Carbohydrate Metabolism and Activity of Pyrophosphate: Fructose-6-Phosphate Phosphotransferase in Photosynthetic Soybean (<i>Glycine max</i>, Merr.) Suspension Cells

Spilatro, Steven R.; Anderson, James M.

doi:10.1104/pp.88.3.862

Cited by 25 publications

(13 citation statements)

References 25 publications

(37 reference statements)

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“…Here too, there is an inhibition of photosynthesis, increased respiration, loss of chlorophyll, a decrease of photosynthetic enzymes and an increase of glycolytic enzymes (Dalton and Street 1977;Spilatro and Anderson 1989). The changes of respiratory metabolites and enzymes are also very similar to those found after adding glucose to heterotrophic cell-suspension cultures (Hatzfeld et al 1990).…”

Section: Short-and Long-term Regulationmentioning

confidence: 75%

“Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes

Stitt

Schaewen

Willmitzer

1991

Planta

214

127

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Leaves on transgenic tobacco plants expressing yeast-derived invertase in the apoplast develop clearly demarcated green and bleached sectors when they mature. The green areas contain low levels of soluble sugars and starch which are turned over on a daily basis, and have high rates of photosynthesis and low rates of respiration. The pale areas accumulate carbohydrate, photosynthesis is inhibited, and respiration increases. This provides a model system to investigate the "sink" regulation of photosynthetic metabolism by accumulating carbohydrate. The inhibition of photosynthesis is accompanied by a decrease of ribulose-1,5-bisphosphate and glycerate-3-phosphate, and an increase of triosephosphate and fructose-1,6-bisphosphate. The extracted activities of ribulose-1,5-bisphosphate carboxylase, fructose-1, 6-bisphosphatase and NADP-glyeraldehyde-3-phosphate dehydrogenase decreased. The activity of sucrose-phosphate synthase remained high or increased, an increased portion of the photosynthate was partitioned into soluble sugars rather than starch, and the pale areas showed few or no oscillations during transitions between darkness and saturating light in saturating CO2. The increased rate of respiration was accompanied by an increased level of hexose-phosphates, triose-phosphates and fructose-1,6-bisphosphate while glycerate-3-phosphate and phosphoenolpyruvate decreased and pyruvate increased. The activities of pyruvate kinase, phosphofructokinase and pyrophosphate: fructose-6-phosphate phosphotransferase increased two- to four-fold. We conclude that an increased level of carbohydrate leads to a decreased level of Calvin-cycle enzymes and, thence, to an inhibition of photosynthesis. It also leads to an increased level of glycolytic enzymes and, thence, to a stimulation of respiration. These changes of enzymes are more important in middle- or long-term adjustments to high carbohydrate levels in the leaf than fine regulation due to depletion of inorganic phosphate or high levels of phosphorylated metabolites.

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Section: Short-and Long-term Regulationmentioning

confidence: 75%

“Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes

Stitt

Schaewen

Willmitzer

1991

Planta

214

127

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“…This is not surprising because sucrose is rapidly hydrolyzed in soybean cell cultures (23). The effect ofsugars was probably not simply osmotic, because maximal stimulation occurred at a sucrose concentration of 58 mm (Fig.…”

Section: Vsp Mrna Levels Are Modulated By Wounding and Photosynthesismentioning

confidence: 82%

“…The sugars in the media were supplied as equivalent mass, because sucrose in these cultures is normally hydrolyzed very quickly by invertase (23 Creelman, and J.E. Mullet, unpublished data).…”

Section: Accumulation Of Vsp Mrnas In Excised Mature Leaves Requires mentioning

confidence: 99%

Coregulation of Soybean Vegetative Storage Protein Gene Expression by Methyl Jasmonate and Soluble Sugars

Mason¹,

DeWald²,

Creelman³

et al. 1992

Plant Physiol.

110

106

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The soybean vegetative storage protein genes vspA and vspB are highly expressed in developing leaves, stems, flowers, and pods as compared with roots, seeds, and mature leaves and stems. In this paper, we report that physiological levels of methyl jasmonate (MeJA) and soluble sugars synergistically stimulate accumulation of vsp mRNAs. Treatment of excised mature soybean (Glycine max Merr. cv Williams) leaves with 0.2 molar sucrose and 10 micromolar MeJA caused a large accumulation of vsp mRNAs, whereas little accumulation occurred when these compounds were supplied separately. In soybean cell suspension cultures, the synergistic effect of sucrose and MeJA on the accumulation of vspB mRNA was maximal at 58 millimolar sucrose and was observed with fructose or glucose substituted for sucrose. In dark-grown soybean seedlings, the highest levels of vsp mRNAs occurred in the hypocotyl hook, which also contained high levels of MeJA and soluble sugars. Lower levels of vsp mRNAs, MeJA, and soluble sugars were found in the cotyledons, roots, and nongrowing regions of the stem. Wounding of mature soybean leaves induced a large accumulation of vsp mRNAs when wounded plants were incubated in the light. Wounded plants kept in the dark or illuminated plants sprayed with dichlorophenyidimethylurea, an inhibitor of photosynthetic electron transport, showed a greatly reduced accumulation of vsp mRNAs. The time courses for the accumulation of vsp mRNAs induced by wounding or sucrose/MeJA treatment were similar. These results strongly suggest that vsp expression is coregulated by endogenous levels of MeJA (or jasmonic acid) and soluble carbohydrate during normal vegetative development and in wounded leaves.We previously investigated changes in protein and mRNA populations that occur when soybean seedlings are exposed to water deficit (3,6,7,16,17). These studies showed that a 28-kD protein accumulates in the hypocotyl cell wall fraction when soybean seedlings are transplanted to low water potential soil (3,16). This protein and an immunologically related 3 1-kD protein are also abundant in soluble hypocotyl fractions (16) and localized in vacuoles (H.S. Mason, L.R. Griffing, and J.E. Mullet, unpublished data). Analysis of the cDNAs that encode the 28-and 3 1-kD proteins (16) revealed that they are identical with the soybean leaf VSP2 first iden-

