Elucidation of structure-function relationships in photosynthetic light-harvesting antenna complexes by non-linear polarization spectroscopy in the frequency domain (NLPF)

Journal of Plant Physiology

Volumn 168, Issue 12, 2011, Pages 1488-1496

  Lokstein, Heiko ^a   Krikunova, Maria ^b   Teuchner, Klaus ^a   Voigt, Bernd ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Excitonic interactions; Laser spectroscopy; Light harvesting complex; Nonlinear polarization spectroscopy in the frequency domain; Pigment pigment interactions

Indexed keywords

PIGMENT;

CHEMISTRY; LIGHT HARVESTING SYSTEM; METABOLISM; METHODOLOGY; NONLINEAR SYSTEM; PHOTOSYNTHESIS; REVIEW; SPECTROSCOPY; STRUCTURE ACTIVITY RELATION;

LIGHT-HARVESTING PROTEIN COMPLEXES; NONLINEAR DYNAMICS; PHOTOSYNTHESIS; PIGMENTS, BIOLOGICAL; SPECTRUM ANALYSIS; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS);

EID: 79958765148     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2010.12.012     Document Type: Review

References (62)

1. Beenken W., May V. Strong field theory of nonlinear polarization spectroscopy. Fundamentals and the two-level system. J Opt Soc Am B 1997, 14:2804-2810.
2. Beenken W., Ehlert J. Subband analysis of molecular electronic transitions by nonlinear polarization spectroscopy in the frequency domain. J Chem Phys 1998, 109:10126-10137.
3. Bode S., Quentmeier C.C., Liao P.-N., Hafi N., Barros T., Wilk L., Bittner F., Walla P.J. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 2009, 106:12311-12316.
4. Damjanovic A., Ritz T., Schulten K. Excitation transfer in the peridinin-chlorophyll-protein of Amphidinium carterae. Biophys J 2000, 79:1695-1705.
5. Photosynthetic protein complexes: a structural approach 2008, Wiley-VCH, Weinheim. P. Fromme (Ed.).
6. Advances in photosynthesis and respiration, chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications 2006, vol. 25. Springer, Dordrecht.
7. Gruszecki W.I., Luchowski R., Zubik M., Grudzinski W., Janik E., Gospodarek M., Goc J., Gryczynski Z., Gryczynski I. Blue-light-controlled photoprotection in plants at the level of the photosynthetic antenna complex LHCII. J Plant Physiol 2010, 167:69-73.
8. Härtel H., Lokstein H., Grimm B., Rank B. Kinetic studies on the xanthophyll cycle in barley leaves: influence of antenna size and relations to nonphotochemical chlorophyll fluorescence quenching. Plant Physiol 1996, 110:471-482.
9. Hofmann E., Wrench P.M., Sharples F.P., Hiller R.G., Welte W., Diederichs K. Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 1996, 272:1788-1791.
10. Humphrey W., Dalke A., Schulten K. VMD - visual molecular dynamics. J Mol Graphics 1996, 14:33-38.
11. Ilagan R.P., Shima S., Melkozernov A., Lin S., Blankenship R.E., Sharples F.P., Hiller R.G., Birge R.R., Frank H.A. Spectroscopic properties of the main-form and high-salt peridinin-chlorophyll a proteins from Amphidinium carterae. Biochemistry 2004, 43:1478-1487.
12. Jansson S. The light harvesting chlorophyll a/b binding proteins. Biochim Biophys Acta 1994, 1184:1-19.
13. Kleima F.J., Wendling M., Hofmann E., Peterman E.J.G., van Grondelle R., van Amerongen H. Peridinin chlorophyll a protein: relating structure steady-state spectroscopy. Biochemistry 2000, 39:5184-5195.
14. Krikunova M., Voigt B., Lokstein H. Direct evidence for excitonically coupled chlorophylls a and b in LHC II of higher plants by non-linear polarization spectroscopy in the frequency domain. Biochim Biophys Acta 2002, 1556:1-5.
