Genetic modification of the fatty acid unsaturation of phosphatidylglycerol in chloroplasts alters the sensitivity of tobacco plants to cold stress

Sakamoto, Atsushi; Sulpice, Ronan; Hou, Can; Kinoshita, Mikio; Higashi, Satoru; Kanaseki, Takeshi; Nonaka, Hideko; Moon, Byoung Yong; Murata, Norio

doi:10.1046/j.0016-8025.2003.01131.x

Cited by 43 publications

(26 citation statements)

References 11 publications

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“…In agreement with this, coldtolerant species (Sakamoto et al, 2004;De Palma et al, 2008) and varieties (Horvath et al, 1983) and cold-acclimated plants (Degenkolbe et al, 2012) have been shown to have relatively high levels of desaturated glycerolipids. Changes in glycerolipid saturation levels are also accompanied by other more specific effects, such as a decrease of monogalactosyldiacylglycerols (MGDGs) (Li et al, 2008) and an increase of triacylglycerides (TAGs) connected with the outer chloroplast envelope remodeling mediated by galactolipid:galactolipid galactosyltransferase (Moellering and Benning, 2011).…”

Section: Introductionsupporting

confidence: 61%

Linking Gene Expression and Membrane Lipid Composition ofArabidopsis

et al. 2014

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Glycerolipid metabolism of plants responds dynamically to changes in light intensity and temperature, leading to the modification of membrane lipid composition to ensure optimal biochemical and physical properties in the new environment. Although multiple posttranscriptional regulatory mechanisms have been reported to be involved in the process, the contribution of transcriptional regulation remains largely unknown. Here, we present an integrative analysis of transcriptomic and lipidomic data, revealing large-scale coordination between gene expression and changes in glycerolipid levels during the Arabidopsis thaliana response to light and temperature stimuli. Using a multivariate regression technique called O2PLS, we show that the gene expression response is strictly coordinated at the biochemical pathway level and occurs in parallel with changes of specific glycerolipid pools. Five interesting candidate genes were chosen for further analysis from a larger set of candidates identified based on their close association with various groups of glycerolipids. Lipidomic analysis of knockout mutant lines of these five genes showed a significant relationship between the coordination of transcripts and glycerolipid levels in a changing environment and the effects of single gene perturbations.

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Section: Introductionsupporting

confidence: 61%

Linking Gene Expression and Membrane Lipid Composition ofArabidopsis

et al. 2014

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“…Furthermore, tolerance at 1°C for 11 d was conferred using a gene encoding a nonspecific cyanobacterial desaturase, and the resultant transgenic tobacco plants showed a reduction in saturated fatty acid content in membrane lipids (Ishizaki-Nishizawa et al, 1996). The overexpression of glycerol-3-phosphate acyltransferase altered the unsaturation of fatty acids and conferred chilling tolerance in transgenic plants (Ariizumi et al, 2002;Sakamoto et al, 2003;Sui et al, 2007). Hence, modifications in lipid composition that stabilize cell membranes and prevent cellular leakage lead to cold tolerance.…”

Section: Discussionmentioning

confidence: 99%

Overexpression of the Arabidopsis 10-Kilodalton Acyl-Coenzyme A-Binding Protein ACBP6 Enhances Freezing Tolerance

