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A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis

Ng, Sophia ; Ivanova, Aneta ; Duncan, Owen ; Law, Simon R ; Van Aken, Olivier LU ; De Clercq, Inge ; Wang, Yan ; Carrie, Chris ; Xu, Lin and Kmiec, Beata , et al. (2013) In Plant Cell 25(9). p.71-3450
Abstract

Plants require daily coordinated regulation of energy metabolism for optimal growth and survival and therefore need to integrate cellular responses with both mitochondrial and plastid retrograde signaling. Using a forward genetic screen to characterize regulators of alternative oxidase1a (rao) mutants, we identified RAO2/Arabidopsis NAC domain-containing protein17 (ANAC017) as a direct positive regulator of AOX1a. RAO2/ANAC017 is targeted to connections and junctions in the endoplasmic reticulum (ER) and F-actin via a C-terminal transmembrane (TM) domain. A consensus rhomboid protease cleavage site is present in ANAC017 just prior to the predicted TM domain. Furthermore, addition of the rhomboid protease inhibitor N-p-Tosyl-l-Phe... (More)

Plants require daily coordinated regulation of energy metabolism for optimal growth and survival and therefore need to integrate cellular responses with both mitochondrial and plastid retrograde signaling. Using a forward genetic screen to characterize regulators of alternative oxidase1a (rao) mutants, we identified RAO2/Arabidopsis NAC domain-containing protein17 (ANAC017) as a direct positive regulator of AOX1a. RAO2/ANAC017 is targeted to connections and junctions in the endoplasmic reticulum (ER) and F-actin via a C-terminal transmembrane (TM) domain. A consensus rhomboid protease cleavage site is present in ANAC017 just prior to the predicted TM domain. Furthermore, addition of the rhomboid protease inhibitor N-p-Tosyl-l-Phe chloromethyl abolishes the induction of AOX1a upon antimycin A treatment. Simultaneous fluorescent tagging of ANAC017 with N-terminal red fluorescent protein (RFP) and C-terminal green fluorescent protein (GFP) revealed that the N-terminal RFP domain migrated into the nucleus, while the C-terminal GFP tag remained in the ER. Genome-wide analysis of the transcriptional network regulated by RAO2/ANAC017 under stress treatment revealed that RAO2/ANAC017 function was necessary for >85% of the changes observed as a primary response to cytosolic hydrogen peroxide (H2O2), but only ~33% of transcriptional changes observed in response to antimycin A treatment. Plants with mutated rao2/anac017 were more stress sensitive, whereas a gain-of-function mutation resulted in plants that had lower cellular levels of H2O2 under untreated conditions.

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type
Contribution to journal
publication status
published
subject
keywords
Arabidopsis, Arabidopsis Proteins, Binding Sites, Cell Nucleus, Endoplasmic Reticulum, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Reporter, Hydrogen Peroxide, Mitochondria, Mitochondrial Proteins, Mutation, Oligonucleotide Array Sequence Analysis, Oxidoreductases, Phenotype, Phylogeny, Plant Proteins, Protein Structure, Tertiary, Recombinant Fusion Proteins, Seedlings, Signal Transduction, Stress, Physiological, Transcription Factors, Transcriptome
in
Plant Cell
volume
25
issue
9
pages
22 pages
publisher
American Society of Plant Biologists
external identifiers
  • scopus:84886451548
  • pmid:24045017
ISSN
1040-4651
DOI
10.1105/tpc.113.113985
language
English
LU publication?
no
id
e1955324-6a5b-4dc2-8918-fa74b79be781
date added to LUP
2017-05-09 10:04:42
date last changed
2024-04-14 10:05:19
@article{e1955324-6a5b-4dc2-8918-fa74b79be781,
  abstract     = {{<p>Plants require daily coordinated regulation of energy metabolism for optimal growth and survival and therefore need to integrate cellular responses with both mitochondrial and plastid retrograde signaling. Using a forward genetic screen to characterize regulators of alternative oxidase1a (rao) mutants, we identified RAO2/Arabidopsis NAC domain-containing protein17 (ANAC017) as a direct positive regulator of AOX1a. RAO2/ANAC017 is targeted to connections and junctions in the endoplasmic reticulum (ER) and F-actin via a C-terminal transmembrane (TM) domain. A consensus rhomboid protease cleavage site is present in ANAC017 just prior to the predicted TM domain. Furthermore, addition of the rhomboid protease inhibitor N-p-Tosyl-l-Phe chloromethyl abolishes the induction of AOX1a upon antimycin A treatment. Simultaneous fluorescent tagging of ANAC017 with N-terminal red fluorescent protein (RFP) and C-terminal green fluorescent protein (GFP) revealed that the N-terminal RFP domain migrated into the nucleus, while the C-terminal GFP tag remained in the ER. Genome-wide analysis of the transcriptional network regulated by RAO2/ANAC017 under stress treatment revealed that RAO2/ANAC017 function was necessary for &gt;85% of the changes observed as a primary response to cytosolic hydrogen peroxide (H2O2), but only ~33% of transcriptional changes observed in response to antimycin A treatment. Plants with mutated rao2/anac017 were more stress sensitive, whereas a gain-of-function mutation resulted in plants that had lower cellular levels of H2O2 under untreated conditions.</p>}},
  author       = {{Ng, Sophia and Ivanova, Aneta and Duncan, Owen and Law, Simon R and Van Aken, Olivier and De Clercq, Inge and Wang, Yan and Carrie, Chris and Xu, Lin and Kmiec, Beata and Walker, Hayden and Van Breusegem, Frank and Whelan, James and Giraud, Estelle}},
  issn         = {{1040-4651}},
  keywords     = {{Arabidopsis; Arabidopsis Proteins; Binding Sites; Cell Nucleus; Endoplasmic Reticulum; Gene Expression Profiling; Gene Expression Regulation, Plant; Genes, Reporter; Hydrogen Peroxide; Mitochondria; Mitochondrial Proteins; Mutation; Oligonucleotide Array Sequence Analysis; Oxidoreductases; Phenotype; Phylogeny; Plant Proteins; Protein Structure, Tertiary; Recombinant Fusion Proteins; Seedlings; Signal Transduction; Stress, Physiological; Transcription Factors; Transcriptome}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{71--3450}},
  publisher    = {{American Society of Plant Biologists}},
  series       = {{Plant Cell}},
  title        = {{A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis}},
  url          = {{http://dx.doi.org/10.1105/tpc.113.113985}},
  doi          = {{10.1105/tpc.113.113985}},
  volume       = {{25}},
  year         = {{2013}},
}