The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth

Abstract

In plant cells, mitochondria are ideally positioned to sense and balance changes in energy metabolism in response to changing environmental conditions. Retrograde signalling from mitochondria to the nucleus is crucial for adjusting the required transcriptional responses. We show that ANAC017, the master regulator of mitochondrial stress, directly recruits a signalling cascade involving the plant hormones ethylene and auxin as well as the MAP KINASE KINASE (MKK) 9 - MAP KINASE (MPK) 3/6 pathway in Arabidopsis thaliana. Chromatin immunoprecipitation followed by sequencing (ChIP-seq) and overexpression demonstrated that ANAC017 directly regulates several genes of the ethylene and auxin pathways, including MKK9, 1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2 and YUCCA 5, in addition to genes encoding transcription factors regulating plant growth and stress responses such as BASIC REGION/LEUCINE ZIPPER MOTIF (bZIP) 60, bZIP53, ANAC081/ATAF2 and RADICAL-INDUCED CELL DEATH1. A time-resolved RNA-seq experiment established that ethylene signalling precedes the stimulation of auxin signalling in the mitochondrial stress response, with a large part of the transcriptional regulation dependent on ETHYLENE INSENSITIVE 3. These results were confirmed by mutant analyses. Our findings identify the molecular components controlled by ANAC017, which integrates the primary stress responses to mitochondrial dysfunction with whole plant growth via the activation of regulatory and partly antagonistic feedback loops.

Co-regulation of mitochondrial and chloroplast function: Molecular components and mechanisms

“…ANAC017 and ANAC013 are required to activate the mitochondrial stress response, which is essential for oxidation of excess chloroplast reducing equivalents ( Chadee et al., 2021 ). ANAC017 directly binds to the promoter of RCD1, positively regulating its expression ( He et al., 2022 ) ( Figure 2 ). RCD1 directly binds ANAC017 and ANAC013 and inhibits their activity in the nucleus ( Shapiguzov et al., 2019 ).…”

“…There are several other direct molecular links between the ANAC pathway and chloroplast function. Chromatin immunoprecipitation sequencing analysis of the direct targets of ANAC017 revealed that it binds to the promoter of MITOGEN-ACTIVATED PROTEIN KINASE KINASE 9, which activates the MITOGEN-ACTIVATED PROTEIN KINASE (MPK) 3/MPK6 pathway and ethylene signaling ( He et al., 2022 ) ( Figure 2 ). This acts as a convergence point with the ability of ethylene to repress photomorphogenesis ( Gommers et al., 2021 ).…”

Metabolism and Signaling of Plant Mitochondria in Adaptation to Environmental Stresses

“…In addition to expression data, ANAC017-based signaling has been shown to independently contribute to submergence and hypoxia tolerance [ 53 , 122 ]. It was recently shown that ANAC017 directly recruits a signaling cascade involving the plant hormones ethylene and auxin [ 123 ]. In parallel, it was previously shown that ethylene enhances HB1 expression, which in turn reduces NO levels and stabilizes ERFVIIs [ 124 ].…”

Aux/IAA11 Is Required for UV-AB Tolerance and Auxin Sensing in Arabidopsis thaliana

“…It was observed that induction of mitochondrial stress results in transient suppression of auxin signaling [ 1 , 40 ]. On the other hand, perturbation of auxin transport and biosynthesis induced expression of mitochondrial retrograde signaling markers [ 41 , 42 ]. Thus, it is suggested that auxin signaling and mitochondrial retrograde signaling operate antagonistically [ 41 , 42 ].…”