Journal of Experimental Botany, Vol. 51, No. 90001, pp. 439-445,
February 2000
© 2000 Oxford University Press
Impact of elevated cytosolic and apoplastic invertase activity on carbon metabolism during potato tuber development
1 Institut für Pflanzengenetik und Kulturpflanzenforschung, Corrensstrasse 3, D-06466 Gatersleben, Germany
2 Max-Planck Institut für Molekulare Pflanzenphysiologie, Karl Liebknecht Str. 25, D-14476 Golm, Germany
Received 26 March 1999; Accepted 4 October 1999
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Abstract |
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During tuberization in Solanum tuberosum var. Desirée maximal catalytic activities of invertase(s) and sucrose synthase are inversely correlated. During the early stages, invertase activity is high and declines during maturation. The decrease in invertase activity is accompanied by a decrease in the hexose to sucrose ratio and an increase in sucrose synthase activity. This switch is paralleled by the onset of the storage phase as shown by the accumulation of starch and storage proteins. Biochemical and genetic evidence suggests that sucrose synthase activity is positively correlated with sink strength. To explore the possibility of enhancing sink strength in potato tubers by elevating the sucrolytic capacity, transgenic potato plants expressing either cytosolic or apoplastic yeast invertase in their tubers were made. Surprisingly, cytosolic invertase led to a decrease and apoplastic invertase to an increase in tuber yield. To understand the causes of the observed phenotypes, carbon metabolism in tubers of transgenic and control plants was analysed during different stages of tuber development. Both cytosolic and apoplastic invertase resulted in decreased sucrose and elevated glucose contents, indicating that sucrose is accessible in both compartments. Metabolic perturbation, however, was found to be compartment specific. Elevated cytosolic invertase activity led to increased carbon flux towards glycolysis and accumulation of phosphorylated intermediates. The phosphorylated intermediates were not used to build up starch. In contrast, apoplastic invertase does not lead to a significant increase in hexose phosphates compared to untransformed controls. Thus, hexoses originating in the apoplast are not efficiently phosphorylated during potato tuber development, which might be explained by an endocytotic uptake of sucrose and/or hexoses from the apoplast into the vacuole bypassing the cytosolic compartment.
Key words: Potato tuber, invertase, development, carbon metabolism, Solanum tuberosum
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Sink regulation of photosynthesis is a well accepted concept, possibly explaining the coordination of assimilate production and consumption (discussed in Stitt et al., 1990). In tobacco and potato the photosynthetic capacity of source leaves is under developmental and environmental control (Miller et al., 1997; Ludewig, 1999). To understand the possible impact of changes in the relative sink strength of storage organs on the regulation of photosynthesis, detailed knowledge on the development of sink tissues is required. As a model system for storage sink development, potato tubers are being studied.
Tuberization in potato is a complex process involving anatomical, hormonal and biochemical changes, leading to the differentiation of a lateral shoot, the stolon, into a vegetative storage organ, the tuber. Tuber initiation involves a shift in stolon growth from extension to radial growth in the sub-apical region of the stolon tip (Booth, 1963). This is accomplished by an increase in cell size and number, and a change in the plane of cell division from longitudinal to random or tangential. In parallel, the hexose to sucrose ratio changes in favour of sucrose in the stolon tip (Davies, 1984). This is mainly due to a decrease in hexose content, especially fructose, which declines to barely detectable concentrations, possibly caused by a higher fructokinase than hexokinase activity in developing tubers (Davies and Oparka, 1985; Gardner et al., 1992; Renz and Stitt, 1993). This process is accompanied by a decline of alkaline and acidic invertase and an increase of sucrose synthase activity (Ross et al., 1994; Appeldoorn et al., 1997). The rise in sucrose synthase activity is positively correlated with the onset of starch and storage protein biosynthesis (Obata-Sasamoto and Suzuki, 1979). Comparison between the estimated rate of sucrose breakdown and the maximum catalytic activity of sucrose synthase strongly suggests a dominant role of sucrose synthase in sucrose breakdown during the storage phase of developing potato tubers (Mares and Marschner, 1980; Morrell and Ap Rees, 1986). The observed changes in enzyme activities are reflected in the transcripts of the respective genes (Visser et al., 1994; Zrenner et al., 1995). In addition, invertase activity has been shown to be subject to regulation via a proteinaceous invertase inhibitor which might influence in vivo enzyme activity (Schwimmer et al., 1961; Pressey, 1966; Bracho and Whitaker, 1990a, b). In maize, both invertase and sucrose synthase mutants have been described (Miller and Chourey, 1992; Chourey and Nelson, 1976). The absence of soluble and wall-bound invertase leads to aberrant pedicel and endosperm development, whereas reduced sucrose synthase activity results in a strong decrease of starch accumulation, which is in agreement with the postulated function