The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis    

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.

Decreasing Electron Flux through the Cytochrome and/or Alternative Respiratory Pathways Triggers Common and Distinct Cellular Responses Dependent on Growth Conditions

“…Under normal growth conditions, aox1a:rpoTmp seems to have already initiated a mitochondrial stress response, which is evidenced by the increase in transcript abundance of several transcription factors from the NAC and WRKY families that have been previously shown to mediate mitochondrial stress responses (Ng et al, 2014). In particular, NAC013, which has been shown to be involved in regulation of the mitochondrial stress response (De Clercq et al, 2013) and also defined as a mitochondrial stress marker (Schwarzländer et al, 2012), was induced 26-fold, far more than what was previously observed after stress treatments. In fact, 8 of 11 transcripts that are markers of mitochondrial stress are all induced in the aox1a:rpoTmp mutant under standard growth conditions (Schwarzländer et al, 2012).…”

“…Finally, seven membrane-bound NAC transcription factors (ANAC013, At13328700; ANAC014, At1g33060; ANAC016, At1g34180; ANAC042, At2g43000; ANAC053, At3g10500; ANAC069, At4g01550; and ANAC089, At5g22290) that are involved in mediating mitochondrial retrograde signaling ( Fig. 10A; De Clercq et al, 2013;Ng et al, 2013aNg et al, , 2013b were also commonly up-regulated.…”

“…10A). It has been shown that NAC013 is responsible for inducing a mitochondrial retrograde response by binding to the promoters of genes that contain a mitochondrial dysfunction motif (De Clercq et al, 2013). NAC013 is a marker for mitochondrial dysfunction (Schwarzländer et al, 2012), and it is induced by H 2 O 2 (Inzé et al, 2012).…”

FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis

“…In addition to these classes, we also observed regulation of Abiotic Stress, Redox, and Tricarboxylic Acid Cycle ( Table I) that can be clearly linked to mitochondrial dysfunction. Interestingly, significant regulation was also determined for Transcription, including by the NAC (for NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON) domain superfamily of transcription factors, members of which have been implicated in mitochondrial retrograde signaling (Tran et al, 2004;Chen et al, 2008;Nakashima et al, 2012;De Clercq et al, 2013;Ng et al, 2013).…”

Subgroup-specific intrinsic disorder profiles of arabidopsis NAC transcription factors: Identification of functional hotspots

“…These NAC proteins function in oxidative stress responses. [21][22][23] and ANAC0013 and ANAC017 may mediate crosstalk between oxidative stress-responsive signaling pathways and mitochondrial retrograde regulation, 21,23 whereas ANAC016 may connect stress-signaling and senescence. 22 Whether the newly identified conserved sequence motif (EF)/ MoRF is implicated in a common interaction and biological function remains to be studied.…”