed  Google Scholar 

  9. E. Emanuele, K. Zakrzewska, D. Markovitsi, R. Lavery and P. Millie, Exciton states of dynamic DNA double helices: alternating dCdG sequences, J. Phys. Chem. B, 2005, 109, 16109–18.

    Article  CAS  PubMed  Google Scholar 

  10. M. Rist, H.-A. Wagenknecht and T. Fiebig, Exciton and excimer formation in DNA at room temperature, ChemPhysChem, 2002, 8, 704–07.

    Article  Google Scholar 

  11. D. F. Lewis, X. Liu, Y. Wu and X. Zuo, Stepwise evolution of the structure and the electronic properties of DNA, J. Am. Chem. Soc., 2003, 125, 12729–31.

    Article  CAS  PubMed  Google Scholar 

  12. F. D. Lewis, L. Zhang, X. Liu, X. Zuo, D. M. Tiede, H. Long and G. C. Schatz, DNA as helical ruler: exciton-coupled circular dichroism in DNA conjugates, J. Am. Chem. Soc., 2005, 14445–53.

    Google Scholar 

  13. F. D. Lewis, Y. Wu, L. Zhang, X. Zuo and R. T. W. Hayes, R., DNA-mediated exciton coupling and electron transfer between donor and acceptor stilbenes separated by a variable number of base pairs, J. Am. Chem. Soc., 2004, 126, 8206–15.

    Article  CAS  PubMed  Google Scholar 

  14. S. L. Shapiro, A. J. Campillo, V. H. Kollman and W. B. Goad, Exciton transfer in DNA, Opt. Commun., 1975, 15, 308–10.

    Article  CAS  Google Scholar 

  15. A. Anders, Energy transfer in nucleic acid-dye complexes, Opt. Commun., 1978, 26, 339–42.

    Article  CAS  Google Scholar 

  16. D. M. Rayner, A. G. Szabo, R. O. Loutfy and R. W. Yip, Singlet energy transfer between nucleic acid bases and dyes in intercalation complexes, J. Phys. Chem., 1980, 84, 289–93.

    Article  CAS  Google Scholar 

  17. T. M. Nordlund, D. Xu and K. O. Evans, Excitation energy transfer in DNA: duplex melting and transfer from normal bases to 2-aminopurine, Biochemistry, 1993, 32, 12090–95.

    Article  CAS  PubMed  Google Scholar 

  18. D.-G. Xu and T. M. Nordlund, Sequence dependence of energy transfer in DNA oligonucleotides, Biophys. J., 2000, 78, 1042–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. J. Cadet and P. Vigny, in Bioorganic Photochemistry, ed. H. Morrison, John Wiley & Sons, New York, 1990, pp. 1–272.

  20. P. Vigny and J. P. Ballini, in Excited states in organic chemistry and biochemistry, ed. B. Pullman and N. Goldblum, D. Reidel Publishing Company, Doordrecht, Holland, 1977

  21. G. Ge and S. Georghiou, Excited-state properties of the alternating polynucleotide poly (dA–dT) poly (dA–dT), Photochem. Photobiol., 1991, 54, 301–05.

    Article  CAS  PubMed  Google Scholar 

  22. G. Ge and S. Georghiou, Room-temperature fluorescence properties of the polynucleotide polydA·polydT, Photochem. Photobiol., 1991, 54, 477–80.

    Article  CAS  PubMed  Google Scholar 

  23. S. Georghiou, G. R. Phillips and G. Ge, Resolution of the electronic absorption spectra of the adenine and thymine residues in poly(dA)·poly(dT), Biopolymers, 1992, 32, 1417–20.

    Article  CAS  PubMed  Google Scholar 

  24. C.-R. Huang and S. Georghiou, Room-temperature steady-state fluorescence properties of poly(dG-dC)·poly(dG-dC), Photochem. Photobiol., 1992, 56, 95–99.

    Article  CAS  PubMed  Google Scholar 

  25. S. Georghiou, T. D. Bradrick, A. Philippetis and J. Beechem, Large-amplitude picosecond anisotropy decay of the intrinsic fluorescence of double-stranded DNA, Biophys. J., 1996, 70, 1909–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. D. Markovitsi, A. Sharonov, D. Onidas and T. Gustavsson, Effect of molecular organisation in DNA oligomers studied by femtosecond fluorescence spectroscopy, ChemPhysChem, 2003, 3, 303–05.

