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

Rudi Berera, Christian Herrero, Ivo H M Van Stokkum, Mikas Vengris, Gerdenis Kodis, Rodrigo E. Palacios, Herbert Van Amerongen, Rienk Van Grondelle, John Devens Gust, Thomas A Moore, Ana L Moore, John T M Kennis

Research output: Contribution to journalArticle

106 Citations (Scopus)

Abstract

Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of non-photochemical 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.

Original languageEnglish
Pages (from-to)5343-5348
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume103
Issue number14
DOIs
Publication statusPublished - Apr 4 2006

Fingerprint

Photosynthesis
Carotenoids
Light
Photosystem II Protein Complex
Chlorophyll
Carbon
Energy Transfer
Lighting
Fluorescence

Keywords

  • Artificial photosynthesis
  • Carotenoid
  • Nonphotochemical quenching
  • Photoprotection
  • Xanthophyll cycle

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis. / Berera, Rudi; Herrero, Christian; Van Stokkum, Ivo H M; Vengris, Mikas; Kodis, Gerdenis; Palacios, Rodrigo E.; Van Amerongen, Herbert; Van Grondelle, Rienk; Gust, John Devens; Moore, Thomas A; Moore, Ana L; Kennis, John T M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 103, No. 14, 04.04.2006, p. 5343-5348.

Research output: Contribution to journalArticle

Berera, Rudi ; Herrero, Christian ; Van Stokkum, Ivo H M ; Vengris, Mikas ; Kodis, Gerdenis ; Palacios, Rodrigo E. ; Van Amerongen, Herbert ; Van Grondelle, Rienk ; Gust, John Devens ; Moore, Thomas A ; Moore, Ana L ; Kennis, John T M. / A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis. In: Proceedings of the National Academy of Sciences of the United States of America. 2006 ; Vol. 103, No. 14. pp. 5343-5348.
@article{e5cdf73922a740b6b1639c43c1711a05,
title = "A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis",
abstract = "Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of non-photochemical 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.",
keywords = "Artificial photosynthesis, Carotenoid, Nonphotochemical quenching, Photoprotection, Xanthophyll cycle",
author = "Rudi Berera and Christian Herrero and {Van Stokkum}, {Ivo H M} and Mikas Vengris and Gerdenis Kodis and Palacios, {Rodrigo E.} and {Van Amerongen}, Herbert and {Van Grondelle}, Rienk and Gust, {John Devens} and Moore, {Thomas A} and Moore, {Ana L} and Kennis, {John T M}",
year = "2006",
month = "4",
day = "4",
doi = "10.1073/pnas.0508530103",
language = "English",
volume = "103",
pages = "5343--5348",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "14",

}

TY - JOUR

T1 - A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

AU - Berera, Rudi

AU - Herrero, Christian

AU - Van Stokkum, Ivo H M

AU - Vengris, Mikas

AU - Kodis, Gerdenis

AU - Palacios, Rodrigo E.

AU - Van Amerongen, Herbert

AU - Van Grondelle, Rienk

AU - Gust, John Devens

AU - Moore, Thomas A

AU - Moore, Ana L

AU - Kennis, John T M

PY - 2006/4/4

Y1 - 2006/4/4

N2 - Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of non-photochemical 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.

AB - Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of non-photochemical 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.

KW - Artificial photosynthesis

KW - Carotenoid

KW - Nonphotochemical quenching

KW - Photoprotection

KW - Xanthophyll cycle

UR - http://www.scopus.com/inward/record.url?scp=33645785599&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33645785599&partnerID=8YFLogxK

U2 - 10.1073/pnas.0508530103

DO - 10.1073/pnas.0508530103

M3 - Article

VL - 103

SP - 5343

EP - 5348

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 14

ER -