Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants
Abstract
Photosynthetic antenna proteins can be thought of as “programmed solvents”, which bind pigments at specific mutual orientations, thus tuning the overall energetic landscape and ensuring highly efficient light-harvesting. While positioning of chlorophyll cofactors is well understood and rationalized by the principle of an “energy funnel”, the carotenoids still pose many open questions. Particularly, their short excited state lifetime (<25 ps) renders them potential energy sinks able to compete with the reaction centers and drastically undermine light-harvesting efficiency. Exploration of the orientational phase-space revealed that the placement of central carotenoids minimizes their interaction with the nearest chlorophylls in the plant antenna complexes LHCII, CP26, CP29 and LHCI. At the same time we show that this interaction is highly sensitive to structural perturbations, which has a profound effect on the overall lifetime of the complex. This links the protein dynamics to the light-harvesting regulation in plants by the carotenoids.
- Authors:
-
[1];
[1];
[3];
[1]
- Queen Mary Univ. of London (United Kingdom)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Univ. of Pisa (Italy)
- Federal Univ. of Lavras (Brazil); Military Inst. of Engineering, Rio de Janeiro (Brazil)
- Publication Date:
- Research Org.:
- Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1500050
- Grant/Contract Number:
- SC0001035
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Balevičius, Vytautas, Fox, Kieran F., Bricker, William P., Jurinovich, Sandro, Prandi, Ingrid G., Mennucci, Benedetta, and Duffy, Christopher D. P. Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants. United States: N. p., 2017.
Web. doi:10.1038/s41598-017-13720-6.
Balevičius, Vytautas, Fox, Kieran F., Bricker, William P., Jurinovich, Sandro, Prandi, Ingrid G., Mennucci, Benedetta, & Duffy, Christopher D. P. Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants. United States. https://doi.org/10.1038/s41598-017-13720-6
Balevičius, Vytautas, Fox, Kieran F., Bricker, William P., Jurinovich, Sandro, Prandi, Ingrid G., Mennucci, Benedetta, and Duffy, Christopher D. P. Tue .
"Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants". United States. https://doi.org/10.1038/s41598-017-13720-6. https://www.osti.gov/servlets/purl/1500050.
@article{osti_1500050,
title = {Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants},
author = {Balevičius, Vytautas and Fox, Kieran F. and Bricker, William P. and Jurinovich, Sandro and Prandi, Ingrid G. and Mennucci, Benedetta and Duffy, Christopher D. P.},
abstractNote = {Photosynthetic antenna proteins can be thought of as “programmed solvents”, which bind pigments at specific mutual orientations, thus tuning the overall energetic landscape and ensuring highly efficient light-harvesting. While positioning of chlorophyll cofactors is well understood and rationalized by the principle of an “energy funnel”, the carotenoids still pose many open questions. Particularly, their short excited state lifetime (<25 ps) renders them potential energy sinks able to compete with the reaction centers and drastically undermine light-harvesting efficiency. Exploration of the orientational phase-space revealed that the placement of central carotenoids minimizes their interaction with the nearest chlorophylls in the plant antenna complexes LHCII, CP26, CP29 and LHCI. At the same time we show that this interaction is highly sensitive to structural perturbations, which has a profound effect on the overall lifetime of the complex. This links the protein dynamics to the light-harvesting regulation in plants by the carotenoids.},
doi = {10.1038/s41598-017-13720-6},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {Tue Oct 24 00:00:00 EDT 2017},
month = {Tue Oct 24 00:00:00 EDT 2017}
}
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Figure 1: Mutual orientation of Cars and their closest co-facial Chl partners in the L1/L2 sites. (a–c) Positioning of Lhcb1 within the membrane (PDB: 3JCU)9. The views are along the membrane plane (a,b) and from the stromal side (c). A close-up view of the L1/L2 sites in b shows themore »
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Excited-State Kinetics of the Carotenoid S 1 State in LHC II and Two-Photon Excitation Spectra of Lutein and β-Carotene in Solution: Efficient Car S 1 →Chl Electronic Energy Transfer via Hot S 1 States? †
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Chlorophyll Triplet Quenching and Photoprotection in the Higher Plant Monomeric Antenna Protein Lhcb5
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On the Photophysics of Carotenoids: A Multireference DFT Study of Peridinin
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Efficient Pathways of Excitation Energy Transfer from Delocalized S 2 Excitons in the Peridinin–Chlorophyll a –Protein Complex
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Molecular Dynamics Simulations of the Dynamic and Energetic Properties of Alkali and Halide Ions Using Water-Model-Specific Ion Parameters
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Atomic model of plant light-harvesting complex by electron crystallography
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Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state
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Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
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Molecular basis of photoprotection and control of photosynthetic light-harvesting
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Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution
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Quantum design of photosynthesis for bio-inspired solar-energy conversion
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Natural strategies for photosynthetic light harvesting
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Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps
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Photoprotection and triplet energy transfer in higher plants: the role of electronic and nuclear fluctuations
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Comparison of simple potential functions for simulating liquid water
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Thermodynamic Investigation into the Mechanism of the Chlorophyll Fluorescence Quenching in Isolated Photosystem II Light-harvesting Complexes
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