Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors.

Alexey Shapiguzov,Jarkko Salojärvi,Arjun Tiwari,Maarit Hellman,Eevi Rintamäki,Saleh Alseekh,Markku Keinänen,Michael Wrzaczek,Mikael Brosché,Katrien Van Der Kelen,Bert De Rybel,Kerri Hunter,Lauri Nikkanen,Fayezeh Aarabi,Perttu Permi,Julia Krasensky-Wrzaczek,Jaakko Kangasjärvi,Sari Järvi,Nina Sipari,Helena Tossavainen,Frank Van Breusegem,Esa Tyystjärvi,Brecht Wybouw,Julia P Vainonen ,Alisdair R Fernie ,Eva‐Mari Aro

doi:10.7554/elife.43284

Abstract

Reactive oxygen species (ROS)-dependent signaling pathways from chloroplasts and mitochondria merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). RCD1 interacts in vivo and suppresses the activity of the transcription factors ANAC013 and ANAC017, which mediate a ROS-related retrograde signal originating from mitochondrial complex III. Inactivation of RCD1 leads to increased expression of mitochondrial dysfunction stimulon (MDS) genes regulated by ANAC013 and ANAC017. Accumulating MDS gene products, including alternative oxidases (AOXs), affect redox status of the chloroplasts, leading to changes in chloroplast ROS processing and increased protection of photosynthetic apparatus. ROS alter the abundance, thiol redox state and oligomerization of the RCD1 protein in vivo, providing feedback control on its function. RCD1-dependent regulation is linked to chloroplast signaling by 3'-phosphoadenosine 5'-phosphate (PAP). Thus, RCD1 integrates organellar signaling from chloroplasts and mitochondria to establish transcriptional control over the metabolic processes in both organelles.

Highlights

Cells of photosynthesizing eukaryotes are unique in harboring two types of energy organelles, the chloroplasts and the mitochondria, which interact at an operational level by the exchange of metabolites, energy and reducing power (Noguchi and Yoshida, 2008; Cardol et al, 2009; Bailleul et al, 2015)
Reactive oxygen species (ROS)-dependent signaling pathways from chloroplasts and mitochondria merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). RCD1 interacts in vivo and suppresses the activity of the transcription factors ANAC013 and ANAC017, which mediate a ROS-related retrograde signal originating from mitochondrial complex III
We demonstrate that RCD1 is a molecular component that integrates organellar signal input from both chloroplasts and mitochondria to exert its influence on nuclear gene expression

Summary

Introduction

Cells of photosynthesizing eukaryotes are unique in harboring two types of energy organelles, the chloroplasts and the mitochondria, which interact at an operational level by the exchange of metabolites, energy and reducing power (Noguchi and Yoshida, 2008; Cardol et al, 2009; Bailleul et al, 2015). The so-called retrograde signaling pathways originating from the organelles influence the expression of nuclear genes (de Souza et al, 2016; Leister, 2017; Waszczak et al, 2018). These pathways provide feedback communication between the organelles and the gene expression apparatus in the nucleus to adjust expression of genes encoding organelle components in accordance with changes in the developmental stage or environmental conditions. The immediate product of this reaction, O2 ̇–, is not likely to directly mediate organellar signaling; H2O2 is involved in many retrograde signaling pathways (Leister, 2017; Mullineaux et al, 2018; Waszczak et al, 2018). PAP is a toxic by-product of sulfate metabolism produced when cytoplasmic sulfotransferases (SOTs, e.g., SOT12)

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Conclusion