Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors
- University of Helsinki, Finland
- University of Turku, Finland
- University of Jyväskylä, Finland
- Max-Planck Institute for Molecular Plant Physiology, Germany
- Ghent University, Belgium
- University of Eastern Finland, Finland
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.
Data availability
The atomic coordinates and structural restraints for the C-terminal domain of RCD1 have been deposited in the Protein Data Bank with the accession code 5N9Q.
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1H, 13C and 15N NMR chemical shift assignments of A. thaliana RCD1 RSTProtein Data Bank Japan, 5N9Q.
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Gene expression analysis in wild-type and OsGRX8 overexpression line in response to various treatmentsNCBI Gene Expression Omnibus, GSE41963.
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Expression data from pam48 (mterf6-1) mutantsNCBI Gene Expression Omnibus, GSE75824.
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Identification of target genes of translation-dependent signalling in ArabidopsisNCBI Gene Expression Omnibus, GSE54573.
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Gene expression from Arabidopsis under high light conditionsNCBI Gene Expression Omnibus, GSE22671.
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Effect of oligomycin on transcript levels in Arabidopsis seedling culturesNCBI Gene Expression Omnibus, GSE38965.
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Differential response of gun mutants to norflurazonNCBI Gene Expression Omnibus, GSE12887.
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Expression data from Arabipdosis msh1 recA3 double mutant under heat stressNCBI Gene Expression Omnibus, GSE19603.
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Transcription profiling by array of Arabidopsis cell cultures treated with rotenoneArrayExpress Archive of Functional Genomics Data, E-MEXP-1797.
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Transcription profiling of Arabidopsis wild type and SAL1 mutant plants grown under normalArrayExpress Archive of Functional Genomics Data, E-MEXP-1495.
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Transcription profiling of Arabidopsis wild type and complex I mutant plantsArrayExpress Archive of Functional Genomics Data, E-MEXP-1967.
Article and author information
Author details
Julia Krasensky-Wrzaczek
Jaakko Kangasjarvi
Funding
Helsingin Yliopisto
- Jaakko Kangasjarvi
Suomen Akatemia
- Jarkko Salojärvi
- Eva-Mari Aro
- Michael Wrzaczek
- Jaakko Kangasjarvi
Fonds Wetenschappelijk Onderzoek
- Brecht Wybouw
- Bert De Rybel
- Frank van Breusegem
Deutsche Forschungsgemeinschaft
- Fayezeh Aarabi
- Alisdair R Fernie
Horizon 2020 Framework Programme
- Saleh Alseekh
- Alisdair R Fernie
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Christian S Hardtke, University of Lausanne, Switzerland
Version history
- Received: November 8, 2018
- Accepted: February 14, 2019
- Accepted Manuscript published: February 15, 2019 (version 1)
- Version of Record published: March 12, 2019 (version 2)
Copyright
© 2019, Shapiguzov et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors
eLife 8:e43284.
https://doi.org/10.7554/eLife.43284
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Transmembrane signaling by plant receptor kinases (RKs) has long been thought to involve reciprocal trans-phosphorylation of their intracellular kinase domains. The fact that many of these are pseudokinase domains, however, suggests that additional mechanisms must govern RK signaling activation. Non-catalytic signaling mechanisms of protein kinase domains have been described in metazoans, but information is scarce for plants. Recently, a non-catalytic function was reported for the leucine-rich repeat (LRR)-RK subfamily XIIa member EFR (elongation factor Tu receptor) and phosphorylation-dependent conformational changes were proposed to regulate signaling of RKs with non-RD kinase domains. Here, using EFR as a model, we describe a non-catalytic activation mechanism for LRR-RKs with non-RD kinase domains. EFR is an active kinase, but a kinase-dead variant retains the ability to enhance catalytic activity of its co-receptor kinase BAK1/SERK3 (brassinosteroid insensitive 1-associated kinase 1/somatic embryogenesis receptor kinase 3). Applying hydrogen-deuterium exchange mass spectrometry (HDX-MS) analysis and designing homology-based intragenic suppressor mutations, we provide evidence that the EFR kinase domain must adopt its active conformation in order to activate BAK1 allosterically, likely by supporting αC-helix positioning in BAK1. Our results suggest a conformational toggle model for signaling, in which BAK1 first phosphorylates EFR in the activation loop to stabilize its active conformation, allowing EFR in turn to allosterically activate BAK1.