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“…Sensitivity to activation by Fru2,6bisP appears to be conferred by a specific ct-subunit, which has been derived from the catalytic 13-subunit during evolution of the higher-plant PFP (Carlisle et al 1990). The observation that PFP activity depends on the developmental stage and conditions (Spilatro and Anderson 1989;Xu et al 1989;Theodorou et al 1992) provides a third indirect line of evidence for the importance of PFP in plant metabolism.…”

mentioning

confidence: 95%

Transgenic potato plants with strongly decreased expression of pyrophosphate:fructose-6-phosphate phosphotransferase show no visible phenotype and only minor changes in metabolic fluxes in their tubers

Hajirezaei

Sonnewald

Viola³

et al. 1993

Planta

100

117

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Abstract.Potato (Solanum tuberosum L.) plants were transformed with "antisense" constructs to the genes encoding the ~-and fl-subunits of pyrophosphate: fructose-6-phosphate phosphotransferase (PEP), their expression being driven by the constitutive CaMV 35S promotor. (i) In several independent transformant lines, PFP expression was decreased by 70-90% in growing tubers and by 88-99% in stored tubers. (ii) The plants did not show any visual phenotype, reduction of growth or decrease in total tuber yield. However, the tubers contained 20-40% less starch than the wild type. Sucrose levels were slightly increased in growing tubers, but not at other stages. The rates of accumulation of sucrose and free hexoses when tubers were stored at 4 ~ C and the final amount accumulated were the same in antisense and wild-type tubers. (iii) Metabolites were investigated at four different stages in tuber life history; growing (sink) tubers, mature tubers, cold-sweetening tubers and sprouting (source) tubers. At all stages, compared to the wild type, antisense tubers contained slightly more hexose-phosphates, two-to threefold less glycerate-3-phosphate and phosphoenolpyruvate and up to four-to fivefold more fructose-2,6-bisphosphate. Abbreviations: Frul,6bisP=fructose-l,6-bisphosphate; Fru2,6bisP =fructose-2,6-bisphosphate; Fru6P=fructose-6-phosphate; GlclP =glucose-l-phosphate; Glc6P=glucose-6-phosphate; NMR=nu-clear magnetic resonance; 3PGA=glycerate-3-phosphate; PEP= phosphoenolpyruvate; PEP = pyrophosphate: fructose-6-phosphate phosphotransferase; PFK=phosphofructokinase; UDPGIc = UDP glucose; WT=wild type Correspondence to: M. Stitt; FAX: 49(6221)565859 surcrose increased 15-fold in discs from growing antisense tubers, compared with growing wild-type tubers. Resynthesis of sucrose was increased by 10-20% when discs from antisense and wild-type tubers stored at 4 ~ C (cold sweetening) were compared. The conversion of [Ut4C]glucose to starch was decreased by about 30% and 50%, respectively. (viii) The randomisation of [1-13C]glucose in the glucosyl and fructosyl moieties of sucrose was decreased from 13.8 and 15.7% in the wild type to 3.6 and 3.9% in an antisense transformant. Simultaneously, randomisation in glucosyl residues isolated from starch was reduced from 14.4 to 4.1%. (ix) These results provide evidence that PFP catalyses a readily reversible reaction in tubers, which is responsible for the recycling of label from triose-phosphates to hexose-phosphates, but with the net reaction in the glycolytic direction. The results do not support the notion that PFP is involved in regulating the cytosolic PPi concentration. They also demonstrate that PFP does not control the rate of glycolysis, and that tubers contain exessive capacity to phosphorylate fructose-6-phosphate. The decreased concentration of phosphoenolpyruvate and glycerate-3-phosphate compensates for the decrease of PFP protein by stimulating ATP-dependent phosphofructokinase, and by stimulating fructose-6-phosphate,2-kinase to increase the fructose-2,6-bisphosphate...

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Carbohydrate Metabolism and Activity of Pyrophosphate: Fructose-6-Phosphate Phosphotransferase in Photosynthetic Soybean (Glycine max, Merr.) Suspension Cells

Cited by 25 publications

References 25 publications

“Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes

“Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes

Coregulation of Soybean Vegetative Storage Protein Gene Expression by Methyl Jasmonate and Soluble Sugars

Transgenic potato plants with strongly decreased expression of pyrophosphate:fructose-6-phosphate phosphotransferase show no visible phenotype and only minor changes in metabolic fluxes in their tubers

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