of sucrose synthase during the storage phase of sink tissues. To investigate the unique role of sucrose synthase with respect to sucrose metabolism and sink strength in growing potato tubers, transgenic plants with decreased sucrose synthase activity have been created (Zrenner et al., 1995). Analysis of the transgenic plants revealed that tuber number and fresh weight were unaltered, whereas starch accumulation was severely reduced, indicating that sucrose synthase is the major sucrolytic determinant during the storage phase, but does not affect tuber initiation. To study the impact of increased sucrolytic activity on tuber development, a yeast-derived invertase, targeted either to the cytosol or the apoplast, has been expressed in transgenic potato plants under the control of a tuber-specific class I patatin promoter (Sonnewald et al., 1997). In both cases sucrose content declined whereas hexose content, especially glucose, increased in mature tubers. Simultaneous expression of a heterologous glucokinase led to a reduction of the glucose content which was accompanied by decreased starch content (Trethewey et al., 1998). Surprisingly, elevated cytosolic invertase was found to cause a severe reduction in tuber yield, whereas over-expression of apoplastic invertase led to an increase in tuber size and a decrease in tuber number per plant. These data indicate that irrespective of the subcellular location of the enzyme, sucrose is hydrolysed in vivo, but the site of hexose formation strongly affects tuber development. The underlying mechanism for the observed differences is largely unknown. It has been speculated that apoplastic invertase expression may lead to an increased osmolarity of the apoplastic space, thereby stimulating sucrose unloading through the symplastic route. In agreement with this hypothesis, it has been suggested that unloading of sucrose occurs symplastically in developing tubers (Oparka, 1986; Oparka and Prior, 1988). Furthermore, cell turgor was shown to be an important regulator of sucrose uptake in tuber discs (Oparka and Wright, 1988) and sugar beet taproot tissue (Wyse et al., 1986). In contrast to Oparka and colleagues, who observed a stimulation of starch biosynthesis in tuber discs incubated in a 300 mM mannitol solution supplemented with glucose, the inhibition of starch biosynthesis has been reported (Geigenberger et al., 1997), which was explained by the stimulation of sucrose synthesis via activation of sucrose phosphate synthase leading to a reduced concentrations of 3PGA and a partial inhibition of ADP-glucose pyrophosphorylase. To clarify the obvious discrepancy, further investigations are needed. Alternatively, extracellular sugars may serve as signals stimulating cell division and sink growth, as has been suggested for legume seed development (summarized in Weber et al., 1997).
To understand the consequences of hexose release in different subcellular compartments of developing potato tubers, metabolic changes induced by either cytosolic or apoplastic yeast invertase were investigated. Here it is reported that hexoses originated in the apoplast do not lead to changes in the steady-state concentrations of phosphorylated intermediates compared to control tubers. Furthermore, biochemical analysis of tubers expressing cytosolic invertase revealed that sucrose hydrolysed via invertase fuels glycolysis rather than starch synthesis, indicating a possible substrate channelling depending on the sucrolytic system used and/or an inefficient uptake of hexose-phosphates into the amyloplast.
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Materials and methods |
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Plant material
Solanum tuberosum L. cv. Desirée was supplied by Saatzucht Lange AG (Bad Schwartau, Germany). Tuber-specific over-expression of cytosolic (U-IN-2) and apoplastic (U-IN-1) invertase was achieved by fusion of the portion of the yeast suc2 gene, encoding the mature invertase, with the class I patatin B33 promoter (Rocha-Sosa et al., 1989), either with or without the potato proteinase II signal peptide (Sonnewald et al., 1997). Following Agrobacterium-mediated gene transfer, three independent transgenic lines for each construct were selected for a detailed analysis.
The transgenic lines over-expressing invertase in the apoplast (U-IN-1-3, 33, 41) and in the cytosol (U-IN-2-17, 30, 34) used in the present study were described previously (Sonnewald et al., 1997). Tissue culture plants were propagated on MS medium (Murashige and Skoog, 1962) supplemented with 2% sucrose with a 16 h light and 8 h dark regime. One hundred plantlets of each genotype were grown in soil (2.5 l pots) in a greenhouse with 16 h supplementary light (200–300 µmol-1 photons m-2 s-1) and 8 h darkness. Relative humidity varied between 60% and 70% and the temperature was adjusted to 21 °C during the light and 18 °C during the dark phases. Plants were harvested at different times starting 2–3 weeks after transfer of the plants to the glasshouse, to obtain stolon tips without visible swelling (stage I), swelling stolon tips (stage II), small tubers (1.0–2.5 g fresh weight; stage III) and mature tubers (stages IV). Plants used for the analysis had no tubers of later developmental stages than the stage being analysed. This precaution was necessary since the presence of mature tubers was found to induce starch and storage protein accumulation in stolons of the same plant, not found in uninduced stolons (data not shown).
