Plants collect light for photosynthesis using light-harvesting complexes (LHCs)-an array of chlorophyll proteins that are able to reversibly switch from harvesting to energy-dissipation mode to prevent damage of the photosynthetic apparatus. LHC antennae as well as other members of the LHC superfamily evolved from cyanobacterial ancestors called high light-inducible proteins (Hlips). Here, we characterized a purified Hlip family member HliD isolated from the cyanobacterium Synechocystis sp. PCC 6803. We found that the HliD binds chlorophyll-a (Chl-a) and β-carotene and exhibits an energy-dissipative conformation. Using femtosecond spectroscopy, we demonstrated that the energy dissipation is achieved via direct energy transfer from a Chl-a Qy state to the β-carotene S1 state. We did not detect any cation of β-carotene that would accompany Chl-a quenching. These results provide proof of principle that this quenching mechanism operates in the LHC superfamily and also shed light on the photoprotective role of Hlips and the evolution of LHC antennae.

] Faculty of Science University of South Bohemia České Budějovice Czech Republic [2] Biology Centre Institute of Plant Molecular Biology Academy of Sciences of the Czech Republic České Budějovice Czech Republic

] Faculty of Science University of South Bohemia České Budějovice Czech Republic [2] Institute of Microbiology Academy of Sciences of the Czech Republic Třeboň Czech Republic

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Komentář v

Nat Chem Biol. 2015 Apr;11(4):242-3. doi: 10.1038/nchembio.1771. PubMed

Zobrazit více v PubMed

Nature. 2007 Nov 22;450(7169):575-8 PubMed

Science. 2005 Jan 21;307(5708):433-6 PubMed

Proc Natl Acad Sci U S A. 2009 Jul 28;106(30):12311-6 PubMed

Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2364-9 PubMed

J Biol Chem. 2011 Apr 29;286(17):14812-9 PubMed

J Biol Chem. 2007 Jan 5;282(1):267-76 PubMed

J Biol Chem. 2004 Jul 2;279(27):27971-9 PubMed

Biochim Biophys Acta. 2004 Jul 9;1657(2-3):82-104 PubMed

Eur J Biochem. 1999 Mar;260(2):453-60 PubMed

PLoS Biol. 2011 Jan 18;9(1):e1000577 PubMed

Plant Cell. 2014 Mar;26(3):1200-12 PubMed

Plant Cell. 2014 Mar;26(3):1267-79 PubMed

PLoS One. 2012;7(1):e29700 PubMed

Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13516-21 PubMed

Plant Physiol. 2009 Feb;149(2):1076-86 PubMed

Chem Rev. 2004 Apr;104(4):2021-71 PubMed

Photosynth Res. 2010 Nov;106(1-2):57-71 PubMed

EMBO J. 2005 Mar 9;24(5):919-28 PubMed

J Biol Chem. 2008 Feb 8;283(6):3550-8 PubMed

FEMS Microbiol Lett. 2002 Oct 8;215(2):209-19 PubMed

Plant Physiol. 2007 Apr;143(4):1802-16 PubMed

BMC Evol Biol. 2010 Jul 30;10:233 PubMed

Nature. 2004 Mar 18;428(6980):287-92 PubMed

Chemphyschem. 2010 Apr 26;11(6):1289-96 PubMed

Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):636-40 PubMed

J Biol Chem. 2007 Dec 28;282(52):37660-8 PubMed

J Biol Chem. 2001 Jan 5;276(1):306-14 PubMed

Nat Struct Mol Biol. 2011 Mar;18(3):309-15 PubMed

J Phys Chem B. 2012 Mar 29;116(12):3834-49 PubMed

Biophys J. 2009 Mar 18;96(6):2261-7 PubMed

Mol Cell Proteomics. 2007 Jul;6(7):1215-25 PubMed

Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16721-5 PubMed

The biogenesis and maintenance of PSII: Recent advances and current challenges

Assembly of D1/D2 complexes of photosystem II: Binding of pigments and a network of auxiliary proteins

Psb34 protein modulates binding of high-light-inducible proteins to CP47-containing photosystem II assembly intermediates in the cyanobacterium Synechocystis sp. PCC 6803

High-light-inducible proteins HliA and HliB: pigment binding and protein-protein interactions

Electronic and Vibrational Properties of Allene Carotenoids

Plant LHC-like proteins show robust folding and static non-photochemical quenching

Trivial Excitation Energy Transfer to Carotenoids Is an Unlikely Mechanism for Non-photochemical Quenching in LHCII

A Protein Environment-Modulated Energy Dissipation Channel in LHCII Antenna Complex

A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly

Sequential deletions of photosystem II assembly factors Ycf48, Ycf39 and Pam68 result in progressive loss of autotrophy in the cyanobacterium Synechocystis PCC 6803

Photoprotective strategies in the motile cryptophyte alga Rhodomonas salina-role of non-photochemical quenching, ions, photoinhibition, and cell motility

The antenna-like domain of the cyanobacterial ferrochelatase can bind chlorophyll and carotenoids in an energy-dissipative configuration

Plant and algal chlorophyll synthases function in Synechocystis and interact with the YidC/Alb3 membrane insertase

Binding of pigments to the cyanobacterial high-light-inducible protein HliC

On the origin of the slow M-T chlorophyll a fluorescence decline in cyanobacteria: interplay of short-term light-responses

Molecular Origin of Photoprotection in Cyanobacteria Probed by Watermarked Femtosecond Stimulated Raman Spectroscopy

Twisting a β-Carotene, an Adaptive Trick from Nature for Dissipating Energy during Photoprotection

Ultrafast spectroscopy tracks carotenoid configurations in the orange and red carotenoid proteins from cyanobacteria

A method to decompose spectral changes in Synechocystis PCC 6803 during light-induced state transitions

Single Molecule Spectroscopy of Monomeric LHCII: Experiment and Theory