Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1

Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in ARABIDOPSIS: There is also evidence, on a ge...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 105; no. 12; pp. 4939 - 4944
Main Authors: Gutiérrez, Rodrigo A, Stokes, Trevor L, Thum, Karen, Xu, Xiaodong, Obertello, Mariana, Katari, Manpreet S, Tanurdzic, Milos, Dean, Alexis, Nero, Damion C, McClung, C. Robertson, Coruzzi, Gloria M
Format: Journal Article
Language:English
Published: United States National Academy of Sciences 25-03-2008
National Acad Sciences
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Abstract Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in ARABIDOPSIS: There is also evidence, on a gene-by-gene basis, that downstream products of nitrogen (N) assimilation such as glutamate (Glu) or glutamine (Gln) might serve as signals of organic N status that in turn regulate gene expression. To identify genome-wide responses to such organic N signals, Arabidopsis seedlings were transiently treated with ammonium nitrate in the presence or absence of MSX, an inhibitor of glutamine synthetase, resulting in a block of Glu/Gln synthesis. Genes that responded to organic N were identified as those whose response to ammonium nitrate treatment was blocked in the presence of MSX. We showed that some genes previously identified to be regulated by nitrate are under the control of an organic N-metabolite. Using an integrated network model of molecular interactions, we uncovered a subnetwork regulated by organic N that included CCA1 and target genes involved in N-assimilation. We validated some of the predicted interactions and showed that regulation of the master clock control gene CCA1 by Glu or a Glu-derived metabolite in turn regulates the expression of key N-assimilatory genes. Phase response curve analysis shows that distinct N-metabolites can advance or delay the CCA1 phase. Regulation of CCA1 by organic N signals may represent a novel input mechanism for N-nutrients to affect plant circadian clock function.
AbstractList Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in Arabidopsis . There is also evidence, on a gene-by-gene basis, that downstream products of nitrogen (N) assimilation such as glutamate (Glu) or glutamine (Gln) might serve as signals of organic N status that in turn regulate gene expression. To identify genome-wide responses to such organic N signals, Arabidopsis seedlings were transiently treated with ammonium nitrate in the presence or absence of MSX, an inhibitor of glutamine synthetase, resulting in a block of Glu/Gln synthesis. Genes that responded to organic N were identified as those whose response to ammonium nitrate treatment was blocked in the presence of MSX. We showed that some genes previously identified to be regulated by nitrate are under the control of an organic N-metabolite. Using an integrated network model of molecular interactions, we uncovered a subnetwork regulated by organic N that included CCA1 and target genes involved in N-assimilation. We validated some of the predicted interactions and showed that regulation of the master clock control gene CCA1 by Glu or a Glu-derived metabolite in turn regulates the expression of key N-assimilatory genes. Phase response curve analysis shows that distinct N-metabolites can advance or delay the CCA1 phase. Regulation of CCA1 by organic N signals may represent a novel input mechanism for N-nutrients to affect plant circadian clock function.
Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in ARABIDOPSIS: There is also evidence, on a gene-by-gene basis, that downstream products of nitrogen (N) assimilation such as glutamate (Glu) or glutamine (Gln) might serve as signals of organic N status that in turn regulate gene expression. To identify genome-wide responses to such organic N signals, Arabidopsis seedlings were transiently treated with ammonium nitrate in the presence or absence of MSX, an inhibitor of glutamine synthetase, resulting in a block of Glu/Gln synthesis. Genes that responded to organic N were identified as those whose response to ammonium nitrate treatment was blocked in the presence of MSX. We showed that some genes previously identified to be regulated by nitrate are under the control of an organic N-metabolite. Using an integrated network model of molecular interactions, we uncovered a subnetwork regulated by organic N that included CCA1 and target genes involved in N-assimilation. We validated some of the predicted interactions and showed that regulation of the master clock control gene CCA1 by Glu or a Glu-derived metabolite in turn regulates the expression of key N-assimilatory genes. Phase response curve analysis shows that distinct N-metabolites can advance or delay the CCA1 phase. Regulation of CCA1 by organic N signals may represent a novel input mechanism for N-nutrients to affect plant circadian clock function.
Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in Arabidopsis . There is also evidence, on a gene-by-gene basis, that downstream products of nitrogen (N) assimilation such as glutamate (Glu) or glutamine (Gln) might serve as signals of organic N status that in turn regulate gene expression. To identify genome-wide responses to such organic N signals, Arabidopsis seedlings were transiently treated with ammonium nitrate in the presence or absence of MSX, an inhibitor of glutamine synthetase, resulting in a block of Glu/Gln synthesis. Genes that responded to organic N were identified as those whose response to ammonium nitrate treatment was blocked in the presence of MSX. We showed that some genes previously identified to be regulated by nitrate are under the control of an organic N-metabolite. Using an integrated network model of molecular interactions, we uncovered a subnetwork regulated by organic N that included CCA1 and target genes involved in N-assimilation. We validated some of the predicted interactions and showed that regulation of the master clock control gene CCA1 by Glu or a Glu-derived metabolite in turn regulates the expression of key N-assimilatory genes. Phase response curve analysis shows that distinct N-metabolites can advance or delay the CCA1 phase. Regulation of CCA1 by organic N signals may represent a novel input mechanism for N-nutrients to affect plant circadian clock function. circadian gene networks glutamate metabolism
Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient availability. Nitrate has been shown to serve as a signal for the control of gene expression in Arabidopsis. There is also evidence, on a gene-by-gene basis, that downstream products of nitrogen (N) assimilation such as glutamate (Glu) or glutamine (Gln) might serve as signals of organic N status that in turn regulate gene expression. To identify genome-wide responses to such organic N signals, Arabidopsis seedlings were transiently treated with ammonium nitrate in the presence or absence of MSX, an inhibitor of glutamine synthetase, resulting in a block of Glu/Gln synthesis. Genes that responded to organic N were identified as those whose response to ammonium nitrate treatment was blocked in the presence of MSX. We showed that some genes previously identified to be regulated by nitrate are under the control of an organic N-metabolite. Using an integrated network model of molecular interactions, we uncovered a subnetwork regulated by organic N that included CCA1 and target genes involved in N-assimilation. We validated some of the predicted interactions and showed that regulation of the master clock control gene CCA1 by Glu or a Glu-derived metabolite in turn regulates the expression of key N-assimilatory genes. Phase response curve analysis shows that distinct N-metabolites can advance or delay the CCA1 phase. Regulation of CCA1 by organic N signals may represent a novel input mechanism for N-nutrients to affect plant circadian clock function. [PUBLICATION ABSTRACT]
Author Gutiérrez, Rodrigo A
Tanurdzic, Milos
McClung, C. Robertson
Thum, Karen
Stokes, Trevor L
Katari, Manpreet S
Dean, Alexis
Coruzzi, Gloria M
Nero, Damion C
Obertello, Mariana
Xu, Xiaodong
Author_xml – sequence: 1
  fullname: Gutiérrez, Rodrigo A
– sequence: 2
  fullname: Stokes, Trevor L
– sequence: 3
  fullname: Thum, Karen
– sequence: 4
  fullname: Xu, Xiaodong
– sequence: 5
  fullname: Obertello, Mariana
– sequence: 6
  fullname: Katari, Manpreet S
– sequence: 7
  fullname: Tanurdzic, Milos
– sequence: 8
  fullname: Dean, Alexis
– sequence: 9
  fullname: Nero, Damion C
– sequence: 10
  fullname: McClung, C. Robertson
– sequence: 11
  fullname: Coruzzi, Gloria M
BackLink https://www.ncbi.nlm.nih.gov/pubmed/18344319$$D View this record in MEDLINE/PubMed
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10.1073/pnas.70.12.3387
ContentType Journal Article
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Communicated by Joanne Chory, Salk Institute for Biological Studies, La Jolla, CA, January 24, 2008
Author contributions: R.A.G., C.R.M., and G.M.C. designed research; R.A.G., T.L.S., K.T., X.X., M.O., M.T., and A.D. performed research; R.A.G., M.S.K., and D.C.N. analyzed data; and R.A.G., C.R.M., and G.M.C. wrote the paper.
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Snippet Understanding how nutrients affect gene expression will help us to understand the mechanisms controlling plant growth and development as a function of nutrient...
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SubjectTerms Amino acid metabolism
ammonium nitrogen
Arabidopsis
Arabidopsis - drug effects
Arabidopsis - genetics
Arabidopsis Proteins - genetics
Arabidopsis thaliana
asparagine
Biological Sciences
Botany
CCA1 gene
Circadian Rhythm - drug effects
Flowers & plants
Gene expression
Gene expression regulation
Gene Expression Regulation, Plant - drug effects
gene networks
Gene Regulatory Networks - drug effects
Genes
Genome, Plant
genomics
Gin
glutamic acid
Glutamic Acid - pharmacology
Glutamine - pharmacology
Messenger RNA
Metabolism
metabolites
Models, Genetic
nitrate nitrogen
Nitrates
Nitrates - pharmacology
Nitrogen
Nitrogen - pharmacology
nitrogen metabolism
Plant growth
Plants
Promoter Regions, Genetic - genetics
Protein Binding - drug effects
Reproducibility of Results
RNA, Messenger - genetics
RNA, Messenger - metabolism
Seedlings
Seedlings - drug effects
Seedlings - genetics
Signal Transduction - drug effects
transcription (genetics)
Transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
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Title Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1
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http://www.pnas.org/content/105/12/4939.abstract
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