A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

doi:10.1073/pnas.0508530103

A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

^†Department of Biophysics, Division of Physics and Astronomy, Faculty of Sciences, Vrije Universiteit, 1081 HV, Amsterdam, The Netherlands;
^‡Department of Chemistry and Biochemistry and Center for the Study of Early Events in Photosynthesis, Arizona State University, Tempe, AZ 85287; and
^§Laboratory for Biophysics, Wageningen University, 6703 HA, Wageningen, The Netherlands

Edited by Robin M. Hochstrasser, University of Pennsylvania, Philadelphia, PA, and approved February 10, 2006 (received for review September 29, 2005)

Abstract

Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of nonphotochemical quenching has been linked to the conversion of a carotenoid with a conjugation length of nine double bonds (violaxanthin) into an 11-double-bond carotenoid (zeaxanthin). It has been suggested that the increase in the conjugation length turns the carotenoid from a nonquencher into a quencher of chlorophyll singlet excited states, but unequivocal evidence is lacking. Here, we present a transient absorption spectroscopic study on a model system made up of a zinc phthalocyanine (Pc) molecule covalently linked to carotenoids with 9, 10, or 11 conjugated carbon–carbon double bonds. We show that a carotenoid can act as an acceptor of Pc excitation energy, thereby shortening its singlet excited-state lifetime. The conjugation length of the carotenoid is critical to the quenching process. Remarkably, the addition of only one double bond can turn the carotenoid from a nonquencher into a very strong quencher. By studying the solvent polarity dependence of the quenching using target analysis of the time-resolved data, we show that the quenching proceeds through energy transfer from the excited Pc to the optically forbidden S₁ state of the carotenoid, coupled to an intramolecular charge-transfer state. The mechanism for excess energy dissipation in photosystem II is discussed in view of the insights obtained on this simple model system.

Footnotes

^¶To whom correspondence should be addressed. E-mail: j.kennis{at}few.vu.nl
Author contributions: H.v.A., R.v.G., D.G., T.A.M., A.L.M., and J.T.M.K. designed research; R.B., M.V., G.K., and R.E.P. performed research; C.H., D.G., T.A.M., and A.L.M. contributed new reagents/analytic tools; R.B., I.H.M.v.S., and J.T.M.K. analyzed data; and R.B., D.G., T.A.M., A.L.M., and J.T.M.K. wrote the paper.
Conflict of interest statement: No conflicts declared.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations:

Abbreviations:

EADS,

evolution-associated difference spectrum;

SADS,

species-associated difference spectrum;

Pc,

phthalocyanine;

ICT,

intramolecular charge transfer;

Chl,

chlorophyll;

PSII,

photosystem II;

THF,

tetrahydrofuran;

LHC,

light-harvesting complex.
Freely available online through the PNAS open access option.