Plant Physiol. (1998) 117: 575-584

The Role of Gibberellin, Abscisic Acid, and Sucrose in the Regulation of Potato Tuber Formation in Vitro¹

Xin Xu, André A.M. van Lammeren, Evert Vermeer, and Dick Vreugdenhil^*

Graduate School Experimental Plant Sciences, Department of Plant Physiology (X.X., E.V., D.V.), and Department of Plant Cytology and Morphology (X.X., A.A.M.v.L.), Wageningen Agricultural University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands

	ABSTRACT

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The effects of plant hormones and sucrose (Suc) on potato (Solanum tuberosum L.) tuberization were studied using in vitro cultured single-node cuttings. Tuber-inducing (high Suc) and -noninducing (low Suc or high Suc plus gibberellin [GA]) media were tested. Tuberization frequencies, tuber widths, and stolon lengths were measured during successive stages of development. Endogenous GAs and abscisic acid (ABA) were identified and quantified by high-performance liquid chromatography and gas chromatography-mass spectrometry. Exogenous GA_4/7 promoted stolon elongation and inhibited tuber formation, whereas exogenous ABA stimulated tuberization and reduced stolon length. Indoleacetic acid-containing media severely inhibited elongation of stolons and smaller sessile tubers were formed. Exogenous cytokinins did not affect stolon elongation and tuber formation. Endogenous GA₁ level was high during stolon elongation and decreased when stolon tips started to swell under inducing conditions, whereas it remained high under noninducing conditions. GA₁ levels were negatively correlated with Suc concentration in the medium. We conclude that GA₁ is likely to be the active GA during tuber formation. Endogenous ABA levels decreased during stolon and tuber development, and ABA levels were similar under inducing and noninducing conditions. Our results indicate that GA is a dominant regulator in tuber formation: ABA stimulates tuberization by counteracting GA, and Suc regulates tuber formation by influencing GA levels.

	INTRODUCTION

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Hormones have been suggested to play a prominent role in the control of tuberization (for review, see Ewing, 1987; Vreugdenhil and Struik, 1989). The possible role of GAs in this process was extensively studied, mainly in experiments in which this compound was applied exogenously. These experiments showed that application of GA promotes stolon elongation and inhibits tuber formation (Smith and Rappaport, 1969; Kumar and Wareing, 1972). It was also reported that a decline of GA activity in potato (Solanum tuberosum L.) plants is associated with tuberization (Okazawa, 1959, 1960; Smith and Rappaport, 1969; Pont Lezica, 1970; Railton and Wareing, 1973; Krauss and Marschner, 1982). Although the inhibiting effect of GA on potato tuberization is well documented, the interaction between GA and other regulating factors on the control of tuberization is still a matter of debate. ABA is normally regarded as a regulator that reduces GA-promoted processes in plant development. It was assumed that ABA is a promoting hormone in potato tuberization (Okazawa and Chapman, 1962; Marschner et al., 1984). However, the functions of ABA with respect to stolon elongation, tuber initiation, and tuber growth are not clear.

Most of the data concerning GA levels obtained from potato come from the determination of endogenous GA-like substances by bioassays (Okazawa, 1959, 1960; Smith and Rappaport, 1960, 1969; Boo, 1961; Rappaport and Smith, 1962; Racca and Tizio, 1968; Pont Lezica, 1970; Railton and Wareing, 1973). These reports described the determination of GA activity in leaves, roots, sprouts, and mature and resting tubers of potato. However, they did not present information about GA levels in the tuber-forming stolon, and the various types of GAs could not be identified with bioassays. In addition, the data might be unreliable because of the interference of acidic growth inhibitors (Jones et al., 1988). Because the concentration of GAs in plants can be extremely low, especially in vegetative parts, a highly sensitive detection method, combined GC-MS, is used more frequently for the precise analysis of GAs. Jones et al. (1988) applied GC-MS to determine the levels of GAs in mature tubers. They detected GA₂₀ and GA₁ in sprouts of potato tubers, but their interest and data were mainly focused on the GA-analysis technique. GA₁ was detected by GC-MS in potato leaves, and higher levels were found in tall plants, as compared with dwarf plants, only the latter ones tuberizing under long-day conditions (Van den Berg et al., 1995a, 1995b). To our knowledge, there is no report of the determination of endogenous GA levels during the whole developing process of tuber formation with GC-MS.