15. Krikunova M., Kummrow A., Voigt B., Rini M., Lokstein H., Moskalenko A., Scheer H., Razjivin A., Leupold D. Fluorescence of native and carotenoid-depleted LH2 from Chromatium minutissimum, originating from simulataneous two-photon absorption in the spectral range of the presumed (optically "dark") S1 state of carotenoids. FEBS Lett 2002, 528:227-229.
16. Krikunova M., Lokstein H., Leupold D., Hiller R.G., Voigt B. Pigment-pigment interactions in PCP of Amphidinium carterae investigated by non-linear polarization spectroscopy in the frequency domain. Biophys J 2006, 90:261-271.
17. Krueger B.P., Lampoura S.S., van Stokkum I.H.M., Papagiannakis E., Salverda J.M., Gradinaru C.C., Rutkauskas D., Hiller R.G., van Grondelle R. Energy transfer in the peridinin chlorophyll-a protein of Amphidinium carterae studied by polarized transient absorption and target analysis. Biophys J 2001, 80:2843-2855.
18. Kühlbrandt W., Wang D.N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 1994, 367:614-621.
19. Leupold D., Voigt B., Pfeiffer M., Bandilla K., Scheer H. Nonlinear polarization spectroscopy (frequency domain) studies of excited state processes: the B800-850 antenna of Rhodobacter sphaeroides. Photochem Photobiol 1993, 57:24-28.
20. Leupold D., Neef E., Voigt B., Nowak F., Ehlert J., Bandilla M., Scheer H. Substructure analysis of the bacterial antenna LH II by nonlinear polarization spectroscopy in the frequency domain. Lietuvos fizikos zurnalas (Lithuanian Journal of Physics) 1994, 34:339-343.
21. Leupold D. Photobiological application of non-linear UV/vis-spectroscopic techniques, exemplified at primary processes of bacterial photosynthesis. Photochem Photobiol 1995, 62:984-996.
22. Leupold D., Stiel H., Teuchner K., Nowak F., Sandner W., Ücker B., Scheer H. Size enhancement of transition dipoles to one- and two exciton bands in a photosynthetic antenna. Phys Rev Lett 1996, 77:4675-4678.
23. Leupold D., Stiel H., Ehlert J., Nowak F., Teuchner K., Voigt B., Bandilla M., Ücker B., Scheer H. Photophysical characterization of the pure light harvesting antenna B850 of Rb. sphaeroides. Implications to ultrafast energy transfer 800-850nm. Chem Phys Lett 1999, 301:537-545.
24. Leupold D., Voigt B., Beenken W., Stiel H. Pigment-protein architecture in the light harvesting antenna complexes of purple bacteria: does the crystal structure reflect the native pigment-protein arrangement?. FEBS Lett 2000, 480:73-78.
25. Leupold D., Teuchner K., Ehlert J., Irrgang K.-D., Renger G., Lokstein H. Two-photon excited fluorescence from higher electronic states of chlorophylls in photosynthetic antenna complexes: a new approach to detect strong excitonic chlorophyll a/b coupling. Biophys J 2002, 82:1580-1585.
26. Leupold D., Lokstein H., Scheer H. Excitation energy transfer between (bacterio) chlorophylls - the role of excitonic coupling. Advances in photosynthesis and respiration, chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications 2006, 25:413-430. Springer, Dordrecht.
27. Leupold D., Teuchner K., Ehlert J., Irrgang K.-D., Renger G., Lokstein H. Stepwise two-photon excited fluorescence from higher excited states of chlorophylls in photosynthetic antenna complexes. J Biol Chem 2006, 281:25381-25387.
28. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., Chang W. Crystal structure of spinach major light-harvesting complex at 2.72Å resolution. Nature 2004, 428:287-292.
29. Lokstein H., Härtel H., Hoffmann P., Renger G. Comparison of chlorophyll fluorescence quenching in leaves of wild-type with a chlorophyll-b-less mutant of barley (Hordeum vulgare L.). J Photochem Photobiol B: Biol 1993, 19:217-225.
30. Lokstein H., Härtel H., Hoffmann P., Woitke P., Renger G. The role of light-harvesting complex II in excess excitation dissipation: an in-vivo fluorescence study on the origin of high-energy quenching. J Photochem Photobiol B: Biol 1994, 26:175-184.
