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Mobilization of seed storage lipid by Arabidopsis seedlings is retarded in the presence of exogenous sugars.

To JP, Reiter WD, Gibson SI - BMC Plant Biol. (2002)

Bottom Line: Wild-type seedlings become insensitive to glucose inhibition of storage lipid breakdown within 3 days of the start of imbibition.This effect is not solely due to the osmotic potential of the media, as substantially higher concentrations of sorbitol than of glucose are required to exert significant effects on lipid breakdown.The inhibitory effect of glucose on lipid breakdown is limited to a narrow developmental window, suggesting that completion of some critical metabolic transition results in loss of sensitivity to the inhibitory effect of glucose on lipid breakdown.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry & Cell Biology, MS140 Rice University, 6100 Main St, Houston, TX 77005-1892, USA. jennto@email.unc.edu

ABSTRACT

Background: Soluble sugar levels must be closely regulated in germinating seeds to ensure an adequate supply of energy and building materials for the developing seedling. Studies on germinating cereal seeds indicate that production of sugars from starch is inhibited by increasing sugar levels. Although numerous studies have focused on the regulation of starch metabolism, very few studies have addressed the control of storage lipid metabolism by germinating oilseeds.

Results: Mobilization of storage lipid by germinating seeds of the model oilseed plant Arabidopsis thaliana (L.) Heynh. occurs at a greatly reduced rate in the presence of exogenous glucose or mannose, but not in the presence of equi-molar 3-O-methylglucose or sorbitol. The sugar-insensitive5-1/abscisic acid-insensitive4-101 (sis5-1/abi4-101) mutant is resistant to glucose inhibition of seed storage lipid mobilization. Wild-type seedlings become insensitive to glucose inhibition of storage lipid breakdown within 3 days of the start of imbibition.

Conclusions: Growth in the presence of exogenous glucose significantly retards mobilization of seed storage lipid in germinating seeds from wild-type Arabidopsis. This effect is not solely due to the osmotic potential of the media, as substantially higher concentrations of sorbitol than of glucose are required to exert significant effects on lipid breakdown. The inhibitory effect of glucose on lipid breakdown is limited to a narrow developmental window, suggesting that completion of some critical metabolic transition results in loss of sensitivity to the inhibitory effect of glucose on lipid breakdown.

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Seedlings become resistant to the inhibitory effects of glucose on breakdown of seed storage lipid and synthesis of membrane lipid within three days of the start of imbibition. Seeds were sown on minimal media supplemented with 0.03 M glucose, 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. After 3 days, some of the seedlings grown on 0.03 M glucose were transferred to media supplemented with 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. Fatty acid levels were measured in seeds/seedlings harvested after an additional 7 days of growth. Note that this figure depicts the amount of 20:1 fatty acid metabolized by an average seedling, rather than the amount of 20:1 fatty acid remaining in an average seedling. See the "Materials and Methods" section for a description of the method used to estimate accumulation of membrane fatty acids. Results presented are means ± SD (n = 3, except n = 2 for seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose). Glc, glucose; Sorb, sorbitol. This experiment was repeated, with similar results.
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Figure 6: Seedlings become resistant to the inhibitory effects of glucose on breakdown of seed storage lipid and synthesis of membrane lipid within three days of the start of imbibition. Seeds were sown on minimal media supplemented with 0.03 M glucose, 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. After 3 days, some of the seedlings grown on 0.03 M glucose were transferred to media supplemented with 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. Fatty acid levels were measured in seeds/seedlings harvested after an additional 7 days of growth. Note that this figure depicts the amount of 20:1 fatty acid metabolized by an average seedling, rather than the amount of 20:1 fatty acid remaining in an average seedling. See the "Materials and Methods" section for a description of the method used to estimate accumulation of membrane fatty acids. Results presented are means ± SD (n = 3, except n = 2 for seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose). Glc, glucose; Sorb, sorbitol. This experiment was repeated, with similar results.

Mentions: As shown in Figure 6, seedlings sown directly on media containing 0.27 M glucose metabolize only a small percentage of their 20:1 fatty acid after 10 days of growth. In addition, these seedlings exhibit a significant reduction in accumulation of membrane fatty acids. In contrast, seedlings shifted from 0.03 to 0.27 M glucose metabolize almost all of their 20:1 fatty acid within 7 days of the shift, despite the fact that only ~30% of the seed storage lipid is metabolized prior to the shift. In addition, these seedlings actually show increased accumulation of membrane fatty acids relative to seedlings grown continuously on 0.03 M glucose. As an osmotic control, seedlings were grown on 0.24 M sorbitol + 0.03 M glucose for 10 days, or on 0.03 M glucose for 3 days followed by an additional 7 days on 0.24 M sorbitol + 0.03 M glucose. As shown in Figure 6, both the seedlings grown continuously on 0.24 M sorbitol + 0.03 M glucose, or transferred to that media after 3 days on 0.03 M glucose, metabolize almost all of their 20:1 fatty acid. In contrast, seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose exhibit a significant reduction in accumulation of membrane fatty acids, whereas seedlings sown directly on 0.24 M sorbitol + 0.03 M glucose exhibit only a slight reduction.


Mobilization of seed storage lipid by Arabidopsis seedlings is retarded in the presence of exogenous sugars.