The effects of ABA on potato tuberization have been investigated with a number of experiments. El-Antably et al. (1967) observed a stimulation of tuber formation by ABA applied to the leaves of long-day-grown potato plants. Wareing and Jennings (1980) found that ABA can replace the effect of the leaf by promoting tuberization in induced cuttings. The promoting effect of exogenous ABA was also demonstrated by the increasing numbers of tubers (Abdullah and Ahmad, 1980), the earlier initiation of tubers, and the formation of sessile tubers (Menzel, 1980). However, other reports described inhibition of tuberization by ABA, with the effect depending on concentration and variety (Palmer and Smith 1969b; Hussey and Stacey, 1984). The analysis of endogenous ABA showed an increase of ABA level under tuber-inducing conditions (Krauss and Marschner, 1982) and a reduction of ABA content when N was supplied during tuber formation (Marschner et al., 1984). Further studies are needed to clarify the conflicting data concerning the effect of ABA on tuberization.

In contrast to GA and ABA, less attention has been paid to cytokinins and IAA. Palmer and Smith (1969a) first reported an increase of the tuberization frequency on various cytokinin-containing media. Their observation was supported by further investigations of exogenous cytokinins (Kumar and Wareing, 1974; Hussey and Stacey, 1984). The level of endogenous cytokinins was high in the induced tissue (Mauk and Langille, 1978) and also during the later stage of tuber growth (Obata-Sasamoto and Suzuki, 1979). However, exogenous cytokinins may also convert a stolon into a leaf-bearing shoot (Kumar and Wareing, 1972). Harmey et al. (1966) observed that IAA treatment induced larger tubers at an earlier stage, whereas Obata-Sasamoto and Suzuki (1979) reported that the auxin content was high in the stage before tuber initiation and decreased during tuber development.

In addition to hormones, the level of sugars in the medium, notably Suc, also affects tuberization in vitro (Lawrence and Barker, 1963). However, not much is known about a possible interaction between hormonal and nutritional regulation of tuber formation.

In this study we used a well-defined tuberization system, culturing single-node cuttings in vitro. Uniform growth of stolons and tubers was obtained under tuber-inducing and -noninducing conditions by varying the level of Suc in the medium. The possible roles of GA and ABA were assessed in two ways: by applying these regulators to the culture medium and by measuring endogenous levels under inducing and noninducing conditions using GC-MS. In addition, the effects of exogenous cytokinins and auxin were determined.

	MATERIALS AND METHODS

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In Vitro Culture of Single-Node Cuttings

1

1

Exogenous Hormones and Suc Treatments

1

1

Determination of Endogenous GA and ABA Levels

For each sample, at least 0.3 g fresh weight was used. Every sample included 10 to 200 developing buds, depending on the developmental stage. The samples were homogenized in liquid N₂. Then, 200 mL of 80% methanol was added together with 0.25 g of ascorbic acid to prevent oxidation reactions during the extraction. The homogenate was stirred overnight at 4°C. The insoluble material was removed first by centrifugation at 18,000g for 30 min and then by filtration with a no. 4 glass filter.

