Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein

Energy-dependent quenching of excess absorbed light energy (qE) is a vital mechanism for regulating photosynthetic light harvesting in higher plants. All of the physiological characteristics of qE have been positively correlated with charge transfer between coupled chlorophyll and zeaxanthin molecules in the light-harvesting antenna of photosystem II (PSII). We found evidence for charge-transfer quenching in all three of the individual minor antenna complexes of PSII (CP29, CP26, and CP24), and we conclude that charge-transfer quenching in CP29 involves a delocalized state of an excitonically coupled chlorophyll dimer. We propose that reversible conformational changes in CP29 can “tune” the electronic coupling between the chlorophylls in this dimer, thereby modulating the energy of the chlorophyll-zeaxanthin charge-transfer state and switching on and off the charge-transfer quenching during qE.

[1]  E. Bergantino,et al.  Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. , 2007, Biochimica et biophysica acta.

[2]  T. Moore,et al.  The design and synthesis of artificial photosynthetic antennas, reaction centres and membranes. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  R. Grondelle,et al.  Understanding the Energy Transfer Function of LHCII, the Major Light-Harvesting Complex of Green Plants† , 2001 .

[4]  Stefan Jansson,et al.  A pigment-binding protein essential for regulation of photosynthetic light harvesting , 2000, Nature.

[5]  C. Külheim,et al.  Rapid Regulation of Light Harvesting and Plant Fitness in the Field , 2002, Science.

[6]  K. Niyogi,et al.  PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. , 1999, Annual review of plant physiology and plant molecular biology.

[7]  Leonas Valkunas,et al.  Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting , 2005, Science.

[8]  P. Horton,et al.  Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness. , 2003, The Plant journal : for cell and molecular biology.

[9]  Stefan Jansson,et al.  Lack of the Light-Harvesting Complex CP24 Affects the Structure and Function of the Grana Membranes of Higher Plant Chloroplasts[OA] , 2006, The Plant Cell Online.

[10]  T. Morosinotto,et al.  Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids , 2003 .

[11]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[12]  K. Niyogi,et al.  Regulation of Photosynthetic Light Harvesting Involves Intrathylakoid Lumen pH Sensing by the PsbS Protein* , 2004, Journal of Biological Chemistry.

[13]  J. Vivanco,et al.  ‡ To whom correspondence should be addressed: , 2022 .

[14]  Graham R. Fleming,et al.  Zeaxanthin Radical Cation Formation in Minor Light-harvesting Complexes of Higher Plant Antenna* , 2008, Journal of Biological Chemistry.

[15]  W. Kühlbrandt,et al.  Two-dimensional structure of plant photosystem II at 8-Å resolution , 1997, Nature.

[16]  J. Briantais,et al.  A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. , 1979, Biochimica et biophysica acta.

[17]  T. Moore,et al.  A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[19]  Zhenfeng Liu,et al.  Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution , 2004, Nature.

[20]  D. Cugini,et al.  Mutational analysis of a higher plant antenna protein provides identification of chromophores bound into multiple sites. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Kennis,et al.  Identification of a mechanism of photoprotective energy dissipation in higher plants , 2007, Nature.

[22]  R. Bassi,et al.  Energy transfer among CP29 chlorophylls: calculated Förster rates and experimental transient absorption at room temperature. , 2000, Biophysical journal.

[23]  P. Horton,et al.  Antisense Inhibition of the Photosynthetic Antenna Proteins CP29 and CP26: Implications for the Mechanism of Protective Energy Dissipation , 2001, Plant Cell.

[24]  W. Kühlbrandt,et al.  Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis. , 2007, The journal of physical chemistry. B.

[25]  R. Bassi,et al.  Interactions between the Photosystem II Subunit PsbS and Xanthophylls Studied in Vivo and in Vitro* , 2008, Journal of Biological Chemistry.

[26]  J. Botto,et al.  The plant cell , 2007, Plant Molecular Biology Reporter.

[27]  J. Barber,et al.  Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Barbara Demmig-Adams,et al.  Carotenoids and photoprotection in plants : a role for the xanthophyll zeaxanthin , 1990 .

[29]  M. Head‐Gordon,et al.  Chlorophyll fluorescence quenching by xanthophylls , 2003 .

[30]  J. P. Connelly,et al.  Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. , 1997, Biochemistry.

[31]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.