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.
-
1H, 13C and 15N NMR chemical shift assignments of A. thaliana RCD1 RSTProtein Data Bank Japan, 5N9Q.
-
Gene expression analysis in wild-type and OsGRX8 overexpression line in response to various treatmentsNCBI Gene Expression Omnibus, GSE41963.
-
Expression data from pam48 (mterf6-1) mutantsNCBI Gene Expression Omnibus, GSE75824.
-
Identification of target genes of translation-dependent signalling in ArabidopsisNCBI Gene Expression Omnibus, GSE54573.
-
Gene expression from Arabidopsis under high light conditionsNCBI Gene Expression Omnibus, GSE22671.
-
Effect of oligomycin on transcript levels in Arabidopsis seedling culturesNCBI Gene Expression Omnibus, GSE38965.
-
Differential response of gun mutants to norflurazonNCBI Gene Expression Omnibus, GSE12887.
-
Expression data from Arabipdosis msh1 recA3 double mutant under heat stressNCBI Gene Expression Omnibus, GSE19603.
-
Transcription profiling by array of Arabidopsis cell cultures treated with rotenoneArrayExpress Archive of Functional Genomics Data, E-MEXP-1797.
-
Transcription profiling of Arabidopsis wild type and SAL1 mutant plants grown under normalArrayExpress Archive of Functional Genomics Data, E-MEXP-1495.
-
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.
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.
Metrics
-
- 7,875
- views
-
- 1,215
- downloads
-
- 129
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors
eLife 8:e43284.
https://doi.org/10.7554/eLife.43284
Further reading
-
- Cell Biology
- Plant Biology
Plants distribute many nutrients to chloroplasts during leaf development and maturation. When leaves senesce or experience sugar starvation, the autophagy machinery degrades chloroplast proteins to facilitate efficient nutrient reuse. Here, we report on the intracellular dynamics of an autophagy pathway responsible for piecemeal degradation of chloroplast components. Through live-cell monitoring of chloroplast morphology, we observed the formation of chloroplast budding structures in sugar-starved leaves. These buds were then released and incorporated into the vacuolar lumen as an autophagic cargo termed a Rubisco-containing body. The budding structures did not accumulate in mutants of core autophagy machinery, suggesting that autophagosome creation is required for forming chloroplast buds. Simultaneous tracking of chloroplast morphology and autophagosome development revealed that the isolation membranes of autophagosomes interact closely with part of the chloroplast surface before forming chloroplast buds. Chloroplasts then protrude at the site associated with the isolation membranes, which divide synchronously with autophagosome maturation. This autophagy-related division does not require DYNAMIN-RELATED PROTEIN 5B, which constitutes the division ring for chloroplast proliferation in growing leaves. An unidentified division machinery may thus fragment chloroplasts for degradation in coordination with the development of the chloroplast-associated isolation membrane.
-
- Plant Biology
Photosynthetic organisms exhibit remarkable diversity in their light-harvesting complexes (LHCs). LHCs are associated with photosystem I (PSI), forming a PSI-LHCI supercomplex. The number of LHCI subunits, along with their protein sequences and pigment compositions, has been found to differ greatly among the PSI-LHCI structures. However, the mechanisms by which LHCIs recognize their specific binding sites within the PSI core remain unclear. In this study, we determined the cryo-electron microscopy structure of a PSI supercomplex incorporating fucoxanthin chlorophyll a/c-binding proteins (FCPs), designated as PSI-FCPI, isolated from the diatom Thalassiosira pseudonana CCMP1335. Structural analysis of PSI-FCPI revealed five FCPI subunits associated with a PSI monomer; these subunits were identified as RedCAP, Lhcr3, Lhcq10, Lhcf10, and Lhcq8. Through structural and sequence analyses, we identified specific protein–protein interactions at the interfaces between FCPI and PSI subunits, as well as among FCPI subunits themselves. Comparative structural analyses of PSI-FCPI supercomplexes, combined with phylogenetic analysis of FCPs from T. pseudonana and the diatom Chaetoceros gracilis, underscore the evolutionary conservation of protein motifs crucial for the selective binding of individual FCPI subunits. These findings provide significant insights into the molecular mechanisms underlying the assembly and selective binding of FCPIs in diatoms.