Internal standard GAs (1 mL each of 100 ng/mL [²H]GA₁, [²H]GA₄, and [²H]GA₉ from Dr. L.N. Mander, Canberra, Australia) were added to the filtrate. Two hundred and fifty microliters of [³H]ABA (35,000 dpm) and approximately 0.1 ng of [³H]GA_1, [³H]GA₄, and [³H]GA₉ (specific activity 3000-4000 Bq ng¹) containing 420 Bq of each GA were added, and radioactivity was checked at successive steps to monitor the loss of GAs and ABA during purification. The amount of tritiated tracer added was less than 5% of the amount in the samples, and no correction was made. The aqueous methanol was evaporated under reduced pressure at 35°C. The residue was dissolved in 15 mL of water and adjusted to pH 8.0. The sample was washed with petroleum ether (3 times 50 mL) to remove lipids, fats, pigments, etc. The aqueous sample was then poured onto a PVP column to remove acidic impurities. The sample was adjusted to pH 2.5 and partitioned against ethyl acetate.

The ethyl acetate fraction containing the free GAs and ABA was partitioned against 5% sodium bicarbonate to leave the neutral compounds in ethyl acetate. Then the sodium bicarbonate solution with the free GAs and ABA was partitioned against ethyl acetate again and dried. The residue was dissolved in 10 mL of water, adjusted to pH 8.0, and applied onto a 5-cm-long QAE-Sephadex A-25 (Pharmacia) column that had been equilibrated with 1% sodium formate at pH 8.0. Neutral impurities were washed off with water (70 mL). The GAs and ABA were eluted with 0.2 M formic acid (20 mL) and loaded onto a C₁₈ Sep-Pak cartridge (Waters), which was prewashed with 5 mL of diethyl ether, 5 mL of methanol, and 10 mL of water. After the cartridge was washed with 2 mM acetic acid plus 1% methanol (10 mL), GAs and ABA were eluted with 5 mL of 80% methanol. The aqueous methanol solution was completely evaporated at 35°C under low pressure. Up to this stage, GAs and ABA were purified together.

HPLC was used to separate GAs and ABA into different fractions. The sample was dissolved in 1 mL of 30% methanol and injected onto a Chromsphere C₁₈ column (Chrompack, Middleburg, The Netherlands) and eluted with a linear gradient of methanol (10-70%), containing 0.01% acetic acid, at a flow rate of 4 mL/min. The retention times of various GAs and ABA were determined by monitoring the elution of standards at 210 nm. The retention times were 19.0 to 21.0 min for GA₁, 28.5 to 30.5 min for GA₂₀, 31.5 to 33.5 min for GA₄, and 34.5 to 36.5 min for GA₉. The retention time of ABA was 24.0 to 26.0 min. The collected fractions were methylated with excess ethereal diazomethane and fractionated again using the same HPLC system and gradient. The retention times shifted 2 to 3 min for each fraction.

Putative methyl-GA- and methyl-ABA-containing fractions were collected. The dried fractions were trimethylsilylated with Deriva-sil (15 µL, Chrompack, Raritan, NJ) at 70°C for 10 min. Derivatized samples were analyzed using a GC-MS system (model 5970, Hewlett-Packard). Samples (4-5 µL) were injected into an Ultra-1-fused silica capillary column (Hewlett-Packard; cross-linked methyl silicone gum; 25-m × 0.2-mm × 0.33-µm film thickness) at an oven temperature of 70°C with the injector splitter closed. After 45 s the splitter was opened, and 2 min later the oven temperature was increased at a rate of 30°C min¹ to 250°C and then at a rate of 4°C min¹ to 300°C and held at that temperature for 9.5 min. The injector and the interface temperature were 250 and 290°C, respectively. After 12 min, mass spectra were acquired by scanning from 200 to 600 or by selected ion monitoring using the following ions: for GA₁, ions 506 and 508; for GA₄, ions 284, 286, 418, and 420; for GA₉, ions 298 and 330; and for GA₂₀, ions 418 and 420. For GA and ABA identification, the Kovats retention index values were determined with a paraffin series for the Ultra-1 column. The spectra were compared with pure standards or to published spectra (Gaskin and MacMillan, 1991). For quantification, corrected calibration curves were made for each GA by isotope-dilution analysis.

