A role for SENSITIVE to FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis

School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, UK.
The Plant Journal (Impact Factor: 5.97). 06/2008; 55(5):734-45. DOI: 10.1111/j.1365-313X.2008.03549.x
Source: PubMed


The sensitive to freezing2 (SFR2) gene has an important role in freezing tolerance in Arabidopsis thaliana. We show that homologous genes are present, and expressed, in a wide range of terrestrial plants, including species not able to tolerate freezing. Expression constructs derived from the cDNAs of a number of different plant species, including examples not tolerant to freezing, are able to complement the freezing sensitivity of the Arabidopsis sfr2 mutant. In Arabidopsis the SFR2 protein is localized to the chloroplast outer envelope membrane, as revealed by the analysis of transgenic plants expressing SFR2 fusions to GFP, by confocal microscopy, and by the immunological analysis of isolated chloroplasts treated with thermolysin protease. Moreover, the chloroplasts of the sfr2 mutant show clear evidence of rapid damage after a freezing episode, suggesting a role for SFR2 in the protection of the chloroplast.

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Available from: Enrique Lopez-Juez, Sep 18, 2014
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    • "Craterostigma plantagineum presumably also contains a gene orthologous to AtDGD2, but no corresponding CpDGD2 sequence was retrieved. In Arabidopsis, SFR2, DGD1 and DGD2 are localized to the chloroplast envelope, where they have access to only a low proportion of MGDG while most of the galactolipids are in the thylakoids (Froehlich et al., 2001; Fourrier et al., 2008). Therefore, it is conceivable that only a limited proportion of MGDG can be converted into DGDG and oligogalactolipids by the DGD1/ DGD2 and SFR2 pathways. "
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    ABSTRACT: Dehydration leads to different physiological and biochemical responses in plants. We analyzed the lipid composition and the expression of genes involved in lipid biosynthesis in the desiccation-tolerant plant Craterostigma plantagineum. A comparative approach was carried out with Lindernia brevidens (desiccation tolerant), and two desiccation-sensitive species, L. subracemosa and A. thaliana. In C. plantagineum the total lipid content remained constant while the lipid composition underwent major changes during desiccation. The most prominent change was the removal of monogalactosyldiacylglycerol (MGDG) from the thylakoids. Analysis of molecular species composition revealed that around 50% of 36:x (number of carbons in the acyl chains: number of double bonds) MGDG was hydrolyzed and diacylglycerol (DAG) used for phospholipid synthesis, while another MGDG fraction was converted into digalactosyldiacylglycerol via the DGD1/DGD2 pathway and subsequently into oligogalactolipids by SFR2. 36:x-DAG was also employed for the synthesis of triacylglycerol. Phosphatidic acid (PA) increased in C. plantagineum, L. brevidens, and L. subracemosa, in agreement with a role of PA as an intermediate of lipid turnover and of phospholipase D in signalling during desiccation. 34:x-DAG, presumably derived from de novo assembly, was converted into phosphatidylinositol (PI) in C. plantagineum and L. brevidens, but not in desiccation-sensitive plants, suggesting that PI is involved in acquisition of desiccation tolerance. The accumulation of oligogalactolipids and PI in the chloroplast and extraplastidial membranes, respectively, increases the concentration of hydroxyl groups and enhances the ratio of bilayer to nonbilayer forming lipids, thus contributing to protein and membrane stabilization. This article is protected by copyright. All rights reserved.
    The Plant Journal 05/2013; 75(5). DOI:10.1111/tpj.12241 · 5.97 Impact Factor
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    • "protein (Sfr2), a galactolipid-remodeling enzyme (Fourrier et al., 2008; Moellering et al., 2010) and CRUMPLED LEAF protein (Crl) and PDV2, which are both involved in plastid division (Asano et al., 2004; Glynn et al., 2008). Additionally, we included proteins, for which significantly more peptides were found in the OE than in the IE fraction, albeit their exact localization is unclear. "
