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Photocatalytic plant LPOR forms helical lattices that shape membranes for chlorophyll synthesis

View ORCID ProfileHenry C. Nguyen, View ORCID ProfileArthur A. Melo, View ORCID ProfileJerzy Kruk, View ORCID ProfileAdam Frost, View ORCID ProfileMichal Gabruk
doi: https://doi.org/10.1101/2020.08.19.257774
Henry C. Nguyen
1Department of Biochemistry & Biophysics, Quantitative Biosciences Institute, University of California, San Francisco, San Francisco, CA, USA
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  • For correspondence: nguyen.henry.c@gmail.com adam.frost@ucsf.edu michal.gabruk@uj.edu.pl
Arthur A. Melo
1Department of Biochemistry & Biophysics, Quantitative Biosciences Institute, University of California, San Francisco, San Francisco, CA, USA
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Jerzy Kruk
2Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland
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Adam Frost
1Department of Biochemistry & Biophysics, Quantitative Biosciences Institute, University of California, San Francisco, San Francisco, CA, USA
3Chan Zuckerberg Biohub, San Francisco, CA, USA
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  • For correspondence: nguyen.henry.c@gmail.com adam.frost@ucsf.edu michal.gabruk@uj.edu.pl
Michal Gabruk
2Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland
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  • For correspondence: nguyen.henry.c@gmail.com adam.frost@ucsf.edu michal.gabruk@uj.edu.pl
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Abstract

Chlorophyll (Chl) biosynthesis, crucial to life on Earth, is tightly regulated because its precursors are phototoxic1. In flowering plants, the enzyme Light-dependent Protochlorophyllide OxidoReductase (LPOR) captures photons to catalyze the penultimate reaction: the reduction of a double-bond within protochlorophyllide (Pchlide) to generate chlorophyllide (Chlide)2,3. In darkness, LPOR oligomerizes to facilitate photon energy transfer and catalysis4,5. However, the complete 3D structure of LPOR, the higher-order architecture of LPOR oligomers, and the implications of these self-assembled states for catalysis, including how LPOR positions Pchlide and the cofactor NADPH, remain unknown. Here we report the atomic structure of LPOR assemblies by electron cryo-microscopy (cryoEM). LPOR polymerizes with its substrates into helical filaments around constricted lipid bilayer tubes. Portions of LPOR and Pchlide insert into the outer membrane leaflet, targeting the product, Chlide, to the membrane for the final reaction site of chlorophyll biosynthesis. In addition to its crucial photocatalytic role, we show that in darkness LPOR filaments directly shape membranes into high-curvature tubules with the spectral properties of the prolammelar body, whose light-triggered disassembly provides lipids for thylakoid assembly. Our structure of the catalytic site, moreover, challenges previously proposed reaction mechanisms6. Together, our results reveal a new and unexpected synergy between photosynthetic membrane biogenesis and chlorophyll synthesis in plants orchestrated by LPOR.

Competing Interest Statement

The authors have declared no competing interest.

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Posted August 23, 2020.
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Photocatalytic plant LPOR forms helical lattices that shape membranes for chlorophyll synthesis
Henry C. Nguyen, Arthur A. Melo, Jerzy Kruk, Adam Frost, Michal Gabruk
bioRxiv 2020.08.19.257774; doi: https://doi.org/10.1101/2020.08.19.257774
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Photocatalytic plant LPOR forms helical lattices that shape membranes for chlorophyll synthesis
Henry C. Nguyen, Arthur A. Melo, Jerzy Kruk, Adam Frost, Michal Gabruk
bioRxiv 2020.08.19.257774; doi: https://doi.org/10.1101/2020.08.19.257774

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