Biogenesis of Glyoxysomes

Trelease, Richard N.

doi:10.1146/annurev.pp.35.060184.001541

Cited by 94 publications

(40 citation statements)

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“…Biogenesis of the organelle is developmentally regulated; glyoxysomes are present primarily in developing seeds and in seedlings, although other peroxisomes are found in mature plant organs (reviewed by Huang et al, 1983;Trelease, 1984). In general, all peroxisomes appear to share a number of common characteristics: they are bounded by a single membrane, usually possess catalase and hydrogen peroxide-generating oxidases, and lack an organellar genome.…”

Section: Introductionmentioning

confidence: 99%

Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L.

et al. 1989

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We have analyzed the temporal and spatial expression of genes encoding the glyoxylate cycle enzymes isocitrate lyase and malate synthase in Brassica napus L. to determine whether they are coordinately expressed. Both enzymes participate in reactions associated with lipid mobilization in oilseed plant seedlings and are sequestered in a specialized organellel the glyoxysome. We have identified an isocitrate lyase cDNA clone containing the complete protein coding region. RNA blot and in situ hybridization studies with isocitrate lyase and malate synthase cDNA clones from B. napus showed that the genes exhibit similar expression patterns. The mRNAs begin to accumulate during late embryogeny, reach maximal levels in seedling cotyledons, are not detected at significant amounts in leaves, and are distributed similarly in cotyledons and axes of seedlings. Furthermore, transcription studies with isolated nuclei indicate that the genes are controlled primarily although not exclusively at the transcriptional level. We conclude that glyoxysome biogenesis is regulated in part through the coordinate expression of isocitrate lyase and malate synthase genes. INTRODUCTIONIsocitrate lyase (threo-D~-isocitrate glyoxylate-lyase, EC 4.1.3.1) and malate synthase (L-malate glyoxylate-lyase [CoA-acetylating], EC 4.1.3.2) are key enzymes involved in storage lipid mobilization during the growth of higher plant seedlings (reviewed by Trelease and Doman, 1984). They participate in reactions of the glyoxylate cycle, a pathway responsible for the net conversion of two molecules of acetyl coenzyme A into succinate. The metabolic intermediate is ultimately converted into sucrose to serve as a primary nutrient source for growing seedlings unti; photosynthetic activity commences.The two glyoxylate cycle enzymes are encoded by nuclear genes and compartmentalized in a specialized peroxisome, the glyoxysome, which contains glyoxylate cycle and/%oxidation enzymes (Breidenbach et al., 1967;Hutton and Stumpf, 1969). Biogenesis of the organelle is developmentally regulated; glyoxysomes are present primarily in developing seeds and in seedlings, although other peroxisomes are found in mature plant organs (reviewed by Huang et al., 1983;Trelease, 1984). In general, all peroxisomes appear to share a number of common characteristics: they are bounded by a single membrane, usually possess catalase and hydrogen peroxide-generating oxidases, and lack an organellar genome. However, the organelle fulfills different roles in distinct cell types that appear to be dictated by the environment or the differen-1 To whom correspondence should be addressed. tiated state of the cell. For example, in contrast to glyoxysomes, leaf-type peroxisomes possess a different set of prevalent enzymes that are involved in photorespiration. Therefore, biogenesis appears to be controlled partially by the regulated accumulation of constituents unique to a particular class of peroxisomes.To investigate the cellular processes controlling glyoxysome biogenesis, we have been studying the ...

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Section: Introductionmentioning

confidence: 99%

Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L.

et al. 1989

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“…In this model, the newly synthesized triacylglycerol is sequestered between the 2 phospholipid layers of the ER membrane (19,23). Enlargement ofthe vesicle eventually produces a lipid body which is composed of a bag of triacylglycerol surrounded by a half-unit membrane of phospholipids and proteins.…”

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Diacylglycerol Acyltransferase in Maturing Oil Seeds of Maize and Other Species

Cao

Huang²

1986

Plant Physiol.

