Modification of the Water Oxidizing Complex in Leaves of the <i>dgd1</i> Mutant of <i>Arabidopsis thaliana</i> Deficient in the Galactolipid Digalactosyldiacylglycerol

Reifarth, F.; Christen, G.; Ag, Seeliger; Dörmann, Peter; Benning, Christoph; Ренгер, Г.

doi:10.1021/bi9709654

Cited by 72 publications

(54 citation statements)

References 40 publications

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“…Structural analysis of crystallized protein complexes revealed that galactolipids are also found within the structures of PSI and PSII, light-harvesting complex II (LHCII), and cytochrome b 6 /f (Jordan et al, 2001;Stroebel et al, 2003;Liu et al, 2004;Loll et al, 2005;Jones, 2007). MGD and DGD play crucial roles in photosynthetic light reactions, and this is in agreement with results obtained from the analysis of galactolipid-deficient Arabidopsis (Arabidopsis thaliana) mutants (Härtel et al, 1997;Reifarth et al, 1997;Guo et al, 2005). The dgd1 mutant of Arabidopsis contains approximately one-tenth of the wild-type amount of DGD (Dö rmann et al, 1995).…”

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confidence: 86%

The Role of Diglycosyl Lipids in Photosynthesis and Membrane Lipid Homeostasis in Arabidopsis

et al. 2009

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The galactolipid digalactosyldiacylglycerol (DGD) is an abundant thylakoid lipid in chloroplasts. The introduction of the bacterial lipid glucosylgalactosyldiacylglycerol (GGD) from Chloroflexus aurantiacus into the DGD-deficient Arabidopsis (Arabidopsis thaliana) dgd1 mutant was previously shown to result in complementation of growth, but photosynthetic efficiency was only partially restored. Here, we demonstrate that GGD accumulation in the double mutant dgd1dgd2, which is totally devoid of DGD, also complements growth at normal and high-light conditions, but photosynthetic efficiency in the GGD-containing dgd1dgd2 line remains decreased. This is attributable to an increased susceptibility of photosystem II to photodamage, resulting in reduced photosystem II accumulation already at normal light intensities. The chloroplasts of dgd1 and dgd1dgd2 show alterations in thylakoid ultrastructure, a phenotype that is restored in the GGD-containing lines. These data suggest that the strong growth retardation of the DGD-deficient lines dgd1 and dgd1dgd2 can be primarily attributed to a decreased capacity for chloroplast membrane assembly and proliferation and, to a smaller extent, to photosynthetic deficiency. During phosphate limitation, GGD increases in plastidial and extraplastidial membranes of the transgenic lines to an extent similar to that of DGD in the wild type, indicating that synthesis and transport of the bacterial lipid (GGD) and of the authentic plant lipid (DGD) are subject to the same mechanisms of regulation.Higher plants contain two galactolipids, monogalactosyldiacylglycerol (MGD) and digalactosyldiacylglycerol (DGD), that constitute about 75 mol % of the thylakoid lipids in chloroplasts (Benson, 1971;Joyard et al., 1998; Dörmann and Benning, 2002). MGD and DGD are synthesized from UDP-Gal and diacylglycerol by MGD and DGD synthases in the chloroplast envelope membranes. While MGD is mostly produced from diacylglycerol originating from the plastid (''prokaryotic lipid''), DGD is largely derived from endoplasmic reticulum (ER) lipid precursors (''eukaryotic lipid'';Heinz and Roughan, 1983;Browse et al., 1986b). The lipid transport from the ER to the plastid is not well understood. However, recent results suggest that an ATP-binding cassette-type transport complex is involved in the transfer of eukaryotic lipids from the ER to the chloroplast (Xu et al., 2003). Galactolipids do not only establish the lipid bilayer into which the photosynthetic complexes are embedded. Structural analysis of crystallized protein complexes revealed that galactolipids are also found within the structures of PSI and PSII, light-harvesting complex II (LHCII), and cytochrome b 6 /f (Jordan et al., 2001;Stroebel et al., 2003;Liu et al., 2004;Loll et al., 2005;Jones, 2007). MGD and DGD play crucial roles in photosynthetic light reactions, and this is in agreement with results obtained from the analysis of galactolipid-deficient Arabidopsis (Arabidopsis thaliana) mutants (Härtel et al., 1997;Reifarth et al., 1997;Guo et al., 2...

