ACONITASE 3 is part of theANAC017 transcription factor-dependent mitochondrial dysfunction response

• Published in: Plant physiology (Bethesda) 2021-08, Vol.186 (4), p.1859-1877
• Main Authors: Pascual, Jesús, Rahikainen, Moona, Angeleri, Martina, Alegre, Sara, Gossens, Richard, Shapiguzov, Alexey, Heinonen, Arttu, Trotta, Andrea, Durian, Guido, Winter, Zsófia, Sinkkonen, Jari, Kangasjärvi, Jaakko, Whelan, James, Kangasjärvi, Saijaliisa
• Format: Article
• Language: English
• Subjects: Aconitate Hydratase - genetics; Aconitate Hydratase - metabolism; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Mitochondria - metabolism; Transcription Factors - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1093/plphys/kiab225

Mitochondria are tightly embedded within metabolic and regulatory networks that optimize plant performance in response to environmental challenges. The best-known mitochondrial retrograde signaling pathway involves stress-induced activation of the transcription factor NAC DOMAIN CONTAINING PROTEIN 17 (ANAC017), which initiates protective responses to stress-induced mitochondrial dysfunction in Arabidopsis (Arabidopsis thaliana). Posttranslational control of the elicited responses, however, 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 key components of stress regulation that are induced by mitochondrial dysfunction. Targeted mass spectrometry-based proteomics revealed that the abundance and phosphorylation of ACO3 increased under stress, which required signaling through ANAC017. Phosphomimetic mutation at ACO3-Ser91 and accumulation of ACO3S91D-YFP promoted the expression of genes related to mitochondrial dysfunction. Furthermore, ACO3 contributed to plant tolerance against ultraviolet B (UV-B) or antimycin A-induced mitochondrial dysfunction. These findings demonstrate that ACO3 is both a target and mediator of mitochondrial dysfunction signaling, and critical for achieving stress tolerance in Arabidopsis leaves.