The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis
Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely cand...
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| Published in | The Plant cell Vol. 25; no. 9; pp. 3472 - 3490 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
American Society of Plant Biologists
01.09.2013
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 1040-4651 1532-298X 1532-298X |
| DOI | 10.1105/tpc.113.117168 |
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| Abstract | Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain—containing NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana. |
|---|---|
| AbstractList | This work reports the discovery of a
cis
-regulatory motif in the promoters of genes that are subject to mitochondrial retrograde regulation and the identification of transcription factors that bind to this element, thereby steering mitochondrial retrograde-induced gene expression.
Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (
MRR
). Although reactive oxygen species and calcium are likely candidate signaling molecules for
MRR
, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of
MRR
and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (
MDS
) genes, we found a
cis
-regulatory element, the mitochondrial dysfunction motif (
MDM
), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain–containing NO APICAL MERISTEM/
ARABIDOPSIS
TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the
MDM
cis
-regulatory element. We demonstrate that ANAC013 mediates
MRR
-induced expression of the
MDS
genes by direct interaction with the
MDM
cis
-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of
MRR
upon stress in
Arabidopsis thaliana
. Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain-containing no apical meristem/Arabidopsis transcription activation factor/cup-shaped cotyledon transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana. Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain–containing NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana. Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain-containing no apical meristem/Arabidopsis transcription activation factor/cup-shaped cotyledon transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana.Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus communication is often referred to as mitochondrial retrograde regulation (MRR). Although reactive oxygen species and calcium are likely candidate signaling molecules for MRR, the protein signaling components in plants remain largely unknown. Through meta-analysis of transcriptome data, we detected a set of genes that are common and robust targets of MRR and used them as a bait to identify its transcriptional regulators. In the upstream regions of these mitochondrial dysfunction stimulon (MDS) genes, we found a cis-regulatory element, the mitochondrial dysfunction motif (MDM), which is necessary and sufficient for gene expression under various mitochondrial perturbation conditions. Yeast one-hybrid analysis and electrophoretic mobility shift assays revealed that the transmembrane domain-containing no apical meristem/Arabidopsis transcription activation factor/cup-shaped cotyledon transcription factors (ANAC013, ANAC016, ANAC017, ANAC053, and ANAC078) bound to the MDM cis-regulatory element. We demonstrate that ANAC013 mediates MRR-induced expression of the MDS genes by direct interaction with the MDM cis-regulatory element and triggers increased oxidative stress tolerance. In conclusion, we characterized ANAC013 as a regulator of MRR upon stress in Arabidopsis thaliana. This work reports the discovery of a cis -regulatory motif in the promoters of genes that are subject to mitochondrial retrograde regulation and the identification of transcription factors that bind to this element, thereby steering mitochondrial retrograde-induced gene expression. |
| Author | Vandepoele, Klaas Van Breusegem, Frank Rombaut, Debbie Kangasjärvi, Jaakko Van de Peer, Yves Van Aken, Olivier Law, Simon R. Ng, Sophia Whelan, James Inzé, Annelies Ivanova, Aneta van de Cotte, Brigitte Vermeirssen, Vanessa Murcha, Monika W. Jaspers, Pinja De Clercq, Inge |
| Author_xml | – sequence: 1 givenname: Inge surname: De Clercq fullname: De Clercq, Inge – sequence: 2 givenname: Vanessa surname: Vermeirssen fullname: Vermeirssen, Vanessa – sequence: 3 givenname: Olivier surname: Van Aken fullname: Van Aken, Olivier – sequence: 4 givenname: Klaas surname: Vandepoele fullname: Vandepoele, Klaas – sequence: 5 givenname: Monika W. surname: Murcha fullname: Murcha, Monika W. – sequence: 6 givenname: Simon R. surname: Law fullname: Law, Simon R. – sequence: 7 givenname: Annelies surname: Inzé fullname: Inzé, Annelies – sequence: 8 givenname: Sophia surname: Ng fullname: Ng, Sophia – sequence: 9 givenname: Aneta surname: Ivanova fullname: Ivanova, Aneta – sequence: 10 givenname: Debbie surname: Rombaut fullname: Rombaut, Debbie – sequence: 11 givenname: Brigitte surname: van de Cotte fullname: van de Cotte, Brigitte – sequence: 12 givenname: Pinja surname: Jaspers fullname: Jaspers, Pinja – sequence: 13 givenname: Yves surname: Van de Peer fullname: Van de Peer, Yves – sequence: 14 givenname: Jaakko surname: Kangasjärvi fullname: Kangasjärvi, Jaakko – sequence: 15 givenname: James surname: Whelan fullname: Whelan, James – sequence: 16 givenname: Frank surname: Van Breusegem fullname: Van Breusegem, Frank |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24045019$$D View this record in MEDLINE/PubMed |
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| Snippet | Upon disturbance of their function by stress, mitochondria can signal to the nucleus to steer the expression of responsive genes. This mitochondria-to-nucleus... This work reports the discovery of a cis -regulatory motif in the promoters of genes that are subject to mitochondrial retrograde regulation and the... This work reports the discovery of a cis -regulatory motif in the promoters of genes that are subject to mitochondrial retrograde regulation and the... |
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| SubjectTerms | Arabidopsis Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Binding Sites Cell Nucleus - metabolism Endoplasmic Reticulum - metabolism gene expression Gene Expression Profiling Gene expression regulation Gene Expression Regulation, Plant Genes Mitochondria Mitochondria - metabolism Mutation Oligonucleotide Array Sequence Analysis Oxidative Stress Paraquat - pharmacology Plant cells Plants Plants, Genetically Modified Promoter Regions, Genetic - genetics Protein Binding Regulatory Sequences, Nucleic Acid - genetics Rotenone - pharmacology Seedlings Seedlings - drug effects Seedlings - genetics Seedlings - physiology stress response transcription (genetics) Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptional Activation Transcriptional regulatory elements Yeasts |
| Title | The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis |
| URI | https://www.jstor.org/stable/23598362 https://www.ncbi.nlm.nih.gov/pubmed/24045019 https://www.proquest.com/docview/1447105991 https://www.proquest.com/docview/2000143628 https://pubmed.ncbi.nlm.nih.gov/PMC3809544 |
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