To JP, Reiter WD, Gibson SI - BMC Plant Biol. (2002)

Seedlings become resistant to the inhibitory effects of glucose on breakdown of seed storage lipid and synthesis of membrane lipid within three days of the start of imbibition. Seeds were sown on minimal media supplemented with 0.03 M glucose, 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. After 3 days, some of the seedlings grown on 0.03 M glucose were transferred to media supplemented with 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. Fatty acid levels were measured in seeds/seedlings harvested after an additional 7 days of growth. Note that this figure depicts the amount of 20:1 fatty acid metabolized by an average seedling, rather than the amount of 20:1 fatty acid remaining in an average seedling. See the "Materials and Methods" section for a description of the method used to estimate accumulation of membrane fatty acids. Results presented are means ± SD (n = 3, except n = 2 for seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose). Glc, glucose; Sorb, sorbitol. This experiment was repeated, with similar results.
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Related In: Results  -  Collection

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Figure 6: Seedlings become resistant to the inhibitory effects of glucose on breakdown of seed storage lipid and synthesis of membrane lipid within three days of the start of imbibition. Seeds were sown on minimal media supplemented with 0.03 M glucose, 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. After 3 days, some of the seedlings grown on 0.03 M glucose were transferred to media supplemented with 0.27 M glucose or 0.24 M sorbitol + 0.03 M glucose. Fatty acid levels were measured in seeds/seedlings harvested after an additional 7 days of growth. Note that this figure depicts the amount of 20:1 fatty acid metabolized by an average seedling, rather than the amount of 20:1 fatty acid remaining in an average seedling. See the "Materials and Methods" section for a description of the method used to estimate accumulation of membrane fatty acids. Results presented are means ± SD (n = 3, except n = 2 for seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose). Glc, glucose; Sorb, sorbitol. This experiment was repeated, with similar results.
Mentions: As shown in Figure 6, seedlings sown directly on media containing 0.27 M glucose metabolize only a small percentage of their 20:1 fatty acid after 10 days of growth. In addition, these seedlings exhibit a significant reduction in accumulation of membrane fatty acids. In contrast, seedlings shifted from 0.03 to 0.27 M glucose metabolize almost all of their 20:1 fatty acid within 7 days of the shift, despite the fact that only ~30% of the seed storage lipid is metabolized prior to the shift. In addition, these seedlings actually show increased accumulation of membrane fatty acids relative to seedlings grown continuously on 0.03 M glucose. As an osmotic control, seedlings were grown on 0.24 M sorbitol + 0.03 M glucose for 10 days, or on 0.03 M glucose for 3 days followed by an additional 7 days on 0.24 M sorbitol + 0.03 M glucose. As shown in Figure 6, both the seedlings grown continuously on 0.24 M sorbitol + 0.03 M glucose, or transferred to that media after 3 days on 0.03 M glucose, metabolize almost all of their 20:1 fatty acid. In contrast, seedlings transferred from 0.03 M glucose to 0.24 M sorbitol + 0.03 M glucose exhibit a significant reduction in accumulation of membrane fatty acids, whereas seedlings sown directly on 0.24 M sorbitol + 0.03 M glucose exhibit only a slight reduction.

Bottom Line: Wild-type seedlings become insensitive to glucose inhibition of storage lipid breakdown within 3 days of the start of imbibition.This effect is not solely due to the osmotic potential of the media, as substantially higher concentrations of sorbitol than of glucose are required to exert significant effects on lipid breakdown.The inhibitory effect of glucose on lipid breakdown is limited to a narrow developmental window, suggesting that completion of some critical metabolic transition results in loss of sensitivity to the inhibitory effect of glucose on lipid breakdown.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry & Cell Biology, MS140 Rice University, 6100 Main St, Houston, TX 77005-1892, USA. jennto@email.unc.edu

ABSTRACT

Background: Soluble sugar levels must be closely regulated in germinating seeds to ensure an adequate supply of energy and building materials for the developing seedling. Studies on germinating cereal seeds indicate that production of sugars from starch is inhibited by increasing sugar levels. Although numerous studies have focused on the regulation of starch metabolism, very few studies have addressed the control of storage lipid metabolism by germinating oilseeds.

Results: Mobilization of storage lipid by germinating seeds of the model oilseed plant Arabidopsis thaliana (L.) Heynh. occurs at a greatly reduced rate in the presence of exogenous glucose or mannose, but not in the presence of equi-molar 3-O-methylglucose or sorbitol. The sugar-insensitive5-1/abscisic acid-insensitive4-101 (sis5-1/abi4-101) mutant is resistant to glucose inhibition of seed storage lipid mobilization. Wild-type seedlings become insensitive to glucose inhibition of storage lipid breakdown within 3 days of the start of imbibition.

Conclusions: Growth in the presence of exogenous glucose significantly retards mobilization of seed storage lipid in germinating seeds from wild-type Arabidopsis. This effect is not solely due to the osmotic potential of the media, as substantially higher concentrations of sorbitol than of glucose are required to exert significant effects on lipid breakdown. The inhibitory effect of glucose on lipid breakdown is limited to a narrow developmental window, suggesting that completion of some critical metabolic transition results in loss of sensitivity to the inhibitory effect of glucose on lipid breakdown.

Show MeSH
Related in: MedlinePlus