Patterns of Protein Oxidation in Arabidopsis Seeds and during Germination

Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein degradation are poorly characterized. In this work, protein carbonylation, which is an irreversible oxidation process leading to a loss of functio...

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Published inPlant physiology (Bethesda) Vol. 138; no. 2; pp. 790 - 802
Main Authors Job, Claudette, Rajjou, Loi̊c, Lovigny, Yoann, Belghazi, Maya, Job, Dominique
Format Journal Article
LanguageEnglish
Published Rockville, MD American Society of Plant Biologists 01.06.2005
American Society of Plant Physiologists
Oxford University Press ; American Society of Plant Biologists
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Abstract Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein degradation are poorly characterized. In this work, protein carbonylation, which is an irreversible oxidation process leading to a loss of function of the modified proteins, has been analyzed by a proteomic approach during the first stages of Arabidopsis (Arabidopsis thaliana) seed germination. In the dry mature seeds, the legumin-type globulins (12S cruciferins) were the major targets. However, the acidic [alpha]-cruciferin subunits were carbonylated to a much higher extent than the basic ([beta]) ones, consistent with a model in which the [beta]-subunits are buried within the cruciferin molecules and the [alpha]-subunits are more exposed to the outside. During imbibition, various carbonylated proteins accumulated. This oxidation damage was not evenly distributed among seed proteins and targeted specific proteins as glycolytic enzymes, mitochondrial ATP synthase, chloroplastic ribulose bisphosphate carboxylase large chain, aldose reductase, methionine synthase, translation factors, and several molecular chaperones. Although accumulation of carbonylated proteins is usually considered in the context of aging in a variety of model systems, this was clearly not the case for the Arabidopsis seeds since they germinated at a high rate and yielded vigorous plantlets. The results indicate that the observed specific changes in protein carbonylation patterns are probably required for counteracting and/or utilizing the production of reactive oxygen species caused by recovery of metabolic activity in the germinating seeds.
AbstractList Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein degradation are poorly characterized. In this work, protein carbonylation, which is an irreversible oxidation process leading to a loss of function of the modified proteins, has been analyzed by a proteomic approach during the first stages of Arabidopsis (Arabidopsis thaliana) seed germination. In the dry mature seeds, the legumin-type globulins (12S cruciferins) were the major targets. However, the acidic alpha-cruciferin subunits were carbonylated to a much higher extent than the basic (beta) ones, consistent with a model in which the beta-subunits are buried within the cruciferin molecules and the alpha-subunits are more exposed to the outside. During imbibition, various carbonylated proteins accumulated. This oxidation damage was not evenly distributed among seed proteins and targeted specific proteins as glycolytic enzymes, mitochondrial ATP synthase, chloroplastic ribulose bisphosphate carboxylase large chain, aldose reductase, methionine synthase, translation factors, and several molecular chaperones. Although accumulation of carbonylated proteins is usually considered in the context of aging in a variety of model systems, this was clearly not the case for the Arabidopsis seeds since they germinated at a high rate and yielded vigorous plantlets. The results indicate that the observed specific changes in protein carbonylation patterns are probably required for counteracting and/or utilizing the production of reactive oxygen species caused by recovery of metabolic activity in the germinating seeds.
Abstract Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein degradation are poorly characterized. In this work, protein carbonylation, which is an irreversible oxidation process leading to a loss of function of the modified proteins, has been analyzed by a proteomic approach during the first stages of Arabidopsis (Arabidopsis thaliana) seed germination. In the dry mature seeds, the legumin-type globulins (12S cruciferins) were the major targets. However, the acidic α-cruciferin subunits were carbonylated to a much higher extent than the basic (β) ones, consistent with a model in which the β-subunits are buried within the cruciferin molecules and the α-subunits are more exposed to the outside. During imbibition, various carbonylated proteins accumulated. This oxidation damage was not evenly distributed among seed proteins and targeted specific proteins as glycolytic enzymes, mitochondrial ATP synthase, chloroplastic ribulose bisphosphate carboxylase large chain, aldose reductase, methionine synthase, translation factors, and several molecular chaperones. Although accumulation of carbonylated proteins is usually considered in the context of aging in a variety of model systems, this was clearly not the case for the Arabidopsis seeds since they germinated at a high rate and yielded vigorous plantlets. The results indicate that the observed specific changes in protein carbonylation patterns are probably required for counteracting and/or utilizing the production of reactive oxygen species caused by recovery of metabolic activity in the germinating seeds.
Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein degradation are poorly characterized. In this work, protein carbonylation, which is an irreversible oxidation process leading to a loss of function of the modified proteins, has been analyzed by a proteomic approach during the first stages of Arabidopsis (Arabidopsis thaliana) seed germination. In the dry mature seeds, the legumin-type globulins (12S cruciferins) were the major targets. However, the acidic α-cruciferin subunits were carbonylated to a much higher extent than the basic (β) ones, consistent with a model in which the β-subunits are buried within the cruciferin molecules and the α-subunits are more exposed to the outside. During imbibition, various carbonylated proteins accumulated. This oxidation damage was not evenly distributed among seed proteins and targeted specific proteins as glycolytic enzymes, mitochondrial ATP synthase, chloroplastic ribulose bisphosphate carboxylase large chain, aldose reductase, methionine synthase, translation factors, and several molecular chaperones. Although accumulation of carbonylated proteins is usually considered in the context of aging in a variety of model systems, this was clearly not the case for the Arabidopsis seeds since they germinated at a high rate and yielded vigorous plantlets. The results indicate that the observed specific changes in protein carbonylation patterns are probably required for counteracting and/or utilizing the production of reactive oxygen species caused by recovery of metabolic activity in the germinating seeds.
Author Job, Claudette
Lovigny, Yoann
Job, Dominique
Belghazi, Maya
Rajjou, Loi̊c
Author_xml – sequence: 1
  fullname: Job, Claudette
– sequence: 2
  fullname: Rajjou, Loi̊c
– sequence: 3
  fullname: Lovigny, Yoann
– sequence: 4
  fullname: Belghazi, Maya
– sequence: 5
  fullname: Job, Dominique
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https://www.ncbi.nlm.nih.gov/pubmed/15908592$$D View this record in MEDLINE/PubMed
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10.1016/S0021-9258(19)61523-1
10.1104/pp.126.2.835
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Issue 2
Keywords O-Acetylhomoserine (thiol)-lyase
Seeds
Enzyme
Germination
Imbibition
Ribulose-bisphosphate carboxylase
Lyases
Synthase
Arabidopsis thaliana
Glycolytic enzyme
Carbon-carbon lyases
Cruciferae
Carboxy-lyases
Dicotyledones
Angiospermae
Proteomics
Aldehyde reductase
Development
Spermatophyta
Oxidoreductases
Carbon-oxygen lyases
ATP
Legumin
Language English
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Snippet Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of protein...
Abstract Increased cellular levels of reactive oxygen species are known to occur during seed development and germination, but the consequences in terms of...
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SubjectTerms Arabidopsis - growth & development
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Biological and medical sciences
Development and Hormone Action
Enzymes
Fundamental and applied biological sciences. Psychology
Gels
Gene Expression Profiling
Germination
Germination - physiology
Germination and dormancy
Globulins
Imbibition
Oxidation
Oxidation-Reduction
Oxidative stress
plant biochemistry
Plant physiology and development
plant proteins
protein carbonylation
proteome
proteomics
Seed germination
seed maturation
Seed storage
seeds
Seeds - metabolism
Storage proteins
two-dimensinal gel electrophoresis
Title Patterns of Protein Oxidation in Arabidopsis Seeds and during Germination
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Volume 138
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