Chemicals
All enzyme were purchased from Boehringer Mannheim (Mannheim, Germany) and chemicals from either Sigma (St Louis, MO, USA) or Merck (Darmstadt, Germany).
Preparation and analysis of samples for enzyme activities
To measure enzyme activities, 50 mg stolon tips (stage I), 100 mg small induced tubers (stage II) or 100–200 mg potato tuber slices (stages III and IV) were homogenized in 0.25–0.5 ml 100 mM 4-(2-hydroxyethyl)-1-piperazine-ethanesulphonic acid (HEPES)—KOH, pH 7.5, 2 mM MgCl2, 1 mM EDTA, 1 mM EGTA, 5 mM mercaptoethanol, 15% glycerine, and 0.1 mM Pefabloc phosphatase inhibitor. After centrifugation for 10 min at 13 000 rpm and 4 °C, the supernatant was frozen immediately for later analysis. All enzyme activities were determined as described previously (Hajirezaei et al., 1994).
Metabolite determination
Metabolites were extracted essentially as described previously (Jelitto et al., 1992). Between 50 and 300 mg tissue material was frozen immediately in liquid nitrogen. After homogenizing the frozen material to a fine powder, 1.5 ml of 16% (w/v) trichloroacetic acid (TCA) in diethylether (4 °C) was added and the tissue further homogenized. After incubating the extract on dry ice for 15 min, 0.8 ml of 16% TCA (w/v) in water containing 5 mM EGTA (4 °C) was added to the homogenate, which was then left for an additional 3 h at 4 °C. Following centrifugation for 5 min at 15 000 rpm, the water phase was washed 3–4 times with 600 µl water-saturated ether each time and thereafter neutralized with 5 M KOH and 1 M triethanolamine.
The concentrations of metabolites and ATP/ADP were determined photometrically (Stitt et al., 1989) using a dual wavelength spectral photometer (Sigma-ZWS II, Germany). The recovery of small, representative amounts of each metabolite through the extraction has been documented (Hajirezaei et al., 1994).
Determination of soluble sugars and starch
Soluble sugars and starch were quantified in tuber samples extracted with 80% ethanol and 20 mM HEPES-KOH, pH 7.5 as described earlier (Sonnewald, 1992).
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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Patatin promoter-driven invertase activity increases during potato tuber development in parallel to storage protein accumulation
Representative examples of invertase activity at selected stages of tuber development are presented in Fig. 1A
. As expected, invertase activity driven by the patatin class I B33 promoter increased during tuber development (Fig. 1B) in parallel with patatin accumulation (data not shown). At stage II, acidic invertase activity of apoplastic lines was 2–3.5-fold and in cytosolic lines 2–3-fold higher than in control tubers (Fig. 1B). Invertase activity reached its maximum at stage III. At stage IV, tubers expressing apoplastic invertase (U-IN-1) activity were 17–24-fold higher and, in those expressing cytosolic invertase (U-IN-2), 10–18-fold higher than in control tubers. This increase in acidic invertase activity is mainly due to increased expression of the heterologous enzyme since the endogenous acidic invertase decreased slightly during development whereas a strong decline of acidic invertase activity in control tubers was observed. As has been reported earlier, sucrose synthase activity increased during tuber development in wild-type plants. This increase was largely unchanged in the transgenic lines. However, a slight decrease in sucrose synthase activity was visible at stage IV in plants expressing cytosolic invertase (Fig. 3).Based on results obtained on plants with antisense to sucrose synthase, decrease of this enzyme activity should not lead to significant biochemical changes (Zrenner et al., 1995).
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), 1-33 (
) and 1-41 (
)). and in the cytosol (U-IN-2-30 (
), 2-17 (
) and 2-34 (
)), over four developmental stages. Sucrose synthase (A, D, G) activity; fructokinase (B, E, H) activity; glucokinase (C, F, I) activity. Data are presented as the mean±SE of measurements from about ten plants (stolons) and from four plants (tubers).
