Compartmentation of Fatty Acid Metabolism in Zygotic Rape Embryos

Fuhrmann, Jochen; Johnen, Thomas; Heise, Klaus-Peter

doi:10.1016/s0176-1617(11)81825-0

Cited by 22 publications

(22 citation statements)

References 16 publications

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“…Light may affect carbon utilization by the developing embryos by driving the production of reductant and ATP for fatty acid synthesis. Browse and Slack (1985) concluded that light could provide cofactors for fatty acid synthesis in linseed plastids, and in canola embryos, light stimulates oil synthesis (Fuhrmann et al, 1994;Aach and Heise, 1998;Bao et al, 1998;Ruuska et al, 2004).…”

Section: Light Increases Biomass Accumulation Lipid Synthesis and Tmentioning

confidence: 99%

“…In heterotrophic tissues, the plastids must import these cofactors or generate them through carbohydrate oxidation or metabolite shuttles (Rawsthorne, 2002). Several studies with developing rapeseed (Brassica napus) embryos showed that lipid accumulation is stimulated by light (Fuhrmann et al, 1994;Aach and Heise, 1998;Bao et al, 1998;Ruuska et al, 2004), 1 This work was supported by the National Science Foundation (grant no. MCB 0224655) and by the U.S. Department of Agriculture (grant no.…”

mentioning

confidence: 99%

“…In heterotrophic tissues, the plastids must import these cofactors or generate them through carbohydrate oxidation or metabolite shuttles (Rawsthorne, 2002). Several studies with developing rapeseed (Brassica napus) embryos showed that lipid accumulation is stimulated by light (Fuhrmann et al, 1994;Aach and Heise, 1998;Bao et al, 1998;Ruuska et al, 2004), suggesting that fatty acid synthesis may be dependent on the supply of reducing power and ATP provided by the light reactions of photosynthesis. Moreover, Ruuska et al (2004) calculated that under ambient light conditions, photosynthetic electron transport can meet the demand for NADPH and ATP for rapeseed fatty acid synthesis.…”

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Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed

et al. 2005

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The conversion of photosynthate to seed storage reserves is crucial to plant fitness and agricultural production, yet quantitative information about the efficiency of this process is lacking. To measure metabolic efficiency in developing seeds, rapeseed (Brassica napus) embryos were cultured in media in which all carbon sources were [U-14 C]-labeled and their conversion into CO 2 , oil, protein, and other biomass was determined. The conversion efficiency of the supplied carbon into seed storage reserves was very high. When provided with 0, 50, or 150 mmol m 22 s 21 light, the proportion of carbon taken up by embryos that was recovered in biomass was 60% to 64%, 77% to 86%, and 85% to 95%, respectively. Light not only improved the efficiency of carbon storage, but also increased the growth rate, the proportion of 14 C recovered in oil relative to protein, and the fixation of external 14 CO 2 into biomass. Embryos grown at 50 mmol m 22 s 21 in the presence of 5 mM 1,1-dimethyl-3-(3,4-dichlorophenyl) urea (an inhibitor of photosystem II) were reduced in total biomass and oil synthesis by 3.2-fold and 2.8-fold, respectively, to the levels observed in the dark. To explore if the reduced growth and carbon conversion efficiency in dark were related to oxygen supplied by photosystem II, embryos and siliques were cultured with increased oxygen. The carbon conversion efficiency of embryos remained unchanged when oxygen levels were increased 3-fold. Increasing the O 2 levels surrounding siliques from 21% to 60% did not increase oil synthesis rates either at 1,000 mmol m 22 s 21 or in the dark. We conclude that light increases the growth, efficiency of carbon storage, and oil synthesis in developing rapeseed embryos primarily by providing reductant and/or ATP.In seed crops, yield is primarily a function of the production of assimilates by the leaves and other green parts of the plant and the utilization of these assimilates to synthesize reserve materials in the seeds. In addition to its importance to agricultural productivity, efficient storage of assimilates by seeds is essential to provide metabolic precursors and chemical energy to power the young seedling until it can capture its own energy from the sun. Within a species, seedling growth is positively correlated with seed size (Howe and Richter, 1982;Stanton, 1984;Vaughton and Ramsey, 1998;Sousa et al., 2003) and seedlings grown from large seeds have higher rates of establishment than those from small seeds (Black, 1958;Grime and Jeffery, 1965;Armstrong and Westoby, 1993;Burke and Grime, 1996). Thus, the amount of reserves stored in the seed will in large part determine the success of the young seedling.Seeds are not simply passive receptacles for the assimilates and minerals provided by the mother plant. They synthesize complex molecules from simple raw materials in relatively precise amounts and proportions (Egli, 1998). Green seeds are photosynthetically active and are able to fix carbon (Watson and Duffus, 1991;Eastmond et al., 1996). As a consequence, the light re...

