Chloroplast damage due to enzymatic hydrolysis of endogenous lipids.

McCarty, Richard E.; Jagendorf, André T.

doi:10.1104/pp.40.4.725

Cited by 116 publications

(59 citation statements)

References 25 publications

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“…It has been shown that incorporation of UDP-Gal into MGDG is gradually decreased, but incorporation into oligogalactolipids is steadily increased or accelerated when chloroplasts (9,19) and envelopes (5) are incubated for prolonged periods. This observation may be partly accounted for by the inhibition of UDGT and the stimulation of GGGT activity by FFA, since FFA is known to be readily produced by aging of chloroplasts (13,17,22).…”

Section: Discussionmentioning

confidence: 99%

Free Fatty Acids Regulate Two Galactosyltransferases in Chloroplast Envelope Membranes Isolated from Spinach Leaves

Sakaki

Kondo²,

Yamada³

1990

Plant Physiol.

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Effects of MgCI2 and free fatty acids (FFA) on galactolipid:galactolipid galactosyltransferase (GGGT) and UDP-galactose:1,2-diacylglycerol galactosyltransferase (UDGT) in chloroplast envelope membranes isolated from spinach (Spinacia oleracea L.) leaves were examined. GGGT activity was sigmoidally stimulated by MgCI2 with a saturated concentration of more than 5 millimolar. Free a-linolenic acid (18:3) caused a drastic increase in GGGT activity under limiting concentrations of MgCI2, without affecting its maximum activity at higher MgCI2 concentrations.Free 18:3 alone did not affect the GGGT activity. The effective species of FFA for the stimulation of GGGT activity in the presence of MgCI2 were unsaturated 16-and 18-carbon fatty acids. GGGT activity was also stimulated by 18:3 in the presence of MnCI2, CaCI2 and a high concentration of KCI in place of MgCI2. UDGT activity was hyperbolically enhanced by MgCI2 with a saturated concentration of 1 to 2 millimolar. In contrast to GGGT, UDGT was severely inhibited by 18:3, and MgCI2-induced stimulation was completely abolished by 18:3. Unsaturated 16-and 18-carbon fatty acids were more inhibitory to UDGT than the saturated acids. The dependence of GGGT activity on monogalactosyldiacylglycerol (MGDG) and MgCI2 concentrations was identical in the envelope membranes isolated from non-and ozone (0.5 microliter/liter)-fumigated spinach leaves, indicating that GGGT remained active in the leaves during ozone fumigation. The results are discussed in relation to the regulation of galactolipid biosynthesis by the endogenous FFA in the envelopes and to the involvement of GGGT in the triacylglycerol synthesis from MGDG in ozone-fumigated leaves.MGDG' and DGDG are the major polar lipid constituents of chloroplast membranes (thylakoids and envelopes), and their biosynthesis has been extensively studied (6,14,20). The final process ofthe galactolipid synthesis proceeds by two galactosylation steps of 1,2-DG to MGDG and MGDG to DGDG in the envelope membranes (6,14). The former 'Abbreviations: MGDG, DGDG, TGDG, and TTGDG, mono-, di-, tri-, and tetragalactosyldiacylglycerol, respectively; 1,2-DG, 1,2-diacylglycerol; UDGT, UDP-galactose: 1,2-diacylglycerol galactosyltransferase; GGGT, galactolipid:galactolipid galactosyltransferase; TG, triacylglycerol; FFA, free fatty acid; 16:3, hexadecatrienoic acid; 18:3, a-linolenic acid; 16:0, palmitic acid; 16:1, palmitoleic acid; 18:0, stearic acid; 18:1, oleic acid; 18:2, linoleic acid. reaction is catalyzed by UDGT (5,11,19) and the latter by GGGT (4,10,26). GGGT can also synthesize TGDG and TTGDG, normally absent in plant leaves in vivo (5, 26).In the preceding papers (22-24), we have shown that treatment of spinach plants with ozone, a major atmospheric pollutant, causes a drastic change in galactolipid composition in leaf tissues, suggesting that the enzymes responsible for the galactolipid metabolism are affected by ozone. We have also demonstrated that ozone stimulates the synthesis of TG from 1,2-DG moieties of MGDG, and that th...