	RESULTS

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Effects of Suc and Exogenous Hormones on Tuber Formation

View larger version (133K): [in this window] [in a new window]   Figure 1. (Continued from facing page.) Photographs showing development of single-node cuttings of potato plants grown in vitro on various media after 10 d of culture. Each photograph, except D, shows one to five representative cuttings for a culture condition. A, Tuber-inducing treatment with 8% Suc in the nutrient medium. B, Noninducing treatment with 1% Suc. C, Noninducing treatment with 8% Suc plus 0.5 µM GA4/7. D, A series of Suc concentrations: 8, 6, 4, 2, and 1% from left to right. E, 8% Suc plus 0.01 µM GA4/7. F, 8% Suc plus 0.03 µM GA4/7. G, 8% Suc plus 0.1 µM GA4/7. H, 8% Suc plus 0.3 µM GA4/7. I, 8% Suc plus 1.0 µM GA4/7. J, Formation of secondary stolons after transfer of the cuttings from 8% Suc medium to 8% Suc plus GA4/7 medium at d 5 (the bottom cutting) or at d 10 (the two top cuttings) and further culture for 5 d. K, Formation of secondary tubers by transferring cuttings first from 8% Suc medium to 8% Suc plus GA4/7 medium at d 5 and then back to 8% Suc medium at d 10 and further culturing for 5 d. The short arrow points to the first tuber and the long arrow points to a secondary one. L, 8% Suc plus ABA. M, 8% Suc plus IAA. N, 1% Suc plus ABA; arrow indicates the short stolon. O, 1% Suc plus IAA. P, 8% Suc plus GA4/7 plus ABA. Q, 8% Suc plus GA4/7 plus IAA. R, 8% Suc (top line) and 8% Suc plus BA (bottom line).

Suc

View larger version (23K): [in this window] [in a new window]   Figure 2. Effects of a series of Suc concentrations on potato tuber formation in hormone-free medium. Data are based on 20 single-node cuttings for each Suc concentration. A, Tuberization frequency during 10 d of culture. B, Average stolon or tuber width () and stolon length () at d 10 at various Suc concentrations. Bars indicate SEs when exceeding the size of the points.

GA

View larger version (25K): [in this window] [in a new window]   Figure 3. A, Effects of a series of GA4/7 concentrations on tuber formation. Data are based on 20 single-node cuttings. B, Tuberization frequency on medium with 3.7 µM ABA supplemented with a series of Suc concentrations. C, Tuberization frequencies on media with 8% Suc plus 3.7 µM ABA (closed symbols) and on media with 8% Suc without ABA (open symbols), supplemented with various concentrations of GA4/7.

A transfer experiment was done to further analyze the effect of GA on stolon elongation and tuber formation. Cuttings were grown on medium with 8% Suc without GA for 5 d. When stolon tips swelled to form small tubers, the cuttings were transferred to medium with 8% Suc plus 0.5 µM GA_4/7. Two days later, stolons developed from the apical region of the young tubers. The tuber size remained unchanged during further culture (Fig. 1J, bottom cutting). These cuttings with tubers and secondary stolons were transferred back to the medium with 8% Suc without GA_4/7 at d 10. New tubers were formed at the stolon tips at approximately d 14 (Fig. 1K).

When a developing bud was transferred before tuber formation from 8% Suc to 8% Suc plus GA medium, i.e. before d 5, that stolon continued to elongate (data not

ABA, IAA, and BA

The effect of ABA was studied further by treating cuttings with a series of Suc concentrations at a constant ABA level. In contrast to the experiment with various Suc concentrations without ABA (Fig. 2A), 100% tuberization occurred at all concentrations of Suc when ABA was added to the media (Fig. 3B). The inhibiting effect of GA could partly be overcome by the addition of ABA to the medium (Fig. 3C).