31. Lokstein H., Leupold D., Voigt B., Nowak F., Ehlert J., Hoffmann P., Garab G. Nonlinear polarization spectroscopy in the frequency domain of light-harvesting complex II: absorption band substructure and exciton dynamics. Biophys J 1995, 69:1536-1543.
32. Lokstein H., Leupold D., Voigt B., Nowak F., Ehlert J., Hoffmann P. Nonlinear polarization spectroscopy in the frequency doma Spectral substructure ultrafast exciton dynamics in light-harvesting complex. Photosynthesis: from light to biosphere 1995, vol. I:287-290. Kluwer Academic Publishers, Dordrecht.
33. Lokstein H., Schubert A., Voigt B., Leupold D. Direct resolution of spectral fine-structure and ultrafast exciton dynamics in light-harvesting complex II by non-linear polarization spectroscopy in the frequency domain. Photosynthesis: mechanisms and effects 1998, vol. I:293-296. Kluwer Academic Publishers, Dordrecht.
34. Lokstein H., Tian L., Polle J., DellaPenna D. Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim Biophys Acta 2002, 1553:93-103.
35. Lokstein H, Grimm B Chlorophyll binding protein. Handbook of plant science 2007, vol. I:1180-1187. J. Wiley & Sons, also In: Encyclopedia of life sciences: Wiley; 2007. p. 1-8. doi: 10.1002/9780470015902.a0020085.
36. Marcano O.A., Marquez L., Aranguren L., Salazar M. Polarization spectra of homogeneously and inhomogeneously broadened two-level systems. J Opt Soc Am B 1990, 7:2145-2149.
37. Mikhailyuk I.K., Lokstein H., Razjivin A.P. A method of spectral subband decomposition by simultaneous fitting the initial spectrum and a set of its derivatives. J Biochem Biophys Methods 2005, 63:9-22.
38. Neef E., Mory S. Content of information of nonlinear polarization spectroscopy. Exp Techn Physik 1991, 39:385-388.
39. Nowak F., Voigt B., Leupold D., Bandilla M., Scheer H., Cogdell R.J. Room temperature investigation of the LH2 antenna of Rb. sphaeroides and Rps. acidophila by non-linear polarization spectroscopy in the frequency domain. Photosynthesis from Light to Biosphere Vol I 1995, 151-154. Kluwer Academic Publishers. P. Mathis (Ed.).
40. Pieper J., Irrgang K.-D., Rätsep M., Voigt J., Renger G., Small G.J. Assignment of the lowest Qy-state and spectral dynamics of the CP29 chlorophyll a/b antenna complex of green plants: a hole-burning study. Photochem Photobiol 2000, 71:574-581.
41. Polivka T., Sundström V. Ultrafast dynamics of carotenoid excited states - from solution to natural and artificial systems. Chem Rev 2004, 104:2021-2071.
42. Rogl H., Schödel R., Lokstein H., Kühlbrandt W., Schubert A. Assignment of spectral substructures to pigment-binding sites in higher plant light-harvesting complex LHC-II. Biochemistry 2002, 41:2281-2287.
43. Ruban A.V., Berera R., Ilioaia C., van Stokkum I.H.V., Kennis J.T.M., Pascal A.A., van Amerongen H., Robert B., Horton P., van Grondelle R. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 2007, 450:575-579.
44. Saikan S., Sei J. Experimental studies of polarization spectroscopy in dye solutions. J Phys Chem 1983, 79:4146-4153.
45. Schlau-Cohen G.S., Calhoun T.R., Ginsberg N.S., Ballottari M., Bassi R., Fleming G.R. Spectroscopic elucidation of uncoupled transition energies in the major photosynthetic light-harvesting complex, LHCII. Proc Natl Acad Sci USA 2010, 107:13276-13281.
46. Schubert A., Voigt B., Leupold D., Beenken W., Ehlert J., Hoffmann P., Lokstein H. Direct observation of spectral substructure in the Qy-absorption band of light-harvesting complex II by nonlinear polarization spectroscopy in the frequency domain at low temperature. Biochim Biophys Acta 1997, 1321:195-199.