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Section: Discussionmentioning

confidence: 99%

Free Fatty Acids Regulate Two Galactosyltransferases in Chloroplast Envelope Membranes Isolated from Spinach Leaves

Sakaki

Kondo²,

Yamada³

1990

Plant Physiol.

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“…Lipases with pH optima of 5.6 for the hydroalysis of uinsatulrated digalactosyild.glvcerides andl 7.0 for the hydrolysis of tnsaturated monogalactosyl,diglycerides were foulnd in runner beans by Sastry and Kates (14). A small galactolipid lipase activity was foulnd at pH 7.0 in spinach (10).…”

Section: Discussionmentioning

confidence: 99%

“…An inhibitory effect on the Hilll relaction by unsatturated fatty acids had been found by Krogmann and Jagendorf (8) and more recently by McCairty and Jagendorf (10) and Molotkovfsky and Zheskova (11). Therefore, it seemed thait an analysis of the free fatty acids of ch'loroplasts might indicate the reason for the loss of Hill activity during a!ging of Ohloroplasts.…”

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confidence: 94%

Release of Free Fatty Acids and Loss of Hill Activity by Aging Spinach Chloroplasts

Constantopoulos

Kenyon

1968

Plant Physiol.

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A bstract. The free fatty acid content of spinach chloroplasts, isolated at pH 5.8 to 8.0, has been found to vary between 3.1 and 5.5 % of the total chloroplast fatty acids. When chloroplasts were incubated at room temperature for 2 hours, the free fatty acids increased by 42 land the Hill activity decreased by 70 g. After 2 hours of incubation at 370, the free fatty acids increased about 3-fold and the Hill activity decreased to almost 0. The addition of crystalline bovine serum albumin largely prevented the loss of Hill activity at room temperature and at 50, but had little effect during incubation at 370. Both the release of free fatty acids and the loss of Hill activity were pH dependent. The losses were the least during incubation at pH 5.8 and the greatest during incubation at pH 8.0. The major free fatty acids released at pH 5.8 were saturated, while those released at pH 7.0 or 8.0 were mainly the unsaturated acids, a-linolenic acid and hexadecatrienoic acid.Approximately 50 % (w/w) of the dry weight of spinach chloroplasts is lipid (9). Almost 40 % (w/w) of these lipids are fatty acids (G. Constanitopouilos, unpublished results). However, aside from a paper written by Speer et al. in 1929 (15) in which the free faitty acids of spinach chloroplasts were said to be 53 % (w/w) of the total fatty acids, no distinction between the free fatty acids ancI lipid-boutnd fatty acids has been reported. Thus, both the amount and the chemical composition of the free fatty acids remain uncertain.\WVhile studying the effect of hydrolytic enzymes on the structure and function of chloroplasts (G. Constanto,poulos and K. Bloch, manuscript in preparation), we noticed a rapid loss of Hill activity of the chloro'plasts after short incubations at 370 or even at roolm temperature. An inhibitory effect on the Hilll relaction by unsatturated fatty acids had been found by Krogmann and Jagendorf (8) ing isolation varies between 3.1 and 5.5 % of the total fatty acids of chloroplasts, depending on the method of preparation. Incubation of chlo,roplasts ait 370 results in the release of bound fatty acids. The rate of release and chemical composition of the released fatty acids is dependent on the pH of the reaction mixture. Under some conditions, addtition of bovine serum albumin (BSA) to the chloroplasit stuspension la,rgely prevents the loss of Hill activity. Materials and MethodsPreptaratioa of Chloroplaist Sutspensionts. Spinach was ptuirchased at the local market. Several different procedures were used for the preparation of chloroplasts from fresh spinach leaves (6,12,17). Chlorophyll was deitermined by the method of Arnon (1). Chloropla,sts were aged in 20 mm potassitum phosphate buffer, pH 7.0, containing 6.7 mM KOl, at a concentration of 1 to 2 mg chlorophyll/ml of suispension.

