Temperature-Dependent Phase Behavior of Phosphatidylglycerols from Chilling-Sensitive and Chilling-Resistant Plants

Murata, Norio; Yamaya, Jun

doi:10.1104/pp.74.4.1016

Cited by 140 publications

(86 citation statements)

References 22 publications

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“…We believe that the collapse of photosynthesis and death of fab1 plants at 2°C is caused by the increase in saturated 16:0 fatty acids and most probably by the presence of approximately 70% high-melting-point fatty acids in chloroplast PG (Wu et al, 1997). This hypothesis is consistent with the other evidence discussed above (Murata et al, 1982;Murata and Yamaya, 1984;Roughan, 1985;Murata et al, 1992;Ishizaki-Nishizawa et al, 1996). It is therefore unexpected that a further increase in chloroplast 16:0 should provide a suppressor phenotype, especially when fad5 mutant plants are themselves compromised in growth and chloroplast biogenesis at low temperature (Hugly and Somerville, 1992).…”

Section: Discussionsupporting

confidence: 82%

“…One hypothesis, specific to chloroplast membranes, proposes that molecular species of chloroplast PG that contain high-melting-point fatty acids at both the sn-1 and sn-2 positions of the glycerol backbone confer chilling sensitivity on plants (Murata, 1983;Nishida and Murata, 1996). This hypothesis is supported by several lines of evidence, including the detection of L a to L b phase transitions in PG isolated from chilling-sensitive plants (Murata and Yamaya, 1984), a correlation across plant species between the proportion of high-melting-point fatty acids in PG and the degree of chilling sensitivity (Murata et al, 1982;Roughan, 1985), and evidence from transgenic plants with engineered alterations in the fatty acid composition of PG (Murata et al, 1992;Wolter et al, 1992).…”

Section: Discussionmentioning

confidence: 48%

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A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function

Barkan

Vijayan²,

Carlsson³

et al. 2006

Plant Physiology

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Leaf membrane lipids of the Arabidopsis (Arabidopsis thaliana) fatty acid biosynthesis 1 (fab1) mutant contain a 35% to 40% increase in the predominant saturated fatty acid 16:0, relative to wild type. This increase in membrane saturation is associated with loss of photosynthetic function and death of mutant plants at low temperatures. We have initiated a suppressor screen for mutations that allow survival of fab1 plants at 2°C. Five suppressor mutants identified in this screen all rescued the collapse of photosynthetic function observed in fab1 plants. While fab1 plants died after 5 to 7 weeks at 2°C, the suppressors remained viable after 16 weeks in the cold, as judged by their ability to resume growth following a return to 22°C and to subsequently produce viable seed. Three of the suppressors had changes in leaf fatty acid composition when compared to fab1, indicating that one mechanism of suppression may involve compensating changes in thylakoid lipid composition. Surprisingly, the suppressor phenotype in one line, S31, was associated with a further substantial increase in lipid saturation. The overall leaf fatty acid composition of S31 plants contained 31% 16:0 compared with 23% in fab1 and 17% in wild type. Biochemical and genetic analysis showed that S31 plants contain a new allele of fatty acid desaturation 5 (fad5), fad5-2, and are therefore partially deficient in activity of the chloroplast 16:0 D7 desaturase. A double mutant produced by crossing fab1 to the original fad5-1 allele also remained alive at 2°C, indicating that the fad5-2 mutation is the suppressor in the S31 (fab1 fad5-2) line. Based on the biophysical characteristics of saturated and unsaturated fatty acids, the increased 16:0 in fab1 fad5-2 plants would be expected to exacerbate, rather than ameliorate, low-temperature damage. We propose instead that a change in shape of the major thylakoid lipid, monogalactosyldiacylglycerol, mediated by the fad5-2 mutation, may compensate for changes in lipid structure resulting from the original fab1 mutation. Our identification of mutants that suppress the low-temperature phenotype of fab1 provides new tools to understand the relationship between thylakoid lipid structure and photosynthetic function.

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Section: Discussionsupporting

confidence: 82%

Section: Discussionmentioning

confidence: 48%

A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function

Barkan

Vijayan²,

Carlsson³

et al. 2006

Plant Physiology

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“…In fubl plants, the proportion of fatty acids with melting points above 2OoC (16:O plus 16:l-trans plus 18:O) in phosphatidylglycerol is 69% compared with a value in wild type of 55%. The significance of this finding lies in the fact that surveys of many plant species (Murata et al, 1982;Murata and Yamaya, 1984;Roughan, 1985) have consistently found that plants containing more than 60% of these high melting point fatty acids in the leaf phosphatidylglycerol are invariably subject to damage at temperatures in the range Oo to 10°C, i.e. they are chilling-sensitive plants.…”

Section: Mutants Ofmentioning

confidence: 99%

A Mutant of Arabidopsis Deficient in the Elongation of Palmitic Acid

James

Dooner

et al. 1994

Plant Physiol.