2008

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Small 10-kD acyl-coenzyme A-binding proteins (ACBPs) are highly conserved proteins that are prevalent in eukaryotes. In Arabidopsis (Arabidopsis thaliana), other than the 10-kD ACBP homolog (designated Arabidopsis ACBP6), there are five larger forms of ACBPs ranging from 37.5 to 73.1 kD. In this study, the cytosolic subcellular localization of Arabidopsis ACBP6 was confirmed by analyses of transgenic Arabidopsis expressing autofluorescence-tagged ACBP6 and western-blot analysis of subcellular fractions using ACBP6-specific antibodies. The expression of Arabidopsis ACBP6 was noticeably induced at 48 h after 4°C treatment by northern-blot analysis and western-blot analysis. Furthermore, an acbp6 T-DNA insertional mutant that lacked ACBP6 mRNA and protein displayed increased sensitivity to freezing temperature (28°C), while ACBP6-overexpressing transgenic Arabidopsis plants were conferred enhanced freezing tolerance. Northern-blot analysis indicated that ACBP6-associated freezing tolerance was not dependent on the induction of cold-regulated COLD-RESPONSIVE gene expression. Instead, ACBP6 overexpressors showed increased expression of mRNA encoding phospholipase Dd. Lipid profiling analyses of rosettes from cold-acclimated, freezingtreated (28°C) transgenic Arabidopsis plants overexpressing ACBP6 showed a decline in phosphatidylcholine (236% and 246%) and an elevation of phosphatidic acid (73% and 67%) in comparison with wild-type plants. From our comparison, the gain in freezing tolerance in ACBP6 overexpressors that was accompanied by decreases in phosphatidylcholine and an accumulation of phosphatidic acid is consistent with previous findings on phospholipase Dd-overexpressing transgenic Arabidopsis. In vitro filterbinding assays indicating that histidine-tagged ACBP6 binds phosphatidylcholine, but not phosphatidic acid or lysophosphatidylcholine, further imply a role for ACBP6 in phospholipid metabolism in Arabidopsis, including the possibility of ACBP6 in the cytosolic trafficking of phosphatidylcholine.

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“…Plants with an increased proportion of eukaryotic PG would be useful for studying not only the function of prokaryotic PG, but it would also be interesting to see how the concomitant reduction of high melting PG species affects chilling sensitivity (9). With regard to this aspect of PG functions, plants such as tobacco (64,84) and rice (85) may be more useful than the cold-tolerant Arabidopsis studied before (86,87).…”

Section: Discussionmentioning

confidence: 99%

Channeling of Eukaryotic Diacylglycerol into the Biosynthesis of Plastidial Phosphatidylglycerol

Fritz

Lokstein

Hackenberg

et al. 2007

Journal of Biological Chemistry

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Plastidial glycolipids contain diacylglycerol (DAG) moieties, which are either synthesized in the plastids (prokaryotic lipids) or originate in the extraplastidial compartment (eukaryotic lipids) necessitating their transfer into plastids. In contrast, the only phospholipid in plastids, phosphatidylglycerol (PG), contains exclusively prokaryotic DAG backbones. PG contributes in several ways to the functions of chloroplasts, but it is not known to what extent its prokaryotic nature is required to fulfill these tasks. As a first step toward answering this question, we produced transgenic tobacco plants that contain eukaryotic PG in thylakoids. This was achieved by targeting a bacterial DAG kinase into chloroplasts in which the heterologous enzyme was also incorporated into the envelope fraction. From lipid analysis we conclude that the DAG kinase phosphorylated eukaryotic DAG forming phosphatidic acid, which was converted into PG. This resulted in PG with 2-3 times more eukaryotic than prokaryotic DAG backbones. In the newly formed PG the unique ⌬3-trans-double bond, normally confined to 3-transhexadecenoic acid, was also found in sn-2-bound cis-unsaturated C18 fatty acids. In addition, a lipidomics technique allowed the characterization of phosphatidic acid, which is assumed to be derived from eukaryotic DAG precursors in the chloroplasts of the transgenic plants. The differences in lipid composition had only minor effects on measured functions of the photosynthetic apparatus, whereas the most obvious phenotype was a significant reduction in growth.

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Genetic modification of the fatty acid unsaturation of phosphatidylglycerol in chloroplasts alters the sensitivity of tobacco plants to cold stress

Cited by 43 publications

References 11 publications

Linking Gene Expression and Membrane Lipid Composition ofArabidopsis

Linking Gene Expression and Membrane Lipid Composition ofArabidopsis

Overexpression of the Arabidopsis 10-Kilodalton Acyl-Coenzyme A-Binding Protein ACBP6 Enhances Freezing Tolerance

Channeling of Eukaryotic Diacylglycerol into the Biosynthesis of Plastidial Phosphatidylglycerol

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