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Section: Light Increases Biomass Accumulation Lipid Synthesis and Tmentioning

confidence: 99%

mentioning

confidence: 99%

“…In heterotrophic tissues, the plastids must import these cofactors or generate them through carbohydrate oxidation or metabolite shuttles (Rawsthorne, 2002). Several studies with developing rapeseed (Brassica napus) embryos showed that lipid accumulation is stimulated by light (Fuhrmann et al, 1994;Aach and Heise, 1998;Bao et al, 1998;Ruuska et al, 2004), suggesting that fatty acid synthesis may be dependent on the supply of reducing power and ATP provided by the light reactions of photosynthesis. Moreover, Ruuska et al (2004) calculated that under ambient light conditions, photosynthetic electron transport can meet the demand for NADPH and ATP for rapeseed fatty acid synthesis.…”

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confidence: 99%

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Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed

et al. 2005

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“…For example, after removing B. napus seeds from siliques, the incorporation of 14 C from different substrates into lipids increased significantly in light (Aach and Heise, 1997) and decreased when photosynthesis was inhibited by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (Fuhrmann et al, 1994 Most studies cited above were conducted in vitro, using excised embryos exposed to light, and, therefore, the situation of the seeds in planta within siliques could not be assessed. Conclusions from such studies may be limited because dissecting plant tissues is known to impair metabolism (e.g.…”

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confidence: 99%

The Capacity of Green Oilseeds to Utilize Photosynthesis to Drive Biosynthetic Processes

2004

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Seeds of many plant species are green during embryogenesis. To directly assess the influence of light on the physiological status of green oilseeds in planta, Brassica napus and soybean (Glycine max) seeds were rapidly dissected from plants growing in the light or dark. The activation state of malate dehydrogenase, which reflects reduced thioredoxin and NADP/NADPH ratios, was found to be as high in seeds exposed to light as in leaves and to decrease in the dark. Rubisco was highly activated (carbamylated) in both light and dark, most likely reflecting high seed CO 2 concentrations. Activities of Rubisco and phosphoribulokinase were sufficient to account for significant refixation of CO 2 produced during B. napus oil biosynthesis. To determine the influence of light on oil synthesis in planta, siliques on intact plants in full sunlight or detached siliques fed 3 H 2 O were partly covered with aluminum foil. Seeds from light and dark sections were analyzed, and fatty acid accumulation was found to be higher in seeds exposed to light than seeds from dark sections. The spectrum of light filtering through silique walls and the pigment composition of developing B. napus embryos were determined. In addition to a low chlorophyll a/b ratio, the carotenoid pigments of seeds can provide additional capture of the green light that filters through siliques. Together, these results demonstrate that even the low level of light reaching seeds plays a substantial role in activating light-regulated enzymes, increasing fatty acid synthesis, and potentially powering refixation of CO 2 .Oilseeds provide a major source of calories for human consumption and are an increasingly significant source of renewable industrial materials. Interest in engineering enhanced seed oil quantity and quality has prompted efforts to better understand the biosynthesis of oil and other storage products of seeds. Several of the major oilseed crops (e.g. soybean [Glycine max], rapeseed, cotton, and linseed) produce seeds that are green during their development, and this fact has prompted questions regarding the contributions of seed photosynthesis to oilseed metabolism.In leaf chloroplasts, fatty acid synthesis (FAS) is light dependent and utilizes ATP and reducing power generated by photosynthesis (Browse et al., 1986;Roughan and Ohlrogge, 1996). By contrast, plastids isolated from heterotrophic tissues, such as pea roots and cauliflower floral buds, require externally supplied ATP and/or reducing power for FAS (Mö hlmann et al., 1994;Xue et al., 1997). Similarly, plastids isolated from developing chlorophylless seeds of safflower and castor bean are heterotrophic in nature and require added ATP or reducing equivalents (Browse and Slack, 1985;Smith et al., 1992). The situation is more complicated in photosynthetic oilseeds that are green during development. Although these seeds are predominantly sink tissues, they contain chloroplasts with the thylakoid structures and enzymes of typical photosynthetic machinery. However, rather than producing carbon for ex...