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confidence: 86%

The Role of Diglycosyl Lipids in Photosynthesis and Membrane Lipid Homeostasis in Arabidopsis

et al. 2009

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“…This might be one explanation for the fact that ␣Gal␤GalDG is the preferred dihexosyldiacylglycerol lipid for the functional stabilization of pigment-protein complexes. In addition, ␣Gal␤GalDG deficiency in the dgd1 mutant was previously shown to affect the integrity of PSI, PSII, and the oxygen evolving complex (37,38). Furthermore, ␣Gal␤GalDG was recently identified in the crystal structure of PSII, and it is possible that this lipid is involved in PSII dimerization (39).…”

Section: Discussionmentioning

confidence: 98%

Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants

Hölzl

Witt

Kelly

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Galactolipids represent the most abundant lipid class in thylakoid membranes, where oxygenic photosynthesis is performed. The identification of galactolipids at specific sites within photosynthetic complexes by x-ray crystallography implies specific roles for galactolipids during photosynthetic electron transport. The preference for galactose and not for the more abundant sugar glucose in thylakoid lipids and their specific roles in photosynthesis are not understood. Introduction of a bacterial glucosyltransferase from Chloroflexus aurantiacus into the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana resulted in the accumulation of a glucose-containing lipid in the thylakoids. At the same time, the growth defect of the dgd1 mutant was complemented. However, the degree of trimerization of light-harvesting complex II and the photosynthetic quantum yield of transformed dgd1 plants were only partially restored. These results indicate that specific interactions of the galactolipid head group with photosynthetic protein complexes might explain the preference for galactose in thylakoid lipids of higher plants. Therefore, galactose in thylakoid lipids can be exchanged with glucose without severe effects on growth, but the presence of galactose is crucial to maintain maximal photosynthetic efficiency.chloroplast ͉ galactose ͉ glucose ͉ lipid ͉ glucosylgalactosyldiacylglycerol D irectly or indirectly, almost all life on earth depends on the photosynthetic conversion of water, CO 2 , and sunlight into chemical energy and oxygen. In cyanobacteria, green algae, and plants, the primary reactions of oxygenic photosynthesis are executed in thylakoid membranes. They harbor a set of multimeric protein complexes embedded into a lipid matrix of unique composition. The structure of the protein complexes and the lipid composition of thylakoid membranes are highly conserved in all organisms performing oxygenic photosynthesis. Thylakoid lipids comprise the two galactolipids monogalactosyldiacylglycerol (␤GalDG) and digalactosyldiacylglycerol (␣Gal␤GalDG), a sulfolipid, and phosphatidylglycerol as the only phospholipid (1-3). Based on their high proportion in thylakoid membranes and the abundance of plants and algae, galactolipids represent the most abundant lipid class in the biosphere (4, 5). Galactolipids are crucial to establish the proton-and ion-impermeable matrix of chloroplast membranes. An appropriate ratio of ␤GalDG to ␣Gal␤GalDG is required to maintain the intricate bilayer characteristics required for insertion, folding, movement, and conformational changes of membrane proteins (6). Crystalline chlorophyll-protein complexes contain galactolipid molecules firmly bound to specific sites, some of them in close proximity to the electron transfer chain. This association implies important roles of galactolipids in photosynthetic exciton and electron transfer within and between the different complexes (7-9). Mutants and transgenic plants of Arabidopsis thaliana are the basis for our current understanding of the role of th...