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The overall fatty acid composition of leaf lipids in a mutant of Arabidopsis thaliana was characterized by an increased level of 160 and a concomitant decrease of 18-carbon fatty acids as a consequence of a single recessive nuclear mutation at the fabl In all plants studied, de novo fatty acid synthesis occurs in the chloroplasts or plastids of the cell (Ohlrogge et al., 1991) by the action of a dissociable type I1 fatty acid synthase (Browse and Somerville, 1991). The primary product of fatty acid synthesis, 16:O-ACP, can undergo one of three competing reactions: (a) hydrolysis by acyl-ACP thioesterase, (b) elongation to 18:O-ACP (which is followed by nearly quantitative desaturation to form 18:1-ACP), or (c) transfer to lysophosphatidic acid. Therefore, the ratio of 16-carbon to 18-carbon fatty acids in the membrane lipids could be determined by the relative fluxes through these three reactions. The significance of these reactions is related to the two pathways that are available for the synthesis of membrane glycerolipids in the leaf cells of higher plants (Browse and Somerville, 1991).In Arabidopsis thaliana, the "prokaryotic" pathway (Roughan and Slack, 1982), located in the chloroplast envelope, uses 18:l-ACP and 16:O-ACP for the sequential acylation of glycerol-3-P to form phosphatidic acid. The phosphatidic acid made by the prokaryotic pathway has 18:l at the sn-1 position and 16:O at the sn-2 position of the glycerol '

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“…One of the most enduring hypotheses in the general area of a plant's susceptibility to chilling stress proposes that the molecular species of chloroplast PG, containing a combination of saturated fatty acids (16:0, 18:0, or 16:l-truns) at both the sn-1 and sn-2 position of the glycerol backbone (high-melting-point PG molecular species), confer chilling sensitivity to plants (Murata and Yamaya, 1984;Murata et al, 1992). Although this hypothesis has been supported by a number of experimental observations, the recent characterization of the Arabidopsis f u b l mutants has provided a counterexample that demonstrates that the high-meltingpoint species of PG can have no more than a contributory effect in inducing chilling sensitivity.…”

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confidence: 99%

Low-Temperature Damage and Subsequent Recovery of fab1 Mutant Arabidopsis Exposed to 2[deg]C

Lightner

Warwick

et al. 1997

Plant Physiology

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The fabl mutant of Arabidopsis tbaliana, which contains increased levels of saturated fatty acids, was indistinguishable from the wild type when it was grown at 22 or 12°C. During the first 7 to 10 d after transfer to 2"C, the growth and photosynthetic characteristics of the fabl plants remained indistinguishable from the wild type, with values for the potential quantum efficiency of photosystem II decreasing from 0.8 to 0.7 in plants of both lines. Whereas wild-type plants maintained quantum efficiency of photosystem II at approximately 0.7 for at least 35 d at 2"C, this parameter declined rapidly in the mutant after 7 d and reached a value of less than 0.1 after 28 d at 2°C. This decline in photosynthetic capacity was accompanied by reductions in chlorophyll content and the amount of chloroplast glycerolipids per gram of leaf. Electron microscopic examination of leaf samples revealed a rapid and extensive disruption of the thylakoid and chloroplast structure in the mutant, which is interpreted here as a form of selective autophagy. Despite the almost complete loss of photosynthetic function and the destruction of photosynthetic machinery, fabl plants retained a substantial capacity for recovery following transfer to 22°C. These results provide a further demonstration of the importance of chloroplast membrane unsaturation to the proper growth and development of plants at low temperature.A remarkable feature of the chloroplast membranes of higher plants is the high number of double bonds that are found in the lipid acyl chains. Typically, only about 10% of the fatty acids that compose the hydrophobic mid-portion of the thylakoid bilayer lack double bonds altogether, whereas more than 80% have two or more double bonds (Harwood, 1982). The relevance of thylakoid lipid composition to the correct functioning of these membranes in photosynthesis has been the subject of considerable speculation and experimentation, but it is still not well understood (Quinn et al., 1989;Murata and Wada, 1995). 347To investigate the functional significance of chloroplast lipid composition, we have isolated a series of Arabidopsis mutants with specific alterations in leaf lipid composition (Browse and Somerville, 1991;Somerville and Browse, 1991). Five genetic loci have been identified that encode the genes that are involved in lipid-linked fatty acid desaturation of chloroplast lipids (fad4, fad5, fad6, fad7, and fad8).(The first four of these were previously known as f a d A , fadB, fadC, and fadD, respectively.) The actl mutants are deficient in the chloroplast glycerol-3-phosphate acyltransferase. Each of these mutants exhibits substantial changes in chloroplast fatty acid composition. For example, thefad5 mutant lacks cis-unsaturated 16-carbon fatty acids because of a deficiency in the desaturation of 16:O on MGD (Kunst et al., 1989a), whereas the fad6 mutant has increased levels of monoenoic fatty acids as a result of a mutation in the chloroplast 16:1/ 18:l desaturase (Browse et al., 1989). However, the m u t a n t s do not exh...

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Temperature-Dependent Phase Behavior of Phosphatidylglycerols from Chilling-Sensitive and Chilling-Resistant Plants

Cited by 140 publications

References 22 publications

A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function

A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function

A Mutant of Arabidopsis Deficient in the Elongation of Palmitic Acid

Low-Temperature Damage and Subsequent Recovery of fab1 Mutant Arabidopsis Exposed to 2[deg]C

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