A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses O2-induced cell death

Institute of Plant Sciences, Plant Genetics, ETH Zurich, CH - 8092 Zurich, Switzerland.
The Plant Journal (Impact Factor: 5.97). 07/2009; 60(3):399-410. DOI: 10.1111/j.1365-313X.2009.03965.x
Source: PubMed


The conditional flu mutant of Arabidopsis thaliana generates singlet oxygen ((1)O(2)) in plastids during a dark-to-light shift. Seedlings of flu bleach and die, whereas mature plants stop growing and develop macroscopic necrotic lesions. Several suppressor mutants, dubbed singlet oxygen-linked death activator (soldat), were identified that abrogate (1)O(2)-mediated cell death of flu seedlings. One of the soldat mutations, soldat10, affects a gene encoding a plastid-localized protein related to the human mitochondrial transcription termination factor mTERF. As a consequence of this mutation, plastid-specific rRNA levels decrease and protein synthesis in plastids of soldat10 is attenuated. This disruption of chloroplast homeostasis in soldat10 seedlings affects communication between chloroplasts and the nucleus and leads to changes in the steady-state concentration of nuclear gene transcripts. The soldat10 seedlings suffer from mild photo-oxidative stress, as indicated by the constitutive up-regulation of stress-related genes. Even though soldat10/flu seedlings overaccumulate the photosensitizer protochlorophyllide in the dark and activate the expression of (1)O(2)-responsive genes after a dark-to-light shift they do not show a (1)O(2)-dependent cell death response. Disturbance of chloroplast homeostasis in emerging soldat10/flu seedlings seems to antagonize a subsequent (1)O(2)-mediated cell death response without suppressing (1)O(2)-dependent retrograde signaling. The results of this work reveal the unexpected complexity of what is commonly referred to as 'plastid signaling'.

