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Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection

Journal Article · · Frontiers in Plant Science
 [1];  [2];  [2];  [3];  [2];  [2];  [2];  [4];  [2];  [4];  [4]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Chemistry; Michigan State University
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
  3. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Cell and Molecular Biology
  4. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. Biochemistry and Molecular Biology
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In wild type plants, decreasing CO2 lowers the activity of the chloroplast ATP synthase, slowing proton efflux from the thylakoid lumen resulting in buildup of thylakoid proton motive force (pmf). The resulting acidification of the lumen regulates both light harvesting, via the qE mechanism, and photosynthetic electron transfer through the cytochrome b6f complex. Here in this paper, we show that the cfq mutant of Arabidopsis, harboring single point mutation in its γ-subunit of the chloroplast ATP synthase, increases the specific activity of the ATP synthase and disables its down-regulation under low CO2. The increased thylakoid proton conductivity (gH+) in cfq results in decreased pmf and lumen acidification, preventing full activation of qE and more rapid electron transfer through the b6f complex, particularly under low CO2 and fluctuating light. These conditions favor the accumulation of electrons on the acceptor side of PSI, and result in severe loss of PSI activity. Comparing the current results with previous work on the pgr5 mutant suggests a general mechanism where increased PSI photodamage in both mutants is caused by loss of pmf, rather than inhibition of CEF per se. Overall, our results support a critical role for ATP synthase regulation in maintaining photosynthetic control of electron transfer to prevent photodamage.
Research Organization:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1368188
Journal Information:
Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 8; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (16)

A γ-subunit point mutation in Chlamydomonas reinhardtii chloroplast F1Fo-ATP synthase confers tolerance to reactive oxygen species journal December 2017
Cyclic Electron Flow around Photosystem I Promotes ATP Synthesis Possibly Helping the Rapid Repair of Photodamaged Photosystem II at Low Light journal February 2018
Moderate Photoinhibition of Photosystem II Significantly Affects Linear Electron Flow in the Shade-Demanding Plant Panax notoginseng journal May 2018
Dehydration Stress Memory: Gene Networks Linked to Physiological Responses During Repeated Stresses of Zea mays journal July 2018
Chloroplastic ATP Synthase Alleviates Photoinhibition of Photosystem I in Tobacco Illuminated at Chilling Temperature journal November 2018
Inter-Organelle NAD Metabolism Underpinning Light Responsive NADP Dynamics in Plants journal July 2019
Optimization of ATP Synthase c–Rings for Oxygenic Photosynthesis journal January 2020
Enhanced Photophosphorylation of a Chloroplast-Entrapping Long-Lived Photoacid journal September 2017
Enhanced Photophosphorylation of a Chloroplast-Entrapping Long-Lived Photoacid journal September 2017
Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system journal November 2018
Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts journal October 2017
In vivo regulation of thylakoid proton motive force in immature leaves journal July 2018
Genetic characterization of a flap1 null mutation in Arabidopsis npq4 and pgr5 plants suggests that the regulatory role of FLAP1 involves the control of proton homeostasis in chloroplasts journal November 2018
Overexpression of the Rieske FeS protein of the Cytochrome b6f complex increases C4 photosynthesis in Setaria viridis journal August 2019
Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system posted_content April 2018
PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I journal July 2018

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
ATP synthase
PSI
PSII
pmf
photoprotection
proton motive force