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“…For these experiments data were collected between 150 s to 60 s following a single saturating flash. Data were analyzed using the equations outlined previously (23). In this mathematical treatment, three exponential decay components and a long-lived ( Ͼ 10 s) residual component were included.…”

Section: Methodsmentioning

confidence: 99%

The PsbP Protein Is Required for Photosystem II Complex Assembly/Stability and Photoautotrophy in Arabidopsis thaliana

Hargett

Liu

et al. 2007

Journal of Biological Chemistry

114

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Interfering RNA was used to suppress the expression of the genes At1g06680 and At2g30790 in Arabidopsis thaliana, which encode the PsbP-1 and PsbP-2 proteins, respectively, of photosystem II (PS II In higher plants, algae, and cyanobacteria, at least six intrinsic proteins appear to be required for oxygen evolution by PS II 2 (1-3). These are CP47, CP43, the D1 and D2 proteins, and the ␣ and ␤ subunits of cytochrome b 559 . Insertional inactivation or deletion of the genes for these components results in the disassembly of the PS II complex and the complete loss of oxygen evolution activity (for review, see Ref. 4). Additionally, a number of low molecular mass, intrinsic membrane protein components are associated with PS II (5-7), although the functions of many of these proteins remain obscure. Although PS II complexes containing only these intrinsic components can evolve oxygen in vitro, they do so at low rates (ϳ25-40% of control), are extremely susceptible to photoinactivation, and require high, nonphysiological levels of calcium and chloride for maximal activity (1, 3).)In higher plants and green algae, three extrinsic proteins, with apparent molecular masses of 33, 24, and 17 kDa, are required for high rates of oxygen evolution at physiological inorganic cofactor concentrations. The 33-kDa component, the PsbO protein, has been termed the manganese-stabilizing protein due to its stabilization of the manganese cluster during exposure to low chloride concentrations or to exogenous reductants. In vitro, the 24-and 17-kDa proteins (termed the PsbP and PsbQ proteins, respectively) appear to modulate the calcium and chloride requirements for efficient oxygen evolution. The precise roles of these proteins in oxygen evolution and PS II assembly/stability in vivo, however, remain unclear. These three extrinsic components interact with intrinsic membrane proteins and possibly with each other to yield fully functional oxygen-evolving complexes.The mature PsbP protein is highly conserved (8) in higher plants. In Arabidopsis, there are two putative genes, At1g06680 and At2g30790, which encode PsbP-1 and PsbP-2, respectively. It should be noted that initially only PsbP-1 was observed in Arabidopsis (9, 10) using two-dimensional IEF-SDS-PAGE. Recently, however, PsbP-2 has been detected during two-dimensional difference gel electrophoresis (11). In the cyanobacterium Synechocystis 6803, mutants in which the homologue of the psbP gene had been deleted exhibited reduced photoautotrophic growth as well as decreased water oxidation activity under CaCl 2 -limiting conditions (7, 12), whereas in Chlamydomonas, a mutant which did not accumulate PsbP was deficient in photoactivation (13).RNAi is a post-transcriptional gene-silencing process in which double-stranded RNA induces the degradation of homologous mRNA sequences (14). RNAi has been successfully applied as a powerful gene-silencing tool in a variety of organisms, including Caenorhabditis elegans and Drosophila melanogaster, and in mouse oocytes. It has also become a pop-* T...

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Modification of the Water Oxidizing Complex in Leaves of the dgd1 Mutant of Arabidopsis thaliana Deficient in the Galactolipid Digalactosyldiacylglycerol

Cited by 72 publications

References 40 publications

The Role of Diglycosyl Lipids in Photosynthesis and Membrane Lipid Homeostasis in Arabidopsis

The Role of Diglycosyl Lipids in Photosynthesis and Membrane Lipid Homeostasis in Arabidopsis

Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants

The PsbP Protein Is Required for Photosystem II Complex Assembly/Stability and Photoautotrophy in Arabidopsis thaliana

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