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    • "The mTERF family in plants is considerably larger than in Metazoa; for example, A. thaliana and Oryza sativa Japonica contain at least 35 and 48 genes for mTERF proteins, respectively (Babiychuk et al., 2011;Kleine et al., 2012), all of which are predicted or known to localize to mitochondria or chloroplasts (Babiychuk et al., 2011;Kleine, 2012). So far, only four plastid mTERFs—SOLDAT10, BSM, ZmmTERF4, and TWIRT1/mTERF9—have been identified and functionally characterized (Meskauskiene et al., 2009;Babiychuk et al., 2011;Mokry et al., 2011;Quesada et al., 2011). In this study, we described coe1 as a new allele of bsm/rug2/Zmmterf4 that causes similar defects in the accumulation of chloroplast proteins and the biogenesis of chloroplasts (Fig. 4). "
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    ABSTRACT: Plastid-to-nucleus retrograde signaling plays an important role in regulating the expression of photosynthesis-associated nuclear genes (PhANGs) in accordance with physiological demands on chloroplast biogenesis and function. Despite its fundamental importance, little is known about the molecular nature of the plastid gene expression (PGE)-dependent type of retrograde signaling. PGE is a multifaceted process, and several factors, including pentatricopeptide repeat (PPR) proteins, are involved in its regulation. The PPR protein GUN1 plays a central role in PGE-dependent retrograde signaling. In this study, we isolated a mutant exhibiting up-regulation of CHLOROPHYLL A/B-BINDING PROTEIN (CAB) under normal growth conditions (named coe1 for CAB overexpression 1). The coe1 mutant has a single-base mutation in the gene for mitochondrial transcription termination factor 4 (mTERF4)/BSM/RUG2, which plays a role in regulating the processing of certain plastid transcripts. Defects in GUN1 or mTERF4 de-repressed the expression of specific plastid mRNAs in the presence of lincomycin (LIN). In wild-type plants, treatment with LIN or spectinomycin (SPE) inhibited processing of plastid transcripts. Comparative analysis revealed that in gun1 and coe1/mterf4, but not in wild-type, gun4, or gun5 plants, the processing of plastid transcripts and expression levels of Lhcb1 mRNA were affected in opposite ways when plants were grown in the presence of LIN or SPE. In addition, the coe1 mutation affected the intracellular accumulation and distribution of GUN1, as well as its plastid signaling activity. Taken together, these results suggest that GUN1 and COE1 cooperate in PGE and retrograde signaling.
    Full-text · Article · Dec 2015 · Journal of Experimental Botany
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    • "In this way, the singlet oxygen pathway initially discovered with the flu mutants (Meskauskiene et al., 2001) and refined by the identification of suppressor mutants (Meskauskiene et al., 2009) appears to take part in a cell death programme under stress, but also possibly participates in retrograde signalling in operational control (Triantaphylidès and Havaux, 2009). 1 O 2 released in the flu mutant activates genes of the JA pathway (op den Camp, 2003) and triggers cell death in an executer-dependent manner (Kim et al., 2012) (Fig. 3). By genetic analysis, Mühlenbock et al. (2008) assigned a linkage function to chloroplast signalling which enables mutual crosstalk between light acclimation and plant immunity. "
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    ABSTRACT: Like no other chemical or physical parameter, the natural light environment of plants changes with high speed and jumps of enormous intensity. To cope with this variability, photosynthetic organisms have evolved sensing and response mechanisms that allow efficient acclimation. Most signals originate from the chloroplast itself. In addition to very fast photochemical regulation, intensive molecular communication is realized within the photosynthesizing cell, optimizing the acclimation process. Current research has opened up new perspectives on plausible but mostly unexpected complexity in signalling events, crosstalk, and process adjustments. Within seconds and minutes, redox states, levels of reactive oxygen species, metabolites, and hormones change and transmit information to the cytosol, modifying metabolic activity, gene expression, translation activity, and alternative splicing events. Signalling pathways on an intermediate time scale of several minutes to a few hours pave the way for long-term acclimation. Thereby, a new steady state of the transcriptome, proteome, and metabolism is realized within rather short time periods irrespective of the previous acclimation history to shade or sun conditions. This review provides a time line of events during six hours in the 'stressful' life of a plant. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email:
    Full-text · Article · Jan 2015 · Journal of Experimental Botany
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    • "Remarkably, all of the A. thaliana mTERF proteins so far described in the literature (Pfalz et al., 2006; Meskauskiene et al., 2009; Babiychuk et al., 2011; Mokry et al., 2011; Quesada et al., 2011)—SOLDAT10, BSM/RUG2, TWIRT1, and PTAC15—belong to this group. The embryo lethality of soldat10 (Meskauskiene et al., 2009), bsm (Babiychuk et al., 2011), and at2g21710 (emb2219) (Tzafrir et al., 2004) mutants, and the gametophyte lethality seen in the mterf5 (at4g14605) mutant (Babiychuk et al., 2011), point to a role for this group of mTERF proteins in important developmental processes . Furthermore, of the eight mTERF proteins identified in maize nucleoids that show homology to A. thaliana mTERFs (Majeran et al., 2011), six belong to this group (Table 1), again suggesting that these mTERF proteins are critical for chloroplast gene expression (Figure 2A). "
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    ABSTRACT: Organellar gene expression (OGE) is crucial for plant development, photosynthesis and respiration, but our understanding of the mechanisms that control it is still relatively poor. Thus, OGE requires various nucleus-encoded proteins that promote transcription, splicing, trimming and editing of organellar RNAs, and regulate translation. In metazoans, proteins of the mitochondrial Transcription tERmination Factor (mTERF) family interact with the mitochondrial chromosome and regulate transcriptional initiation and termination. Sequencing of the Arabidopsis thaliana genome led to the identification of a diversified MTERF gene family but, in contrast to mammalian mTERFs, knowledge about the function of these proteins in photosynthetic organisms is scarce. In this hypothesis article, I show that tandem duplications and one block duplication contributed to the large number of MTERF genes in A. thaliana, and propose that the expansion of the family is related to the evolution of land plants. The MTERF genes - especially the duplicated genes - display a number of distinct mRNA accumulation patterns, suggesting functional diversification of mTERF proteins to increase adaptability to environmental changes. Indeed, hypothetical functions for the different mTERF proteins can be predicted using co-expression analysis and gene ontology annotations. On this basis, mTERF proteins can be sorted into five groups. Members of the “chloroplast” and “chloroplast-associated” clusters are principally involved in chloroplast gene expression, embryogenesis and protein catabolism, while representatives of the “mitochondrial” cluster seem to participate in DNA and RNA metabolism in that organelle. Moreover, members of the “mitochondrion-associated” cluster and the “low expression” group may act in the nucleus and/or the cytosol. As proteins involved in OGE and presumably nuclear gene expression, mTERFs are ideal candidates for the coordination of the expression of organelle and nuclear genomes.
    Preview · Article · Oct 2012 · Frontiers in Plant Science
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