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Diacylglycerol acyltransferase (EC 2.3.1.20) activity was detected in the microsomal fractions of maturing maize scutellum, soybean cotyledon, peanut cotyledon, and castor bean endosperm. The activity detected was high enough to account for the in vivo rate of triacylglycerol synthesis. The activity of the maize enzyme was characterized using diolein micelles prepared by sonication in Tween 20 as the substrate. The activity was highest at pH values of 6 to 7. The activity was proportional to the amount of enzyme added, and the reaction rate was linear for about 2 minutes. The enzyme was not inactivated by Tween 20, Zwitterion 3-08, Triton-X 100, and cholate, but was inactivated completely by sodium dodecyl sulfate. The enzyme was active on linoleoyl coenzyme A (CoA), palmitoyl CoA, and oleoyl CoA, although the activity was highest on linoleoyl CoA. Endogenous diacylglycerol was present in the microsomes, and the enzyme activity was only partially dependent on the addition of external diolein. Subcellular fractionation of the total scutellum extract in sucrose density gradients was performed. By comparing the migration of the enzyme between rate and equilibrium centrifugation, and between equilibrium centrifugation in the presence and absence of magnesium ions in the preparative media, the enzyme was shown to be associated with the rough endoplasmic reticulum. Some of the above findings on the maize enzyme were extended to the enzymes from castor bean, soybean, and peanuts.Diacylglycerol acyltransferase (EC 2.3.1.20) catalyzes the final step in the synthesis of triacylglycerols in oil seeds (18,22). It is also the only known enzyme unique to the long biosynthetic pathway of triacylglycerols, since the diacylglycerol produced could also be used to produce phospholipids or galactolipids. In spite of the importance of this enzyme in triacylglycerol biosynthesis in oil seeds, its properties have not been well studied.Diacylglycerol acyltransferase in the microsomal fraction of developing seeds has been assayed directly or together with other enzymes (6,10,20,21). In a recent, and so far the most detailed, study, the general properties of the enzyme in a safflower microsomal fraction were characterized (10). However, the detected level ofactivity was almost a magnitude lower than that required to catalyze the sequence of reaction from glycerol phosphate to triacylglycerol (21, 22). Using an enzyme assay which had been used successfully to study the enzyme in spinach leaves, Martin and Wilson (13) failed to detect enzyme activity in the cotyledon extract of developing soybean.An important but unknown aspect of diacylglycerol acyltransferase is its subcellular location. In general, the microsomal fractions were used to study the enzyme activity, and they 'Supported by National Science Foundation grant DMB 85-15556.presumably contained vesicles of the ER as well as membranes of other subcellular particles, including broken plastids. In a recent detailed analysis of the subcellular location ofthe enzyme in spinach...

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“…They contain enzymes of the P-oxidation pathway and the glyoxylate cycle that largely account for the ability of plants to utilize lipids as a carbon source (Trelease and Doman, 1984). These organelles play a prominent role in the metabolism of postgerminative seedlings by converting storage lipids into carbohydrates that serve as carbon and energy sources for the growing seedling (Bridenbach et al, 1967;Huang et al, 1983;Trelease, 1984). Functional glyoxysomes are also present in senescing organs, where they are thought to play a similar role in transforming membrane lipids into carbohydrates that can be translocated to other parts of the plant (Gut and Matile, 1988;De Bellis et a]., 1990;De Bellis and Nishimura, 1991;Wanner et al, 1991;Graham et al, 1992).…”

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DNA Sequences That Activate Isocitrate Lyase Gene Expression during Late Embryogenesis and during Postgerminative Growth

et al. 1996

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We analyzed DNA sequences that regulate the expression of an isocitrate lyase gene from Brasska napus L. during late embryogenesis and during postgerminative growth to determine whether glyoxysomal function is induced by a common mechanism at different developmental stages. P-Clucuronidase constructs were used both in transient expression assays in 6. napus and in transgenic Arabidopsis thaliana to identify the segments of the isocitrate lyase 5' flanking region that influence promoter activity. DNA sequences that play the principal role in activating the promoter during postgerminative growth are located more than 1200 bp upstream of the gene. Distinct DNA sequences that were sufficient for high-leve1 expression during late embryogenesis but only low-leve1 expression during postgerminative growth were also identified. Other parts of the 5' flanking region increased promoter activity both in developing seed and in seedlings. We conclude that a combination of elements is involved in regulating the isocitrate lyase gene and that distinct DNA sequences play primary roles in activating the gene in embryos and in seedlings. These findings suggest that different signals contribute to the induction of glyoxysomal function during these two developmental stages. We also showed that some of the constructs were expressed differently in transient expression assays and in transgenic plants.Glyoxysomes are peroxisomes with a specialized function in lipid mobilization. They contain enzymes of the P-oxidation pathway and the glyoxylate cycle that largely account for the ability of plants to utilize lipids as a carbon source (Trelease and Doman, 1984). These organelles play a prominent role in the metabolism of postgerminative seedlings by converting storage lipids into carbohydrates that serve as carbon and energy sources for the growing seedling (Bridenbach et al., 1967;Huang et al., 1983;Trelease, 1984). Functional glyoxysomes are also present in senescing organs, where they are thought to play a similar role in transforming membrane lipids into carbohydrates that can This work was supported by grants from the National Science Foundation. C.M.S. was supported in part by a fellowship from the North Atlantic Treaty Organization. Bellis and Nishimura, 1991;Wanner et al., 1991;Graham et al., 1992). The findings that genes encoding the two glyoxysome-specific enzymes, isocitrate lyase and malate synthase, are active during pollen and seed development as well as during postgerminative growth opens the possibility that peroxisomes present at these stages of the life cycle may have a glyoxysomal function (Pais and Feijo, 1987;Charzynska et al., 1989;Comai et al., 1989;Turley and Trelease, 1990;Zhang et al., 1994). Thus, glyoxysomal enzymes are present at severa1 stages of the plant life cycle.Although genes encoding the key glyoxylate-cycle enzymes are activated in developing pollen and in maturing seed, the pathway's precise metabolic role(s) at these developmental stages is not known. Understanding the mechanisms that induce these...

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Biogenesis of Glyoxysomes

Cited by 94 publications

References 71 publications

Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L.

Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L.

Diacylglycerol Acyltransferase in Maturing Oil Seeds of Maize and Other Species

DNA Sequences That Activate Isocitrate Lyase Gene Expression during Late Embryogenesis and during Postgerminative Growth

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