The major trimeric antenna complexes serve as a site for qH-energy dissipation in plants

Pierrick Bru; Collin J Steen; Soomin Park; Cynthia L Amstutz; Emily J Sylak-Glassman; Lam Lam; Agnes Fekete; Martin J Mueller; Fiamma Longoni; Graham R Fleming; Krishna K Niyogi; Alizée Malnoë

doi:10.1016/j.jbc.2022.102519

The major trimeric antenna complexes serve as a site for qH-energy dissipation in plants

J Biol Chem. 2022 Nov;298(11):102519. doi: 10.1016/j.jbc.2022.102519. Epub 2022 Sep 22.

Authors

Affiliations

¹ Department of Plant Physiology, Umeå Plant Science Centre (UPSC), Umeå University, Umeå, Sweden.
² Department of Chemistry, University of California, Berkeley, California, USA; Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA; Kavli Energy Nanoscience Institute, Berkeley, California, USA.
³ Department of Chemistry, University of California, Berkeley, California, USA; Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA; Kavli Energy Nanoscience Institute, Berkeley, California, USA; School of Energy, Materials and Chemical Engineering, Korea University of Technology and Education, Cheonan, Chungnam, Republic of Korea.
⁴ Department of Plant and Microbial Biology, Howard Hughes Medical Institute, University of California, Berkeley, California, USA.
⁵ Department of Chemistry, University of California, Berkeley, California, USA; Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA.
⁶ Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA; Kavli Energy Nanoscience Institute, Berkeley, California, USA; Graduate Group in Biophysics, University of California, Berkeley, California, USA.
⁷ Julius-von-Sachs-Institute, Biocenter, Pharmaceutical Biology, University of Wuerzburg, Wuerzburg, Germany.
⁸ Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
⁹ Department of Chemistry, University of California, Berkeley, California, USA; Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA; Kavli Energy Nanoscience Institute, Berkeley, California, USA; Graduate Group in Biophysics, University of California, Berkeley, California, USA.
¹⁰ Molecular Biophysics and Integrated Bioimaging Division (Formerly Physical Biosciences Division), Lawrence Berkeley National Laboratory, Berkeley, California, USA; Department of Plant and Microbial Biology, Howard Hughes Medical Institute, University of California, Berkeley, California, USA.
¹¹ Department of Plant Physiology, Umeå Plant Science Centre (UPSC), Umeå University, Umeå, Sweden. Electronic address: alizee.malnoe@umu.se.

Abstract

Plants and algae are faced with a conundrum: harvesting sufficient light to drive their metabolic needs while dissipating light in excess to prevent photodamage, a process known as nonphotochemical quenching. A slowly relaxing form of energy dissipation, termed qH, is critical for plants' survival under abiotic stress; however, qH location in the photosynthetic membrane is unresolved. Here, we tested whether we could isolate subcomplexes from plants in which qH was induced that would remain in an energy-dissipative state. Interestingly, we found that chlorophyll (Chl) fluorescence lifetimes were decreased by qH in isolated major trimeric antenna complexes, indicating that they serve as a site for qH-energy dissipation and providing a natively quenched complex with physiological relevance to natural conditions. Next, we monitored the changes in thylakoid pigment, protein, and lipid contents of antenna with active or inactive qH but did not detect any evident differences. Finally, we investigated whether specific subunits of the major antenna complexes were required for qH but found that qH was insensitive to trimer composition. Because we previously observed that qH can occur in the absence of specific xanthophylls, and no evident changes in pigments, proteins, or lipids were detected, we tentatively propose that the energy-dissipative state reported here may stem from Chl-Chl excitonic interaction.

Keywords: Arabidopsis thaliana; CRISPR–Cas9; abiotic stress; energy dissipation; light-harvesting complexes; nonphotochemical quenching qH; photosynthesis; time-resolved fluorescence.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Chlorophyll* / chemistry
Light
Light-Harvesting Protein Complexes* / chemistry
Photosynthesis
Photosystem II Protein Complex* / chemistry
Plants* / chemistry
Thylakoids / chemistry
Xanthophylls / chemistry

Substances

Chlorophyll
Light-Harvesting Protein Complexes
Photosystem II Protein Complex
Xanthophylls