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Title: 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:
ORCiD logo [1]; ORCiD logo [1];  [2];  [3];  [4]; ORCiD logo [3]; ORCiD logo [1]
  1. Queen Mary Univ. of London (United Kingdom)
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  3. Univ. of Pisa (Italy)
  4. 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. doi: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. doi: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 = {2017},
month = {10}
}

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Cited by: 24 works
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Figures / Tables:

Figure 1 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 » pigment pairs and the naming nomenclature according to Liu et al.7. Transmembrane helices A, B, C and amphipathic helices D and E are shown in light-blue. The remaining pigment composition of Lhcb1 is shown in c: 8 Chl a’s are shown in green, 6 Chl b’s are in red, Vio and neoxanthin are shown in pink and yellow, accordingly (molecules and proteins plotted with VMD31). (d) The full trimer of the LHCII antenna (lumenal view). Monomers are emphasized by colors. (e,f) Superposition of all the L1 and L2 pairs from Lhcb1-5 and Lhca1-4 protein units. The front view (e) and the side view (f) also show the coordinate system associated with the Chl. Cars are shown as ghost atoms to emphasize the distribution rather than the actual positions, except for Lut 620 from L1 site of Lhcb1 which is highlighted for comparison. Only Chl a612 from the L1 site of Lhcb1 represents all the Chls for clarity because the other Chls from the pairs largely differ only by the conformation of their phytol tails, which do not contribute to the transition density (Supplementary Fig. 1a).« less

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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.