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“…The release of fatty acids during aging processes in vitro has been demonstrated in several cells and organelles such as human erythrocytes (30), mitochondria (10) and chloroplasts (8,16,22,39,41). In chloroplasts, the main fatty acids released in the course of aging are Cis-unsaturated fatty acids (8,16,39), particularly linolenic acid; these acids are the most abundant in the thylakoid (8,39) and envelope (21) membrane lipids.…”

mentioning

confidence: 99%

“…A hypothesis explaining the inhibition of photosynthesis by linolenate is presented. Key words: Chloroplasts -Linolenic acid treatment -3-P-glyceraldehyde effluxPhosphate uptake -Photosynthesis -Spinach -Transport.The release of fatty acids during aging processes in vitro has been demonstrated in several cells and organelles such as human erythrocytes (30), mitochondria (10) and chloroplasts (8,16,22,39,41). In chloroplasts, the main fatty acids released in the course of aging are Cis-unsaturated fatty acids (8,16,39), particularly linolenic acid; these acids are the most abundant in the thylakoid (8, 39) and envelope (21) membrane lipids.…”

mentioning

confidence: 99%

Effect of linolenate on photosynthesis by intact spinach chloroplasts I. Inhibition of orthophosphate uptake and of 3-P-glyceraldehyde efflux across the chloroplast envelope

Siegenthaler

Akamba

1979

Plant and Cell Physiology

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Linolenic acid (Cis:3) inhibited photosynthesis by intact spinach chloroplasts. This inhibition was due neither to a lack of NADPH in chloroplasts nor to a direct inhibition of the enzyme activities in the Calvin-Benson cycle. Linolenate inhibited CO2 fixation and oxygen evolution more effectively than NADP+ photoreduction but did not inhibit the activity of several key enzymes of the Calvin cycle. Linolenate inhibited phosphate influx and 3-phosphoglyceraldehyde efflux across the chloroplast envelope. A hypothesis explaining the inhibition of photosynthesis by linolenate is presented. Key words: Chloroplasts -Linolenic acid treatment -3-P-glyceraldehyde effluxPhosphate uptake -Photosynthesis -Spinach -Transport.The release of fatty acids during aging processes in vitro has been demonstrated in several cells and organelles such as human erythrocytes (30), mitochondria (10) and chloroplasts (8,16,22,39,41). In chloroplasts, the main fatty acids released in the course of aging are Cis-unsaturated fatty acids (8,16,39), particularly linolenic acid; these acids are the most abundant in the thylakoid (8, 39) and envelope (21) membrane lipids. So far, the action of endogenous (31, 38,39) and exogenous (26,(35)(36)(37)(38) fatty acids has been mainly studied in relation to the photochemical reactions of the thylakoid. It has been shown that such unsaturated fatty acids inhibit electron flow in photosystems II and I and the associated photophosphorylation (35,37), light-induced shrinkage in chloroplasts (35), and the light-generated ZlpH across thyalkoid membranes in a sequential fashion (37). In addition, fatty acids modify the physicochemical properties of the thylakoid membrane in such a way that swelling occurs (27,34) and that the JpH is diminished and pHi increased, inducing a shift of the pH optimum of electron flow towards acidity (37)(38)(39).In order to elucidate further the control of photosynthetic activities by these fatty acids, we have now studied the action of linolenate on the photosynthetic apparatus at a higher level of structural integrity. The initial point of interest was: Would free fatty acids influence photosynthetic carbon metabolism in intact chloro-1 This work is part of a doctoral program which is carried out by L. Mv6 Akamba in this laboratory. 395

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Chloroplast damage due to enzymatic hydrolysis of endogenous lipids.

Cited by 116 publications

References 25 publications

Free Fatty Acids Regulate Two Galactosyltransferases in Chloroplast Envelope Membranes Isolated from Spinach Leaves

Free Fatty Acids Regulate Two Galactosyltransferases in Chloroplast Envelope Membranes Isolated from Spinach Leaves

Release of Free Fatty Acids and Loss of Hill Activity by Aging Spinach Chloroplasts

Effect of linolenate on photosynthesis by intact spinach chloroplasts I. Inhibition of orthophosphate uptake and of 3-P-glyceraldehyde efflux across the chloroplast envelope

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