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Title: Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I

Abstract

We describe a new member of the class of mutants in Arabidopsis exhibiting high rates of cyclic electron flow around photosystem I (CEF), a light-driven process that produces ATP but not NADPH. High cyclic electron flow 2 (hcef2) shows strongly increased CEF activity through the NADPH dehydrogenase complex (NDH), accompanied by increases in thylakoid proton motive force (pmf), activation of the photoprotective qE response, and the accumulation of H 2O 2 . Surprisingly, hcef2 was mapped to a nonsense mutation in the TADA1 (tRNA adenosine deaminase arginine) locus, coding for a plastid targeted tRNA editing enzyme required for efficient codon recognition. Comparison of protein content from representative thylakoid complexes, the cytochrome bf complex and the ATP synthase, suggests that inefficient translation of hcef2 leads to compromised complex assembly or stability leading to alterations in stoichiometries of major thylakoid complexes as well as their constituent subunits. Altered subunit stoichiometries for photosystem I, ratios and properties of cytochrome bf hemes, and the decay kinetics of the flash induced thylakoid electric field suggest that these defect lead to accumulation of H 2O 2 in hcef2, which we have previously shown leads to activation of NDHrelated CEF. We observed similar increases in CEF andmore » H 2O 2 accumulation in other translation defective mutants, suggesting that loss of coordination in plastid protein levels lead to imbalances in the photosynthetic energy balance that leads to increased CEF. These results, together with a large body of previous observations, support a general model in which processes that imbalances in chloroplast energetics result in the production of H 2O 2 , which activates CEF, either as a redox signal or by inducing deficits in ATP levels.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1344642
Report Number(s):
PNNL-SA-118306
Journal ID: ISSN 1664-462X; KP1704020
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Frontiers in Plant Science; Journal Volume: 7
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hcef2; cyclic electron flow

Citation Formats

Strand, Deserah D., Livingston, Aaron K., Satoh-Cruz, Mio, Koepke, Tyson, Enlow, Heather M., Fisher, Nicholas, Froehlich, John E., Cruz, Jeffrey A., Minhas, Deepika, Hixson, Kim K., Kohzuma, Kaori, Lipton, Mary, Dhingra, Amit, and Kramer, David M. Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I. United States: N. p., 2017. Web. doi:10.3389/fpls.2016.02073.
Strand, Deserah D., Livingston, Aaron K., Satoh-Cruz, Mio, Koepke, Tyson, Enlow, Heather M., Fisher, Nicholas, Froehlich, John E., Cruz, Jeffrey A., Minhas, Deepika, Hixson, Kim K., Kohzuma, Kaori, Lipton, Mary, Dhingra, Amit, & Kramer, David M. Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I. United States. doi:10.3389/fpls.2016.02073.
Strand, Deserah D., Livingston, Aaron K., Satoh-Cruz, Mio, Koepke, Tyson, Enlow, Heather M., Fisher, Nicholas, Froehlich, John E., Cruz, Jeffrey A., Minhas, Deepika, Hixson, Kim K., Kohzuma, Kaori, Lipton, Mary, Dhingra, Amit, and Kramer, David M. Fri . "Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I". United States. doi:10.3389/fpls.2016.02073.
@article{osti_1344642,
title = {Defects in the Expression of Chloroplast Proteins Leads to H2O2 Accumulation and Activation of Cyclic Electron Flow around Photosystem I},
author = {Strand, Deserah D. and Livingston, Aaron K. and Satoh-Cruz, Mio and Koepke, Tyson and Enlow, Heather M. and Fisher, Nicholas and Froehlich, John E. and Cruz, Jeffrey A. and Minhas, Deepika and Hixson, Kim K. and Kohzuma, Kaori and Lipton, Mary and Dhingra, Amit and Kramer, David M.},
abstractNote = {We describe a new member of the class of mutants in Arabidopsis exhibiting high rates of cyclic electron flow around photosystem I (CEF), a light-driven process that produces ATP but not NADPH. High cyclic electron flow 2 (hcef2) shows strongly increased CEF activity through the NADPH dehydrogenase complex (NDH), accompanied by increases in thylakoid proton motive force (pmf), activation of the photoprotective qE response, and the accumulation of H2O2 . Surprisingly, hcef2 was mapped to a nonsense mutation in the TADA1 (tRNA adenosine deaminase arginine) locus, coding for a plastid targeted tRNA editing enzyme required for efficient codon recognition. Comparison of protein content from representative thylakoid complexes, the cytochrome bf complex and the ATP synthase, suggests that inefficient translation of hcef2 leads to compromised complex assembly or stability leading to alterations in stoichiometries of major thylakoid complexes as well as their constituent subunits. Altered subunit stoichiometries for photosystem I, ratios and properties of cytochrome bf hemes, and the decay kinetics of the flash induced thylakoid electric field suggest that these defect lead to accumulation of H2O2 in hcef2, which we have previously shown leads to activation of NDHrelated CEF. We observed similar increases in CEF and H2O2 accumulation in other translation defective mutants, suggesting that loss of coordination in plastid protein levels lead to imbalances in the photosynthetic energy balance that leads to increased CEF. These results, together with a large body of previous observations, support a general model in which processes that imbalances in chloroplast energetics result in the production of H2O2 , which activates CEF, either as a redox signal or by inducing deficits in ATP levels.},
doi = {10.3389/fpls.2016.02073},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Fri Jan 13 00:00:00 EST 2017},
month = {Fri Jan 13 00:00:00 EST 2017}
}