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Efficient Photosynthetic Functioning of Arabidopsis thaliana Through Electron Dissipation in Chloroplasts and Electron Export to Mitochondria Under Ammonium Nutrition

Podgórska, Anna ; Mazur, Radosław ; Ostaszewska-Bugajska, Monika ; Kryzheuskaya, Katsiaryna ; Dziewit, Kacper ; Borysiuk, Klaudia ; Wdowiak, Agata ; Burian, Maria ; Rasmusson, Allan G. LU and Szal, Bożena (2020) In Frontiers in Plant Science 11.
Abstract

An improvement in photosynthetic rate promotes the growth of crop plants. The sink-regulation of photosynthesis is crucial in optimizing nitrogen fixation and integrating it with carbon balance. Studies on these processes are essential in understanding growth inhibition in plants with ammonium ((Formula presented.)) syndrome. Hence, we sought to investigate the effects of using nitrogen sources with different states of reduction (during assimilation of (Formula presented.) versus (Formula presented.)) on the photosynthetic performance of Arabidopsis thaliana. Our results demonstrated that photosynthetic functioning during long-term (Formula presented.) nutrition was not disturbed and that no indication of photoinhibition of PSII was... (More)

An improvement in photosynthetic rate promotes the growth of crop plants. The sink-regulation of photosynthesis is crucial in optimizing nitrogen fixation and integrating it with carbon balance. Studies on these processes are essential in understanding growth inhibition in plants with ammonium ((Formula presented.)) syndrome. Hence, we sought to investigate the effects of using nitrogen sources with different states of reduction (during assimilation of (Formula presented.) versus (Formula presented.)) on the photosynthetic performance of Arabidopsis thaliana. Our results demonstrated that photosynthetic functioning during long-term (Formula presented.) nutrition was not disturbed and that no indication of photoinhibition of PSII was detected, revealing the robustness of the photosynthetic apparatus during stressful conditions. Based on our findings, we propose multiple strategies to sustain photosynthetic activity during limited reductant utilization for (Formula presented.) assimilation. One mechanism to prevent chloroplast electron transport chain overreduction during (Formula presented.) nutrition is for cyclic electron flow together with plastid terminal oxidase activity. Moreover, redox state in chloroplasts was optimized by a dedicated type II NAD(P)H dehydrogenase. In order to reduce the amount of energy that reaches the photosynthetic reaction centers and to facilitate photosynthetic protection during (Formula presented.) nutrition, non-photochemical quenching (NPQ) and ample xanthophyll cycle pigments efficiently dissipate excess excitation. Additionally, high redox load may be dissipated in other metabolic reaA ctions outside of chloroplasts due to the direct export of nucleotides through the malate/oxaloacetate valve. Mitochondrial alternative pathways can downstream support the overreduction of chloroplasts. This mechanism correlated with the improved growth of A. thaliana with the overexpression of the alternative oxidase 1a (AOX1a) during (Formula presented.) nutrition. Most remarkably, our findings demonstrated the capacity of chloroplasts to tolerate (Formula presented.) syndrome instead of providing redox poise to the cells.

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author
; ; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
alternative oxidase, ammonium toxicity syndrome, nitrogen assimilation, non-photochemical quenching, oxidative damage, photosynthetic efficiency, redox dissipation, redox export
in
Frontiers in Plant Science
volume
11
article number
103
publisher
Frontiers Media S. A.
external identifiers
  • pmid:32174931
  • scopus:85082423516
ISSN
1664-462X
DOI
10.3389/fpls.2020.00103
language
English
LU publication?
yes
id
5ba0a93d-20e1-4918-ad2d-53e1e79886ea
date added to LUP
2020-12-30 13:59:36
date last changed
2024-04-03 19:53:54
@article{5ba0a93d-20e1-4918-ad2d-53e1e79886ea,
  abstract     = {{<p>An improvement in photosynthetic rate promotes the growth of crop plants. The sink-regulation of photosynthesis is crucial in optimizing nitrogen fixation and integrating it with carbon balance. Studies on these processes are essential in understanding growth inhibition in plants with ammonium ((Formula presented.)) syndrome. Hence, we sought to investigate the effects of using nitrogen sources with different states of reduction (during assimilation of (Formula presented.) versus (Formula presented.)) on the photosynthetic performance of Arabidopsis thaliana. Our results demonstrated that photosynthetic functioning during long-term (Formula presented.) nutrition was not disturbed and that no indication of photoinhibition of PSII was detected, revealing the robustness of the photosynthetic apparatus during stressful conditions. Based on our findings, we propose multiple strategies to sustain photosynthetic activity during limited reductant utilization for (Formula presented.) assimilation. One mechanism to prevent chloroplast electron transport chain overreduction during (Formula presented.) nutrition is for cyclic electron flow together with plastid terminal oxidase activity. Moreover, redox state in chloroplasts was optimized by a dedicated type II NAD(P)H dehydrogenase. In order to reduce the amount of energy that reaches the photosynthetic reaction centers and to facilitate photosynthetic protection during (Formula presented.) nutrition, non-photochemical quenching (NPQ) and ample xanthophyll cycle pigments efficiently dissipate excess excitation. Additionally, high redox load may be dissipated in other metabolic reaA ctions outside of chloroplasts due to the direct export of nucleotides through the malate/oxaloacetate valve. Mitochondrial alternative pathways can downstream support the overreduction of chloroplasts. This mechanism correlated with the improved growth of A. thaliana with the overexpression of the alternative oxidase 1a (AOX1a) during (Formula presented.) nutrition. Most remarkably, our findings demonstrated the capacity of chloroplasts to tolerate (Formula presented.) syndrome instead of providing redox poise to the cells.</p>}},
  author       = {{Podgórska, Anna and Mazur, Radosław and Ostaszewska-Bugajska, Monika and Kryzheuskaya, Katsiaryna and Dziewit, Kacper and Borysiuk, Klaudia and Wdowiak, Agata and Burian, Maria and Rasmusson, Allan G. and Szal, Bożena}},
  issn         = {{1664-462X}},
  keywords     = {{alternative oxidase; ammonium toxicity syndrome; nitrogen assimilation; non-photochemical quenching; oxidative damage; photosynthetic efficiency; redox dissipation; redox export}},
  language     = {{eng}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Plant Science}},
  title        = {{Efficient Photosynthetic Functioning of Arabidopsis thaliana Through Electron Dissipation in Chloroplasts and Electron Export to Mitochondria Under Ammonium Nutrition}},
  url          = {{http://dx.doi.org/10.3389/fpls.2020.00103}},
  doi          = {{10.3389/fpls.2020.00103}},
  volume       = {{11}},
  year         = {{2020}},
}