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“…In Brassica napus seeds both microsomes and oil body fractions have acyl-CoA elongation activity. The ATP-independent activity is found almost exclusively in the microsomal fraction (Fuhrmann et al, 1994), whereas the ATP-dependent activity is found in both microsomes and oil body fractions (Whitfield et al, 1993; HlousekRadojcic et al, 1995; Imai et al, 1995). Oil bodies prepared by Suc gradients showed minimal levels of the ER marker enzyme cholinephosphotransferase (Whitfield et al, 1993), whereas oil bodies prepared by differential centrifugation showed moderate levels (Imai et al, 1995).…”

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confidence: 99%

Fatty Acid Elongation Is Independent of Acyl-Coenzyme A Synthetase Activities in Leek and Brassica napus1

et al. 1998

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In both animal and plant acyl elongation systems, it has been proposed that fatty acids are first activated to acyl-coenzyme A (CoA) before their elongation, and that the ATP dependence of fatty acid elongation is evidence of acyl-CoA synthetase involvement. However, because CoA is not supplied in standard fatty acid elongation assays, it is not clear if CoA-dependent acyl-CoA synthetase activity can provide levels of acyl-CoAs necessary to support typical rates of fatty acid elongation. Therefore, we examined the role of acyl-CoA synthetase in providing the primer for acyl elongation in leek (Allium porrum L.) epidermal microsomes and Brassica napus L. cv Reston oil bodies. As presented here, fatty acid elongation was independent of CoA and proceeded at maximum rates with CoAfree preparations of malonyl-CoA. We also showed that stearic acid ( Very-long-chain fatty acids (Ͼ18 carbons) are found in the glucocerebrosides of plant plasma membranes (Cahoon and Lynch, 1991), in the storage lipids of many oil seed species (Harwood, 1980), and as precursors of plant epicuticular waxes (Post-Beittenmiller, 1996). These fatty acids are synthesized by successive 2-carbon additions donated from malonyl-CoA. In each cycle of elongation, an acylprimer condenses with malonyl-CoA; this step is followed by a reduction of the 3-ketoacyl-CoA, dehydration of the hydroxyacyl-CoA, and reduction of the enoyl-CoA to the saturated and fully reduced acyl-CoA. These reactions are analogous to those of de novo fatty acid biosynthesis (Ohlrogge and Browse, 1995). However, unlike the soluble, stroma-localized enzymes of fatty acid synthase, the enzymes of acyl elongation are membrane bound and generally thought to be associated with the ER and possibly the plasma membranes in vegetative cells (von WettsteinKnowles, 1993) or with the ER (Agrawal et al., 1984) and oil bodies of developing seeds (Imai et al., 1995). Furthermore, the intermediates of acyl elongation are esterified to CoA rather than to the acyl carrier protein cofactor of fatty acid synthase (Fehling and Mukherjee, 1991).Studies on acyl elongation in plants and animals indicate that, in general, the properties of acyl elongation in plants and animals are quite similar (for review, see Cinti et al., 1992;Cassagne et al., 1994). Both plant and animal elongases require malonyl-CoA and NAD(P)H and use a variety of primers with varied requirements for ATP. For example, relatively high rates of acyl elongation can be achieved without supplied primer, i.e. by ATP-dependent elongation of endogenous substrates. This implies that there is a sufficient endogenous primer pool, but that ATP is necessary to use it.The extent of the ATP requirement for elongation of exogenous acyl-CoAs apparently depends on the system studied. In Brassica napus seeds both microsomes and oil body fractions have acyl-CoA elongation activity. The ATP-independent activity is found almost exclusively in the microsomal fraction (Fuhrmann et al., 1994), whereas the ATP-dependent activity is found in both microsomes...

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Compartmentation of Fatty Acid Metabolism in Zygotic Rape Embryos

Cited by 22 publications

References 16 publications

Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed

Light Enables a Very High Efficiency of Carbon Storage in Developing Embryos of Rapeseed

The Capacity of Green Oilseeds to Utilize Photosynthesis to Drive Biosynthetic Processes

Fatty Acid Elongation Is Independent of Acyl-Coenzyme A Synthetase Activities in Leek and Brassica napus1

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