Determination of Endogenous GA and ABA Levels under Tuber-Inducing and -Noninducing Conditions

GA

The same qualitative differences in GA₁ levels were observed in the second series of experiments. At d 5 and 10, GA₁ levels were highest in stolons grown at 1% Suc and 3- to 6-fold lower in tubers developing on 8% Suc medium (Fig. 4A). Comparing tuber-inducing (8% Suc) and -noninducing (1% Suc) conditions, it appeared that the level of GA₁ increased more than 5-fold during the first 2 d of culture in both treatments (Fig. 4A). This coincided with the onset of stolon formation. The level remained high under noninducing conditions, whereas it sharply decreased in the inducing treatment at d 4, i.e. 1 d before visible swelling. It decreased further at d 5 and remained low thereafter. In another noninducing treatment (8% plus GA_4/7), the endogenous level of GA₁ increased gradually until d 5 and then slightly decreased, reaching an intermediate level at d 10. 

View larger version (23K): [in this window] [in a new window]   Figure 4. Endogenous contents of GA1 and ABA during the development of axillary buds of potato under one tuber-inducing condition (medium with 8% Suc) and two noninducing conditions (media with 1% Suc or 8% Suc plus 0.5 µM GA4/7). Data were obtained from 10 to 200 cuttings per sample. A, GA1 content. B, ABA content.

Comparing the two experiments, a similar pattern of the changing GA₁ levels was obtained, although the absolute levels varied between the two experiments.

ABA

Localization of GA₁ Content in Developing Stolons and Tubers

At d 4, which was 1 d before visible swelling, the GA₁ level in the stolon tip for all three culture conditions (8% Suc, 1% Suc, and 8% Suc plus GA) was much higher than the average GA₁ level in the whole stolon (Fig. 5A). Comparing the three conditions, the stolon tips contained high GA₁ levels in the 1% Suc- and 8% Suc plus GA_4/7-noninducing conditions and a low GA₁ level in the inducing condition (8% Suc). The latter one would start swelling 1 d later. At d 10, tubers and stolons in the 8% Suc-inducing condition both had much lower levels of GA₁ than those grown in the two noninducing conditions (Fig. 5B). Stolons grown in the 1% Suc-noninducing condition showed a high level of GA₁ in the tip and a relatively low GA₁ level in the elongated part of the stolon. In the 8% Suc plus GA_4/7 treatment, the stolon tip had almost the same GA₁ level as found in the elongated part of the stolon.

View larger version (18K): [in this window] [in a new window]   Figure 5. Localization of GA1 in various regions of developing stolons of potato cuttings cultured under tuber-inducing (8% Suc) and -noninducing conditions (1% Suc and 8% Suc plus GA4/7) at d 4 (A) and at d 10 (B). The data inside of the drawings indicate GA1 concentrations (ng g1) in those regions. The data in the boxes above the drawings are derived from Figure 4 and represent GA1 levels (ng g1) in the whole developing stolon. Data are averages of duplicate measurements on samples from a single series of experiments, unless the amount of tissue was insufficient for replication.

	DISCUSSION

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GAs

It could be argued that tuberization causes the change in GA levels rather than vice versa. However, the timing of both processes favors a prime role for GA. Moreover, studies with GA-synthesis inhibitors (Perl et al., 1991; Vreugdenhil et al., 1994), as well as analysis of GA-deficient lines (Van den Berg et al., 1995b), also point to a crucial role of GA in regulating tuber formation.

The prominent role of endogenous GA on tuberization was supported further by observations of the effects of GA_4/7 in the medium on the development of the axillary buds of the cuttings. Increasing concentrations of exogenous GA_4/7 progressively inhibited tuber initiation, reduced the final size of the tubers, and stimulated stolon elongation.

