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Title: Limitations to photosynthesis by proton motive force-induced photosystem II photodamage

Abstract

The thylakoid proton motive force (pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [4];  [6];  [4];  [6]; ORCiD logo [7]
  1. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Graduate Program of Cell and Molecular Biology, Michigan State University, East Lansing, United States
  2. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Department of Chemistry, Michigan State University, East Lansing, United States
  3. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam-Golm, Germany
  4. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States
  5. Department of Life Sciences, Imperial College London, London, United Kingdom
  6. Department of Horticulture, Washington State University, Pullman, United States
  7. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, United States, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1328499
Alternate Identifier(s):
OSTI ID: 1328500; OSTI ID: 1602544
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 5; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, and Kramer, David M. Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. United States: N. p., 2016. Web. doi:10.7554/eLife.16921.
Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, & Kramer, David M. Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. United States. doi:10.7554/eLife.16921.
Davis, Geoffry A., Kanazawa, Atsuko, Schöttler, Mark Aurel, Kohzuma, Kaori, Froehlich, John E., Rutherford, A. William, Satoh-Cruz, Mio, Minhas, Deepika, Tietz, Stefanie, Dhingra, Amit, and Kramer, David M. Tue . "Limitations to photosynthesis by proton motive force-induced photosystem II photodamage". United States. doi:10.7554/eLife.16921.
@article{osti_1328499,
title = {Limitations to photosynthesis by proton motive force-induced photosystem II photodamage},
author = {Davis, Geoffry A. and Kanazawa, Atsuko and Schöttler, Mark Aurel and Kohzuma, Kaori and Froehlich, John E. and Rutherford, A. William and Satoh-Cruz, Mio and Minhas, Deepika and Tietz, Stefanie and Dhingra, Amit and Kramer, David M.},
abstractNote = {The thylakoid proton motive force (pmf) generated during photosynthesis is the essential driving force for ATP production; it is also a central regulator of light capture and electron transfer. We investigated the effects of elevated pmf on photosynthesis in a library of Arabidopsis thaliana mutants with altered rates of thylakoid lumen proton efflux, leading to a range of steady-state pmf extents. We observed the expected pmf-dependent alterations in photosynthetic regulation, but also strong effects on the rate of photosystem II (PSII) photodamage. Detailed analyses indicate this effect is related to an elevated electric field (Δψ) component of the pmf, rather than lumen acidification, which in vivo increased PSII charge recombination rates, producing singlet oxygen and subsequent photodamage. The effects are seen even in wild type plants, especially under fluctuating illumination, suggesting that Δψ-induced photodamage represents a previously unrecognized limiting factor for plant productivity under dynamic environmental conditions seen in the field.},
doi = {10.7554/eLife.16921},
journal = {eLife},
number = ,
volume = 5,
place = {United States},
year = {2016},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.7554/eLife.16921

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Cited by: 19 works
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