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In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant

Podgorska, Anna; Ostaszewska, Monika; Gardestrom, Per; Rasmusson, Allan LU and Szal, Bozena (2015) In Plant, Cell and Environment 38(1). p.224-237
Abstract
Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron... (More)
Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron transport chain may improve the energy metabolism of fro1 plants grown on ammonium. Additionally, the observed changes in reactive oxygen species (ROS) metabolism in the apoplast may be important for determining the growth of fro1 under ammonium nutrition. Moreover, bioinformatic analyses showed that the gene expression changes in fro1 plants significantly overlap with the changes previously observed in plants with a modified apoplastic pH. Overall, the results suggest a pronounced connection between the mitochondrial redox system and the apoplastic pH and ROS levels, which may modify cell wall plasticity and influence growth. In this paper, we analysed the redox metabolism of frostbite1 (fro1) plants lacking Complex I under ammonium nutrition. We showed that, although ammonium leads to stress in wild type plants, ammonium does not cause reductive stress in fro1 plants. Our experimental and bioinformatic analyses indicated that mtETC dysfunction strongly influences apoplastic reactive oxygen species content and pH, and suggested that the faster growth of fro1 plants under ammonium nutrition probably results from modification of the cell wall. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
ammonium syndrome, apoplast, apoplastic pH, complex I, dysfunction of, mtETC, mitochondria, redox homeostasis, respiration
in
Plant, Cell and Environment
volume
38
issue
1
pages
224 - 237
publisher
Wiley-Blackwell
external identifiers
  • wos:000346429800019
  • scopus:84917733532
ISSN
0140-7791
DOI
10.1111/pce.12404
language
English
LU publication?
yes
id
a040a095-43f8-4b83-b0a9-86840e2cf072 (old id 4941608)
date added to LUP
2015-01-28 08:13:20
date last changed
2017-09-24 03:19:58
@article{a040a095-43f8-4b83-b0a9-86840e2cf072,
  abstract     = {Ammonium nutrition inhibits the growth of many plant species, including Arabidopsis thaliana. The toxicity of ammonium is associated with changes in the cellular redox state. The cellular oxidant/antioxidant balance is controlled by mitochondrial electron transport chain. In this study, we analysed the redox metabolism of frostbite1 (fro1) plants, which lack mitochondrial respiratory chain complex I. Surprisingly, the growth of fro1 plants increased under ammonium nutrition. Ammonium nutrition increased the reduction level of pyridine nucleotides in the leaves of wild-type plants, but not in the leaves of fro1 mutant plants. The observed higher activities of type II NADH dehydrogenases and cytochrome c oxidase in the mitochondrial electron transport chain may improve the energy metabolism of fro1 plants grown on ammonium. Additionally, the observed changes in reactive oxygen species (ROS) metabolism in the apoplast may be important for determining the growth of fro1 under ammonium nutrition. Moreover, bioinformatic analyses showed that the gene expression changes in fro1 plants significantly overlap with the changes previously observed in plants with a modified apoplastic pH. Overall, the results suggest a pronounced connection between the mitochondrial redox system and the apoplastic pH and ROS levels, which may modify cell wall plasticity and influence growth. In this paper, we analysed the redox metabolism of frostbite1 (fro1) plants lacking Complex I under ammonium nutrition. We showed that, although ammonium leads to stress in wild type plants, ammonium does not cause reductive stress in fro1 plants. Our experimental and bioinformatic analyses indicated that mtETC dysfunction strongly influences apoplastic reactive oxygen species content and pH, and suggested that the faster growth of fro1 plants under ammonium nutrition probably results from modification of the cell wall.},
  author       = {Podgorska, Anna and Ostaszewska, Monika and Gardestrom, Per and Rasmusson, Allan and Szal, Bozena},
  issn         = {0140-7791},
  keyword      = {ammonium syndrome,apoplast,apoplastic pH,complex I,dysfunction of,mtETC,mitochondria,redox homeostasis,respiration},
  language     = {eng},
  number       = {1},
  pages        = {224--237},
  publisher    = {Wiley-Blackwell},
  series       = {Plant, Cell and Environment},
  title        = {In comparison with nitrate nutrition, ammonium nutrition increases growth of the frostbite1 Arabidopsis mutant},
  url          = {http://dx.doi.org/10.1111/pce.12404},
  volume       = {38},
  year         = {2015},
}