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Title: ‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis

Abstract

High solar flux is known to diminish photosynthetic growth rates, reducing biomass productivity and lowering disease tolerance. Photosystem II (PSII) of plants is susceptible to photodamage (also known as photoinactivation) in strong light, resulting in severe loss of water oxidation capacity and destruction of the water‐oxidizing complex (WOC). The repair of damaged PSIIs comes at a high energy cost and requires de novo biosynthesis of damaged PSII subunits, reassembly of the WOC inorganic cofactors and membrane remodeling. Employing membrane‐inlet mass spectrometry and O 2 ‐polarography under flashing light conditions, we demonstrate that newly synthesized PSII complexes are far more susceptible to photodamage than are mature PSII complexes. We examined these ‘PSII birth defects’ in barley seedlings and plastids (etiochloroplasts and chloroplasts) isolated at various times during de‐etiolation as chloroplast development begins and matures in synchronization with thylakoid membrane biogenesis and grana membrane formation. We show that the degree of PSII photodamage decreases simultaneously with biogenesis of the PSII turnover efficiency measured by O 2 ‐polarography, and with grana membrane stacking, as determined by electron microscopy. Our data from fluorescence, Q B ‐inhibitor binding, and thermoluminescence studies indicate that the decline of the high‐light susceptibility of PSII to photodamagemore » is coincident with appearance of electron transfer capability Q A  →  Q B during de‐etiolation. This rate depends in turn on the downstream clearing of electrons upon buildup of the complete linear electron transfer chain and the formation of stacked grana membranes capable of longer‐range energy transfer.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [4];  [3];  [2];  [5]
  1. Umea Univ. (Sweden)
  2. Rutgers Univ., Piscataway, NJ (United States)
  3. University of Stavanger (Norway)
  4. Uppsala Univ. (Sweden)
  5. Umea Univ. (Sweden); Uppsala Univ. (Sweden)
Publication Date:
Research Org.:
Rutgers Univ., Piscataway, NJ (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1613246
Alternate Identifier(s):
OSTI ID: 1496906
Grant/Contract Number:  
SC0019460; DOE DE‐SC0019460
Resource Type:
Accepted Manuscript
Journal Name:
Physiologia Plantarum
Additional Journal Information:
Journal Volume: 166; Journal Issue: 1; Journal ID: ISSN 0031-9317
Publisher:
Wiley - Scandinavian Plant Physiology Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Plant Sciences

Citation Formats

Shevela, Dmitry, Ananyev, Gennady, Vatland, Ann K., Arnold, Janine, Mamedov, Fikret, Eichacker, Lutz A., Dismukes, G. Charles, and Messinger, Johannes. ‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis. United States: N. p., 2019. Web. doi:10.1111/ppl.12932.
Shevela, Dmitry, Ananyev, Gennady, Vatland, Ann K., Arnold, Janine, Mamedov, Fikret, Eichacker, Lutz A., Dismukes, G. Charles, & Messinger, Johannes. ‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis. United States. https://doi.org/10.1111/ppl.12932
Shevela, Dmitry, Ananyev, Gennady, Vatland, Ann K., Arnold, Janine, Mamedov, Fikret, Eichacker, Lutz A., Dismukes, G. Charles, and Messinger, Johannes. Wed . "‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis". United States. https://doi.org/10.1111/ppl.12932. https://www.osti.gov/servlets/purl/1613246.
@article{osti_1613246,
title = {‘Birth defects’ of photosystem II make it highly susceptible to photodamage during chloroplast biogenesis},
author = {Shevela, Dmitry and Ananyev, Gennady and Vatland, Ann K. and Arnold, Janine and Mamedov, Fikret and Eichacker, Lutz A. and Dismukes, G. Charles and Messinger, Johannes},
abstractNote = {High solar flux is known to diminish photosynthetic growth rates, reducing biomass productivity and lowering disease tolerance. Photosystem II (PSII) of plants is susceptible to photodamage (also known as photoinactivation) in strong light, resulting in severe loss of water oxidation capacity and destruction of the water‐oxidizing complex (WOC). The repair of damaged PSIIs comes at a high energy cost and requires de novo biosynthesis of damaged PSII subunits, reassembly of the WOC inorganic cofactors and membrane remodeling. Employing membrane‐inlet mass spectrometry and O 2 ‐polarography under flashing light conditions, we demonstrate that newly synthesized PSII complexes are far more susceptible to photodamage than are mature PSII complexes. We examined these ‘PSII birth defects’ in barley seedlings and plastids (etiochloroplasts and chloroplasts) isolated at various times during de‐etiolation as chloroplast development begins and matures in synchronization with thylakoid membrane biogenesis and grana membrane formation. We show that the degree of PSII photodamage decreases simultaneously with biogenesis of the PSII turnover efficiency measured by O 2 ‐polarography, and with grana membrane stacking, as determined by electron microscopy. Our data from fluorescence, Q B ‐inhibitor binding, and thermoluminescence studies indicate that the decline of the high‐light susceptibility of PSII to photodamage is coincident with appearance of electron transfer capability Q A −  →  Q B during de‐etiolation. This rate depends in turn on the downstream clearing of electrons upon buildup of the complete linear electron transfer chain and the formation of stacked grana membranes capable of longer‐range energy transfer.},
doi = {10.1111/ppl.12932},
journal = {Physiologia Plantarum},
number = 1,
volume = 166,
place = {United States},
year = {Wed Feb 27 00:00:00 EST 2019},
month = {Wed Feb 27 00:00:00 EST 2019}
}

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Works referencing / citing this record:

Beyond the darkness: recent lessons from etiolation and de-etiolation studies
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Beyond the darkness: recent lessons from etiolation and de-etiolation studies
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