Expression of cytosolic and apoplastic invertase leads to a decreased sucrose and an increased glucose content
Sucrose uptake in mature potato tubers has been suggested to occur via the symplastic route. This conclusion was mainly based on counting the number of plasmodesmata and dye distribution experiments (Frommer and Sonnewald, 1995; Oparka and Prior, 1988). Nevertheless, in mature tubers, expression of cytosolic and apoplastic 
invertase has been shown to result in a strong reduction of the sucrose content (Sonnewald et al., 1997). Thus, sucrose must be available in the apoplastic space. The sugar content of transgenic and control tubers was, therefore, measured during tuber development to investigate whether this is true for all developmental stages. As expected no significant difference in soluble sugars was observed in non-induced and swelling stolon tips of control and transgenic plants (stages I and II; Fig. 2). This might be explained by the low activity of the patatin promoter at these developmental stages and the already high amount of hexoses found in the untransformed control. Starting at stage III, sucrose content declined and glucose content increased in both transgenic lines. Fructose and starch content was found to be largely unaffected by the presence of the invertase activity (Fig. 2).
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Increased activity of cytosolic invertase strongly affects accumulation of phosphorylated intermediates
To study sugar metabolism in more detail, hexose-phosphates, UDP-glucose and the accumulation of glycolytic intermediates were analysed during tuber development. In control plants, all metabolites investigated declined from stage I to stage IV, with the exception of UDP-glucose. The content of UDP-glucose remained unaltered (data not shown). Metabolite accumulation in tubers expressing apoplastic invertase was unaltered compared to wild type. In contrast, analysis of plants expressing cytosolic invertase revealed that hexose phosphates and glycolytic intermediates accumulated as tubers developed from stage I to stage IV (Fig. 4). Accumulation of both glycolytic intermediates and hexose phosphates, can be taken as further evidence that downstream processing, rather than the phosphorylating capacity of the tuber tissue, limits the use of hexoses and may cause the sugar accumulation observed.
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The availability of ATP and the activity of hexose phosphorylating enzymes cannot explain the inefficient use of the liberated hexoses
There were no differences in amounts of the major carbohydrates in transgenic and control tubers in cytosolic and apoplastic invertase expressing tubers (Fig. 2). In addition, glucose content increased greatly during development, indicating inefficient use of the liberated hexoses in the transgenic tubers, possibly caused by a rapid compartmention of the hexoses and/or insufficient hexose phosphorylating capacity of the storage parenchyma cells. To determine the hexose phosphorylating capacity, the ATP/ADP content and the hexose phosphorylating enzyme activity of transgenic and control tubers were determined during development. As evident from the data shown in Fig. 4, the ATP content of untransformed control tubers strongly declines during development. However, no difference in the ATP content of control and transgenic tubers could be detected throughout development (Fig. 4). Furthermore, the ATP to ADP ratio was unaffected by the presence of the heterologous invertase and did not change significantly during development (data not shown). Thus, insufficient ATP availability is unlikely to be the cause of the observed hexose accumulation.
To investigate whether the activity of hexose phosphorylating enzymes might be reduced in the transgenic plants, glucokinase and fructokinase activities were measured at the developmental stages indicated (Fig. 3 ). In contrast to what has been reported for the cultivar Record (Ross et al., 1994), a strong but transient increase of fructokinase activity was observed at stage II (swelling stolon tips). This transient increase was found in all plants analysed (Fig. 3). At stage IV (mature tubers) fructokinase activity was increased by up to 7-fold and glucokinase by more than 2-fold in plants expressing cytosolic invertase compared to untransformed controls. In the case of plants expressing apoplastic invertase, fructokinase and glucokinase activities remained unaltered. Based on these results inefficient phosphorylation of glucose is unlikely to be the reason for the observed accumulation of glucose.
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Conclusion |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionReferences |
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The results reported here demonstrate that sucrose is available in the apoplastic space throughout tuber development. Furthermore, hydrolysis of sucrose in the apoplastic space does not perturb glycolysis and does not lead to accumulation of hexose phosphates. In contrast, cytosolic expression of invertase leads to dramatic changes in primary metabolism. Similar results have also been obtained by analysing double transformants carrying an AGPase antisense and an invertase sense construct (Trethewey et al., 1999). The authors concluded that regulation of glycolysis is linked to cytosolic sucrose hydrolysis. A possible explanation for the observed differences between apoplastic and cytosolic invertase could be an endocytotic uptake mechanism into the vacuole as previously suggested (Oparka and Prior, 1988).
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Acknowledgements |
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The authors are grateful to Ulrike Schlereth and Christiane Prüßner for tuber harvest and technical assistance. We thank Andrea Knospe for taking care of the tissue culture plants, Birgit Schäfer and Heike Ernst for patient photographic work, Hellmuth Fromme, and the greenhouse personnel for attending plant growth and development, and Karin Herbers for critically reading the manuscript.
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Footnotes |
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3 Present address: Department of Crop Breeding, Kyushu National Agricultural Experiment Station, Suya 2421, Nishigoshi, Kumamoto, 861–1192, Japan.
4 To whom correspondence should be addressed. Fax: +49 39482 5515. E-mail:sonnewal{at}ipk\|[hyphen]\|gatersleben.de
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