    Article  Google Scholar 

  27. D. Markovitsi, D. Onidas, F. Talbot, S. Marguet, T. Gustavsson and E. Lazzarotto, UVB/UVC induced processes in model DNA helices studied by time-resolved spectroscopy: pitfalls and tricks, J. Photochem. Photobiol., A, 2006, 183, 1–8.

    Article  CAS  Google Scholar 

  28. C. E. Crespo-Hernández, B. Cohen and B. Kohler, Base stacking controls excited state dynamics in A–T DNA, Nature, 2005, 436, 1141–44.

    Article  PubMed  CAS  Google Scholar 

  29. D. Markovitsi, F. Talbot, T. Gustavsson, D. Onidas, E. Lazzarotto and S. Marguet, Complexity of excited state dynamics in DNA, Nature, 2006, 441, E7.

    Article  CAS  PubMed  Google Scholar 

  30. C. E. Crespo-Hernández, B. Cohen, B. Kohler, Nature, 2006, 441, E8.

    Article  CAS  Google Scholar 

  31. J. Řezáč and P. Hobza, On the nature of the duplex stability, Chem.–Eur. J., 2007, 13, 2983–2989.

    Article  PubMed  CAS  Google Scholar 

  32. I. Buchvarov, Q. Wang, M. Raytchev, A. Trifonov and T. Fiebig, Electronic energy delocalization and dissipation in single- and double-stranded DNA, Proc. Natl. Acad. Sci. USA, 2007, 104, 4794–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. R. Plessow, A. Brockhinke, W. Eimer, K. Kohse-Höinghaus, Intrinsic Time- and Wavelength-Resolved Fluorescence of Oligonucleotides: A Systematic Investigation Using a Novel Picosecond Laser Approach, J. Phys. Chem. B, 2000, 104, 3695–704.

    Article  CAS  Google Scholar 

  34. G. D. Scholes, Energy transfer and spectroscopic characterization of multichromophoric assemblies, J. Phys. Chem., 1996, 100, 18731–39.

    Article  CAS  Google Scholar 

  35. G. D. Scholes and K. P. Ghiggino, Electronic interactions and interchromophore excitation transfer, J. Phys. Chem., 1994, 98, 4580–90.

    Article  CAS  Google Scholar 

  36. T. Mančal, L. Valkunas and G. R. Fleming, Theory of exciton-charge transfer state coupled systems, Chem. Phys. Lett., 2006, 432, 301–05.

    Article  CAS  Google Scholar 

  37. S. Krawczyk and R. Lucowski, Electronic excited states of polynucleotides. A study by electroabsorption spectroscopy, J. Phys. Chem. B, 2007, 111, 1213–21.

    Article  CAS  PubMed  Google Scholar 

  38. D. Onidas, D. Markovitsi, S. Marguet, A. Sharonov and T. Gustavsson, Fluorescence properties of DNA nucleosides and nucleotides: a refined steady-state and femtosecond investigation, J. Phys. Chem. B, 2002, 106, 11367–74.

    Article  CAS  Google Scholar 

  39. R. A. Velapoldi and K. D. Mielenz, A fluorescence standard reference material: quinine sulfate dihydrate, U. S. Government Printing Office: Washington, D. C., Washington, 1980

    Google Scholar 

  40. T. Gustavsson, L. Cassara, V. Gulbinas, G. Gurzadyan, J.-C. Mialocq, S. Pommeret, M. Sorgius, P. von der Meulen, Femtosecond spectroscopic study of relaxation processes of three amino-substituted coumarin dyes in methanol and dimethyl sulfoxide, J. Phys. Chem. A, 1998, 102, 4229–45.

    Article  CAS  Google Scholar 

  41. S. K. Pal, L. Zhao, T. Xia and A. H. Zewail, Site- and sequence-selective ultrafast hydration of DNA, Proc. Natl. Acad. Sci. USA, 2003, 100, 13746–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. D. Andreatta, J. L. Pérez Lustres, S. A. Kovalenko, N. P. Ernsting, C. J. Murphy, R. S. Coleman and M. A. Berg, Power-law solvation dynamics in DNA over six decades in time, J. Am. Chem. Soc., 2005, 127, 7270–71.

