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Title: Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4

Abstract

Phytochrome photoreceptors control plant growth, development, and the shade avoidance response that limits crop yield in high-density agricultural plantings. Cyanobacteriochromes (CBCRs) are distantly related photosensory proteins that control cyanobacterial metabolism and behavior in response to light. Photoreceptors in both families reversibly photoconvert between two photostates via photoisomerization of linear tetrapyrrole (bilin) chromophores. Spectroscopic and biochemical reprorts have demonstrated heterogeneity in both photostates, but the structural basis for such heterogeneity remains unclear. We discuss solution NMR structures for both photostates of the red/green CBCR NpR6012g4 fromNostoc punctiforme. In addition to identifying structural changes accompanying photoconversion, these structures reveal structural heterogeneity for residues Trp655 and Asp657 in the red-absorbing NpR6012g4 dark state, yielding two distinct environments for the phycocyanobilin chromophore. We use site-directed mutagenesis and fluorescence and absorbance spectroscopy to assign an orange-absorbing population in the NpR6012g4 dark state to the minority configuration for Asp657. This population does not undergo full, productive photoconversion, as shown by time-resolved spectroscopy and absorption spectroscopy at cryogenic temperature. Our research thus elucidate the spectral and photochemical consequences of structural heterogeneity in a member of the phytochrome superfamily, insights that should inform efforts to improve photochemical or fluorescence quantum yields in the phytochrome superfamily.

Authors:
 [1];  [1];  [2];  [1];  [1];  [1];  [1]; ORCiD logo [1];  [1];  [1]
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  1. Univ. of California, Davis, CA (United States)
  2. Univ. of California, Davis, CA (United States); Allan Hancock College, Santa Maria, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)
OSTI Identifier:
1540279
Grant/Contract Number:  
SC0002395; FG02-09ER16117
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 17; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biliprotein; light sensor; photoswitch; photoacclimation; optogenetics

Citation Formats

Lim, Sunghyuk, Yu, Qinhong, Gottlieb, Sean M., Chang, Che-Wei, Rockwell, Nathan C., Martin, Shelley S., Madsen, Dorte, Lagarias, J. Clark, Larsen, Delmar S., and Ames, James B. Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4. United States: N. p., 2018. Web. doi:10.1073/pnas.1720682115.
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Lim, Sunghyuk, Yu, Qinhong, Gottlieb, Sean M., Chang, Che-Wei, Rockwell, Nathan C., Martin, Shelley S., Madsen, Dorte, Lagarias, J. Clark, Larsen, Delmar S., & Ames, James B. Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4. United States. https://doi.org/10.1073/pnas.1720682115
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Lim, Sunghyuk, Yu, Qinhong, Gottlieb, Sean M., Chang, Che-Wei, Rockwell, Nathan C., Martin, Shelley S., Madsen, Dorte, Lagarias, J. Clark, Larsen, Delmar S., and Ames, James B. Mon . "Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4". United States. https://doi.org/10.1073/pnas.1720682115. https://www.osti.gov/servlets/purl/1540279.
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@article{osti_1540279,
title = {Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4},
author = {Lim, Sunghyuk and Yu, Qinhong and Gottlieb, Sean M. and Chang, Che-Wei and Rockwell, Nathan C. and Martin, Shelley S. and Madsen, Dorte and Lagarias, J. Clark and Larsen, Delmar S. and Ames, James B.},
abstractNote = {Phytochrome photoreceptors control plant growth, development, and the shade avoidance response that limits crop yield in high-density agricultural plantings. Cyanobacteriochromes (CBCRs) are distantly related photosensory proteins that control cyanobacterial metabolism and behavior in response to light. Photoreceptors in both families reversibly photoconvert between two photostates via photoisomerization of linear tetrapyrrole (bilin) chromophores. Spectroscopic and biochemical reprorts have demonstrated heterogeneity in both photostates, but the structural basis for such heterogeneity remains unclear. We discuss solution NMR structures for both photostates of the red/green CBCR NpR6012g4 fromNostoc punctiforme. In addition to identifying structural changes accompanying photoconversion, these structures reveal structural heterogeneity for residues Trp655 and Asp657 in the red-absorbing NpR6012g4 dark state, yielding two distinct environments for the phycocyanobilin chromophore. We use site-directed mutagenesis and fluorescence and absorbance spectroscopy to assign an orange-absorbing population in the NpR6012g4 dark state to the minority configuration for Asp657. This population does not undergo full, productive photoconversion, as shown by time-resolved spectroscopy and absorption spectroscopy at cryogenic temperature. Our research thus elucidate the spectral and photochemical consequences of structural heterogeneity in a member of the phytochrome superfamily, insights that should inform efforts to improve photochemical or fluorescence quantum yields in the phytochrome superfamily.},
doi = {10.1073/pnas.1720682115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 17,
volume = 115,
place = {United States},
year = {2018},
month = {4}
}
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https://doi.org/10.1073/pnas.1720682115
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