In a previous study we observed that, depending on the presence or absence of GA in the medium, cell division in the subapical region of developing stolons is either transverse, resulting in further elongation of the stolon, or longitudinal, leading to tuber formation (Xu et al., 1998). Therefore, we hypothesized that this region is especially sensitive to GA. This idea is supported by the results of the transfer experiments (Fig. 1, J and K): applying or removing GA switches elongation of the stolons on and off by acting on the apical meristematic region, leaving the more basal parts of the developing axillary bud unaltered. To further test this hypothesis we also analyzed GA₁ levels in various parts of developing buds separately. The GA level was much higher in the stolon tip than in the basal part of the stolon; it was also higher in the young stolon tip than in the mature stolon tip, whereas it was extremely low in the swelling tuber. The changes in GA₁ levels, as induced by culture conditions, were much more extreme in the apical part than in the rest of the stolon. As stated by Brent Loy (1977), GA promotes cell division and cell elongation in the subapical meristem. High GA levels might keep the transversal cortical microtubular cytoskeleton stable so that cells in the subapical region divide transversally, and cell elongation will hence result in stolon elongation. Low GA levels cause reorientation of cortical microtubules to longitudinal or oblique directions and then allow the cells in the subapical region to enlarge and divide longitudinally, leading to the swelling of the tuber (Shibaoka, 1993; Sanz et al., 1996).

ABA

Analysis of endogenous ABA levels showed that the levels decreased during the first 2 d of culture for all three treatments (8% Suc, 1% Suc, and 8% Suc plus GA) and remained low from d 5 to 10. No differences were detected among the three treatments. Hence, we conclude that ABA is not likely to be the main regulator of tuber formation. The effect of exogenous ABA, as observed here and in other experiments (Krauss and Marschner, 1982), is proposed to be due to an antagonistic effect between ABA and GA. Alternatively, exogenously applied ABA might stimulate tuber formation by inhibiting stolon elongation, a prerequisite for tuber formation (Vreugdenhil and Struik, 1989).

Cytokinins and IAA

The application of IAA in the tuber-inducing medium led to earlier tuber initiation, as also mentioned by Harmey et al. (1966). Contrary to their observation, slightly smaller tubers were formed, which were all sessile. In the presence of GA, addition of IAA resulted in much shorter stolons than found under GA conditions alone. The growth of the lateral buds of the cuttings was totally blocked with the application of IAA in 1% Suc medium. Thus, it seems that IAA has a significant negative effect on elongation under both tuber-inducing and -noninducing conditions. We assume that this inhibition of tuber formation is due to the well-known effect of stimulation of ethylene production by IAA, which in turn reduces stolon elongation (Vreugdenhil and van Dijk, 1989). IAA would, therefore, indirectly favor tuber formation by blocking stolon elongation and counteracting effects of endogenous GA.

Interaction between Suc and Hormones

Contrary to GA, the endogenous ABA levels did not vary under both 8% and 1% Suc conditions. This is in agreement with the report by Van den Berg et al. (1991), in which it was pointed out that changes in carbohydrate levels were not triggered by a change in ABA levels. These data support the hypothesis that Suc acts as a regulator by influencing endogenous GA levels during tuber formation.

In conclusion, it is clear that GA is a dominant regulator, responding to the environmental conditions and controlling all steps of tuber formation, as a stimulus in stolon elongation and an inhibitor in both tuber initiation and growth. Other plant hormones are assumed to be involved in the regulation of tuber formation as well; however, their effects seem to depend on the final GA content in the tissues. ABA functions as an antagonist of GAs, and Suc regulates tuber formation by changing the GA level of the developing stolons and tubers.

	FOOTNOTES

   Received November 6, 1997; accepted March 6, 1998.

	ACKNOWLEDGMENTS

We thank Wilma Pons-Drexhage and Jan Vos for their assistance with the in vitro cultures, Henk Kieft for technical assistance with the morphological investigations, and Sijbout Massalt and Allex Haasdijk for photography and art work.

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