47. Schubert A., Krikunova M.A., Stiel H., Ehlert J., Leupold D., Lokstein H. Determination of the aggregate size in chlorophyll a oligomers by non-linear absorption spectroscopy on the ps and fs timescale. Photosynthesis: mechanisms and effects 1998, vol. I:469-472. Kluwer Academic Publishers, Dordrecht.
48. Schubert A., Beenken W., Stiel H., Voigt B., Leupold D., Lokstein H. Excitonic coupling of chlorophylls in the plant light-harvesting complex LHC-II. Biophys J 2002, 82:1030-1039.
49. Shima S., Ilagan R.P., Gillespie N., Sommer B.J., Hiller R.G., Sharples F.P., Frank H.A., Birge R.R. Two-photon and fluorescence spectroscopy and the effect of environment on the photochemical properties of peridinin in solution and in the peridinin-chlorophyll-protein from Amphidinium carterae. J Phys Chem A 2003, 108:8052-8066.
50. Song J.J., Lee J.H., Levenson M.D. Picosecond relaxation measurements by polarization spectroscopy in condensed phases. Phys Rev A 1978, 17:1439-1447.
51. Standfuss J., Terwischa van Scheltinga A.C., Lamborghini M., Kühlbrandt W. Mechanism of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5Å resolution. EMBO J 2005, 24:919-928.
52. Stiel H., Voigt B., Hirsch J., Teuchner K., Leupold D. One and biexcitonic states in J-aggregates of pseudoisocyanin studied by nonlinear polarization and nonlinear absorption spectroscopy. Adv Mater 1995, 7:445-448.
53. Stiel H., Leupold D., Teuchner K., Nowak F., Scheer H., Cogdell R.J. One- and two-exciton bands in the LH2 antenna of Rhodopseudomonas acidophila. Chem Phys Lett 1997, 276:62-69.
54. Theiss C., Leupold D., Moskalenko A.A., Razjivin A.P., Eichler H.J., Lokstein H. Femtosecond transient absorption spectroscopy of native and carotenoid-less purple bacterial LH2 clarifies functions of carotenoids. Biophys J 2008, 94:4808-4811.
55. Voigt B., Nowak F., Ehlert J., Beenken W., Leupold D., Sandner W. Substructures and different energy relaxation times within the first electronic transition of pinacyanol. Chem Phys Lett 1997, 278:380-390.
56. Voigt B., Nowak F.R., Beenken W. A new set-up for nonlinear polarization spectroscopy in the frequency domain: experimental examples and theoretical background. Meas Sci Technol 1999, 10:N7-N11.
57. Voigt B., Irrgang K.D., Ehlert J., Beenken W., Renger G., Leupold D., Lokstein H. Spectral substructure and excitonic interactions in the minor photosystem II antenna complex CP29 as revealed by non-linear polarization spectroscopy in the frequency domain. Biochemistry 2002, 41:3049-3056.
58. Voigt B., Krikunova M., Lokstein H. Influence of detergent concentration on aggregation and the spectroscopic properties of light-harvesting complex II. Photosynth Res 2008, 95:317-325.
59. Wörmke S., Mackowski S., Brotosudarmo T.H.P., Jung C., Zumbusch A., Ehrl M., Scheer H., Hofmann E., Hiller R.G., Bräuchle C. Monitoring fluorescence of individual chromophores in peridinin-chlorophyll-protein complex using single molecule spectrsocopy. Biochim Biophys Acta 2007, 1767:956-964.
60. Yan H., Zhang P., Wang C., Liu Z., Chang W. Two lutein molecules in LHCII have different conformations and functions: Insights into the molecular mechanism of thermal dissipation in plants. Biochem Biophys Res Commun 2007, 355:457-463.
61. Zigmantas D., Hiller R.G., Sundström V., Polivka T. Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc Natl Acad Sci USA 2002, 99:16760-16765.
62. Zigmantas D., Hiller R.G., Sharples F.P., Frank H.A., Sundström V., Polivka T. Effect of a conjugated carbonyl group on the photophysical properties of carotenoids. Phys Chem Chem Phys 2004, 6. 3009-2016.