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Ethylene Signaling Enhances Mitochondrial Stress Tolerance Independently of ANAC017 in Arabidopsis

ABSTRACT: Mitochondria are central to plant metabolism, yet the diversity of mechanisms plants use to cope with mitochondrial stress and its implications as a cellular signal are not fully understood. In this study, we analyzed Arabidopsis noxy (non-responding to oxylipins) mutants affected in mitochondrial function and ethylene (ET) signaling to dissect plant responses to diverse mitochondrial stresses, including inhibitors of all electron transport chain complexes and mitochondrial translation. All noxy mutants showed resistance to antimycin A (AA), implicating Complex III and oxylipin signaling in mitochondrial stress adaptation. Notably, noxy22/eto1-14, an ET overproducer mutant, displayed broad resistance to all tested inhibitors independently of the canonical mitochondrial retrograde pathway mediated by ANAC017, suggesting a protective role for constitutive ET production. RNA-seq analysis revealed that AA induced ANAC017-regulated genes early and independently of ET signaling, whereas EIN2 was required for later induction of AA-associated defense responses, suggesting that mitochondrial disturbances signal environmental stress through the ET pathway. Accordingly, EIN2 contributed to AA-induced resistance to the biotrophic pathogen Hyaloperonospora arabidopsidis, but not to the necrotroph Plectosphaerella cucumerina. Collectively, our findings point to a complex network that coordinates distinct but overlapping responses to mitochondrial dysfunction and integrates them into broader stress and immune signaling pathways.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE299881 | GEO | 2026/02/28

REPOSITORIES: GEO

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Ethylene Signaling Enhances Mitochondrial Stress Tolerance Independently of ANAC017 in Arabidopsis

Project description:Ethylene Signaling Enhances Mitochondrial Stress Tolerance Independently of ANAC017 in Arabidopsis

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Project description:Mitochondria are tightly embedded within metabolic and regulatory networks that optimize plant performance upon environmental challenges. The best-known mitochondrial retrograde signaling pathway involves stress-induced activation of the transcription factor ANAC017, which mediates the onset of protective responses upon stress-induced mitochondrial dysfunction in Arabidopsis. Post-translational control of the elicited responses, in contrast, remains poorly understood. Previous studies linked protein phosphatase 2A subunit PP2A-B’γ, a key negative regulator of stress responses, with reversible phosphorylation of ACONITASE 3 (ACO3). Here we report on ACO3 and its phosphorylation at Ser91 as regulatory components induced by mitochondrial dysfunction. Targeted mass spectrometry-based proteomics revealed that the abundance and phosphorylation of ACO3 increased under stress, and that this required signaling through ANAC017. Phosphomimetic mutation at ACO3-Ser91 and the accumulation of ACO3S91D-YFP, in turn, promoted the expression of stress related genes and ACO3 function associated with plant tolerance against UV-B or antimycin A-induced mitochondrial dysfunction. These findings positioned ACO3 both as a target and modulator of mitochondrial dysfunction signaling, critical in the attainment of stress tolerance in Arabidopsis leaves.

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Retrograde signalling during caused by heritable mitochondrial dysfunction is partly mediated by ANAC017 and improves plant performance.

Project description:Mitochondria are crucial for plant viability and are able to communicate information on their functional status to the cellular nucleus via retrograde signalling, thereby affecting gene expression. It is currently unclear if retrograde signalling in response to constitutive mitochondrial biogenesis defects is mediated by the same pathways as those triggered during acute mitochondrial dysfunction. Furthermore, it is unknown if retrograde signalling can effectively improve plant performance when mitochondrial function is constitutively impaired. Here we show that retrograde signalling in mutants defective in mitochondrial proteins RNA polymerase rpotmp or prohibitin atphb3 can be suppressed by knocking out the transcription factor ANAC017. Genome-wide RNA-seq expression analysis revealed that ANAC017 is almost solely responsible for the most dramatic transcriptional changes common to rpotmp and atphb3 mutants, regulating both classical marker genes such as alternative oxidase 1a (AOX1a) and also previously-uncharacterised DUF295 genes that appear to be new retrograde markers. In contrast, ANAC017 does not regulate intra-mitochondrial gene expression or transcriptional changes unique to either rpotmp or atphb3 genotype, suggesting the existence of currently unknown signalling cascades. The data show that the role of ANAC017 extends beyond common retrograde transcriptional responses and affects downstream protein abundance and enzyme activity of alternative oxidase, as well as steady state energy metabolism in atphb3 plants. Furthermore, detailed growth analysis revealed that ANAC017-dependent retrograde signalling provides benefits for growth and productivity in plants with mitochondrial defects. In conclusion, ANAC017 plays a key role in both biogenic and operational mitochondrial retrograde signalling, and improves plant performance when mitochondrial function is constitutively impaired.

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ACONITASE 3 is part of the ANAC017 transcription factor-dependent mitochondrial dysfunction response

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