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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| Veröffentlicht in: | The Plant cell Jg. 25; H. 9; S. 3472 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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01.09.2013
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| ISSN: | 1532-298X, 1532-298X |
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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. |
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| AbstractList | 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. |
| Author | Vandepoele, Klaas Van Breusegem, Frank Murcha, Monika W Law, Simon R Rombaut, Debbie Kangasjärvi, Jaakko Van de Peer, Yves Van Aken, Olivier Ng, Sophia Whelan, James Inzé, Annelies Ivanova, Aneta van de Cotte, Brigitte Vermeirssen, Vanessa Jaspers, Pinja De Clercq, Inge |
| Author_xml | – sequence: 1 givenname: Inge surname: De Clercq fullname: De Clercq, Inge organization: Department of Plant Systems Biology, VIB, 9052 Ghent, Belgium – 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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| PublicationTitle | The Plant cell |
| PublicationTitleAlternate | Plant Cell |
| PublicationYear | 2013 |
| SSID | ssj0001719 |
| Score | 2.5686457 |
| 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... |
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| StartPage | 3472 |
| SubjectTerms | Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Binding Sites Cell Nucleus - metabolism Endoplasmic Reticulum - metabolism Gene Expression Profiling Gene Expression Regulation, Plant Mitochondria - metabolism Mutation Oligonucleotide Array Sequence Analysis Oxidative Stress Paraquat - pharmacology Plants, Genetically Modified Promoter Regions, Genetic - genetics Protein Binding Regulatory Sequences, Nucleic Acid - genetics Rotenone - pharmacology Seedlings - drug effects Seedlings - genetics Seedlings - physiology Transcription Factors - genetics Transcription Factors - metabolism Transcriptional Activation |
| Title | The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis |
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