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    ABSTRACT: High-throughput protein localization studies require multiple strategies. Mass spectrometric analysis of defined cellular fractions is one of the complementary approaches to a diverse array of cell biological methods. In recent years, the protein content of different cellular (sub-)compartments was approached. Despite of all the efforts made, the analysis of membrane fractions remains difficult, in that the dissection of the proteomes of the envelope membranes of chloroplasts or mitochondria is often not reliable because sample purity is not always warranted. Moreover, proteomic studies are often restricted to single (model) species, and therefore limited in respect to differential individual evolution. In this study we analyzed the chloroplast envelope proteomes of different plant species, namely, the individual proteomes of inner and outer envelope (OE) membrane of Pisum sativum and the mixed envelope proteomes of Arabidopsis thaliana and Medicago sativa. The analysis of all three species yielded 341 identified proteins in total, 247 of them being unique. 39 proteins were genuine envelope proteins found in at least two species. Based on this and previous envelope studies we defined the core envelope proteome of chloroplasts. Comparing the general overlap of the available six independent studies (including ours) revealed only a number of 27 envelope proteins. Depending on the stringency of applied selection criteria we found 231 envelope proteins, while less stringent criteria increases this number to 649 putative envelope proteins. Based on the latter we provide a map of the outer and inner envelope core proteome, which includes many yet uncharacterized proteins predicted to be involved in transport, signaling, and response. Furthermore, a foundation for the functional characterization of yet unidentified functions of the inner and OE for further analyses is provided.
    Frontiers in Plant Science 02/2013; 4:11. DOI:10.3389/fpls.2013.00011 · 3.95 Impact Factor
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    • "LACS9 Long-chain acyl-CoA synthase AtLacs9 (At1g77590) Schnurr et al. (2002), Zhao et al. (2010) DGD Digalactosyldiacylglycerol (DGDG) synthase AtDGD1 (At3g11670), AtDGD2 (At4g00550) Dörmann et al. (1995), Dörmann et al. (1999), Härtel et al. (2000), Froehlich et al. (2001a), Kelly and Dörmann (2002), Xu et al. (2003) MGD Monogalactosyldiacyl glycerol (MGDG) synthase AtMGD2 (At5g20410), AtMGD3 (At2g11810) Miege et al. (1999), Härtel et al. (2000), Awai et al. (2001) GGGT/SFR2 Galactolipid:galactolipid galactosyltransferase AtGGGT/AtSFR2 (At3g06510) Heemskerk et al. (1983), Heemskerk et al. (1986), Kelly and Dörmann (2002), Xu et al. (2003), Thorlby et al. (2004), Fourrier et al. (2008), Moellering et al. (2010) "
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    ABSTRACT: Plastids are the defining organelles of all photosynthetic eukaryotes. They are the site of photosynthesis and of a large number of other essential metabolic pathways, such as fatty acid and amino acid biosyntheses, sulfur and nitrogen assimilation, and aromatic and terpenoid compound production, to mention only a few examples. The metabolism of plastids is heavily intertwined and connected with that of the surrounding cytosol, thus causing massive traffic of metabolic precursors, intermediates, and products. Two layers of biological membranes that are called the inner (IE) and the outer (OE) plastid envelope membranes bound the plastids of Archaeplastida. While the IE is generally accepted as the osmo-regulatory barrier between cytosol and stroma, the OE was considered to represent an unspecific molecular sieve, permeable for molecules of up to 10 kDa. However, after the discovery of small substrate-specific pores in the OE, this view has come under scrutiny. In addition to controlling metabolic fluxes between plastid and cytosol, the OE is also crucial for protein import into the chloroplast. It contains the receptors and translocation channel of the TOC complex that is required for the canonical post-translational import of nuclear-encoded, plastid-targeted proteins. Further, the OE is a metabolically active compartment of the chloroplast, being involved in, e.g., fatty acid metabolism and membrane lipid production. Also, recent findings hint on the OE as a defense platform against several biotic and abiotic stress conditions, such as cold acclimation, freezing tolerance, and phosphate deprivation. Moreover, dynamic non-covalent interactions between the OE and the endomembrane system are thought to play important roles in lipid and non-canonical protein trafficking between plastid and endoplasmatic reticulum (ER). While proteomics and bioinformatics has provided us with comprehensive but still incomplete information on proteins localized in the plastid IE, the st
    Frontiers in Plant Science 12/2011; 2:97. DOI:10.3389/fpls.2011.00097 · 3.95 Impact Factor
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