    Article  CAS  PubMed  Google Scholar 

  43. N. J. Kim, G. Jeong, J. Sung, Y. S. Kim and Y. D. Park, Resonant two-photon ionization and laser induced fluorescence spectroscopy of jet cooled adenine, J. Chem. Phys., 2000, 113, 10051–55.

    Article  CAS  Google Scholar 

  44. C. Canuel, M. Elhanine, M. Mons, F. Piuzzi, B. Tardivel and I. Dimicoli, Time-resolved photoelectron and photoion fragmentation spectroscopy study of 9-methyladenine and its hydrates: a contribution to the understanding of the ultrafast radiationless decay of excited DNA bases, Phys. Chem. Chem. Phys., 2006, 8, 3978–87.

    Article  CAS  PubMed  Google Scholar 

  45. T. Gustavsson, A. Banyasz, E. Lazzarotto, D. Markovitsi, G. Scalmani, M. J. Frisch, V. Barone and R. Improta, Singlet excited state behavior of uracil and thymine in aqueous solution: a combined experimental and computational study of 11 uracil derivatives, J. Am. Chem. Soc., 2006, 128, 607–19.

    Article  CAS  PubMed  Google Scholar 

  46. T. Gustavsson, N. Sarkar, E. Lazzarotto, D. Markovitsi, V. Barone and R. Improta, Solvent effect on the singlet excited state dynamics of 5-fluorouracil in acetonitrile as compared to water, J. Phys. Chem. B, 2006, 110, 12843–47.

    Article  CAS  PubMed  Google Scholar 

  47. J. Peon and A. H. Zewail, DNA/RNA nucleotides and nucleosides: direct measurement of excited-state lifetimes by femtosecond fluorescence up-conversion, Chem. Phys. Lett., 2001, 348, 255–62.

    Article  CAS  Google Scholar 

  48. T. Gustavsson, A. Sharonov and D. Markovitsi, Thymine, thymidine and thymidine 5′-monophosphate studied by femtosecond fluorescence upconversion spectroscopy, Chem. Phys. Lett., 2002, 351, 195–200.

    Article  CAS  Google Scholar 

  49. T. Gustavsson, A. Sharonov, D. Onidas and D. Markovitsi, Adenine, deoxyadenine and deoxyadenine 5′-monophosphate studied by femtosecond fluorescence upconversion spectroscopy, Chem. Phys. Lett., 2002, 356, 49–54.

    Article  CAS  Google Scholar 

  50. J. M. Jean and B. P. Krueger, Structural fluctuations and excitation transfer between adenine and 2-aminopurine in single stranded deoxynucleotides, J. Phys. Chem. B, 2006, 110, 2899–909.

    Article  CAS  PubMed  Google Scholar 

  51. A. Blumen, J. Klafter and G. Zumofen, Optical spectroscopy of glasses, ed. I. Zschokke, Reidel Publishing Co., Dordecht, 1986, pp. 199–265.

  52. T. Douki, Low ionic strength reduces cytosine photoreactivity in UVC-irradiated isolated DNA, Photochem. Photobiol. Sci., 2006, 1045–51.

    Google Scholar 

  53. E. R. Bittner, Lattice theory of ultrafast excitonic and charge transfer dynamics in DNA, J. Chem. Phys., 2006, 125 1–12, 094909.

    Article  PubMed  CAS  Google Scholar 

  54. M. Riley, B. Maling and M. J. Chamberling, Physical and chemical characterization of two- and three-stranded adenine–thymine and adenine–uracil homopolymer complexes, J. Mol. Biol., 1966, 20, 359–89.

    Article  CAS  PubMed  Google Scholar 

  55. P. O. P. Ts’o, A. Seymour, S. A. Rapaport and F. J. Bollum, A comparative study of polydeoxyribonucleotides and polyribonucleotides by optical rotatory dispersion, Biochemistry, 1966, 5, 4153–70.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire Francis Perrin, CEA/DSM/DRECAM/SPAM-CNRS URA 2453, CEA/Saclay, 91191, Gif-sur-Yvette, France

    Dimitra Markovitsi, Thomas Gustavsson & Francis Talbot

Authors
  1. Dimitra Markovitsi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Gustavsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francis Talbot
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Markovitsi, D., Gustavsson, T. & Talbot, F. Excited states and energy transfer among DNA bases in double helices. Photochem Photobiol Sci 6, 717–724 (2007). https://doi.org/10.1039/b705674e

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b705674e

Search

Navigation