Behavior of carbohydrates in mother and daughter bulbs of tulips (Tulipa gesneriana)
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1 Soil Science and Plant Nutrition ISSN: (Print) (Online) Journal homepage: Behavior of carbohydrates in mother and daughter bulbs of tulips (Tulipa gesneriana) Takuji Ohyama, Taro Ikarashi, Tizuko Matsubara & Akira Baba To cite this article: Takuji Ohyama, Taro Ikarashi, Tizuko Matsubara & Akira Baba (1988) Behavior of carbohydrates in mother and daughter bulbs of tulips (Tulipagesneriana), Soil Science and Plant Nutrition, 34:3, , DOI: / To link to this article: Published online: 04 Jan Submit your article to this journal Article views: 321 Citing articles: 6 View citing articles Full Terms & Conditions of access and use can be found at
2 Soil Sci. Plant Nlttr., 34 (3), , 1988 BEHAVIOR OF CARBOHYDRATES IN MOTHER AND DAUGHTER BULBS OF TULIPS ( Tulipa gesneriana) Takuji OHYAMA, Taro IKARASHI, Tizuko MATSUBARA, and Akira BABA Department of Agricultttral Chemist13,, Faculty of Agrictdtltre, Niigata University, Niigata, Japan Received September 18, 1987 The changes in the reserve carbohydrate constituents were observed in the mother bulb scales and bulblets of tulip plants (Tulipa gesneriana) grown in a culture solution. At the time of planting, starch was the predominant reserve carbohydrate in mother bulb scales. The starch content decreased continuously until January, but starch degradation was interrupted for about 2 months until sprouting occurred. Thereafter rapid starch consumption resumed and the starch content was depleted until anthesis. The concentration of soluble carbohydrates especially the sucrose concentration in the mother bulb scales increased rapidly in winter, with maximum values of 64 mg/g FW on January 13. Regarding the changes in the fructosylsucrose content after planting, the content of isokestose (GFz) increased, and that of nystose (GF3) remained constant, while the content of pentasaccharide (GF4) and insoluble fructan with a high degree of polymerization decreased as in the case of starch. All the fructosylsucroses were consumed rapidly after sprouting, and the content was completely depleted at antbesis. Therefore, starch and the oligofructans with a high degree of polymerization (DP>5) are considered to be reserve carbohydrate sources for the development of the roots and shoots as well as for nutrient absorption before the onset of photosynthesis. On the other hand, sucrose and isokestose converted from starch and oligofructan were considered to be temporary storage carbohydrates accumulated in the mother bulb scales during the winter season. Regarding the behavior of carbohydrates in the bulblets, the starch content increased significantly after the removal of a flower (defloration). The sucrose concentration also increased markedly after defloration, showing a maximum value of about 20 mg/g FW. The content of the fructans with a low degree of polymerization (DP<5) which was initially negligible, increased as in the case of sucrose. On May 12, the concentration of isokestose and nystose was found to be very high, i.e. 15 and 8 mg/g FW, respectively. Thereafter the concentration decreased markedly until the maturity stage. Therefore, the low DP fructosylsucroses as in the case of sucrose are considered to be carbohydrates temporarily accumulated in the bulblets, some of which could be converted to starch as maturation proceeds. Based on morphological observations, two types of starch granules were observed in the bulb scales, one which consisted of large granules with a thin lenticular shape and the other Abbreviations: DMSO, dimethylsulfoxide; DP, degree of polymerization; DW, dry weight; Frc, fructose; FW, fresh weight; GFn, fructosylsucroses in which n molecules of Frc residues are combined with Glc; Glc, glucose; Suc, sucrose. 405
3 406 T. OHYAMA, T. IKARASHI, T. MATSUBARA, and A. BABA type which consisted of small granules spherical in the shape. The small granules were produced in the bulblets just before maturation and they disappeared immediately after planting. Key Words: tulip, bulb, starch, fructan. Tulip plants (Tulipa gesneriana) store a large amount of carbohydrates in the bulb scales for supporting the root and shoot development and for nutrient absorption during the underground life. Starch is also known to be a major source of carbohydrates for tulip bulbs (AuNG et al. 1973). In addition, Glc, Frc, Suc, and/3(2-1)-linked fructosylsucrose are the principal soluble constituents (HAMMER 1969; MOE and WICK- STROM 1973; OHYAMA et al. 1985a, 1986). It was reported that the content of inulin (ethanol insoluble high DP oligofructan) was very low in planting bulb scales of tulip plants (MOE and WICKSTROM 1973; OHYAMA et al. 1986), whereas, the content of low DP fructosylsucroses was high (OHYAMA et ai. 1986). Therefore, it was assumed that all the low DP fructosylsucroses in tulip bulbs not necessarily play a role as precursors of inulin synthesis. Very few reports have been published on the changes of the concentration of fructosylsucroses in the mother and daughter bulb scales of tulip plants throughout the growth period, and their physiological role is not fully understood. Many studies have dealt with the effect of cold treatment on carbohydrate changes in bulb scales in relation to forcing cultivation (AuNG 1976; DAVIES and KFMPrON 1975; HAALAND and WmKSTROM 1975; MOE and WICKSTROM 1973, 1979), and it has been reported that cold treatment enhanced starch degradation and the accumulation of Suc and low DP fructosylsucroses (MoE and WICKSTROM 1973). The interconversion of carbohydrates, starch ~ sucrose,~-fructosylsucrose, was suggested by the injection of [U-14C]sucrose to bulb scales, and the reaction rates were affected by the temperature during the treatment (HAALAND and WIC~:STROM 1975). In this report, the changes in the concentration of the carbohydrate constituents were observed in the bulb scales of tulip plants from planting to maturity, either in relation to their utilization in the mother bulb scales or their accumulation in the bulblets. The role of the accumulation of low DP fructosylsucroses in the mother and daugher bulb scales will be discussed. In addition, the changes in the shape and size of the starch granules were observed by scanning electron microscopy. MATERIALS AND METHODS Tulip plants were cultivated in solution culture. Eight bulbs ( g FW) each were planted in a 1/2,000 Wagner pot containing 9.5 liters of culture solution. Tulips were planted in demineralized water on October 26, and Ca (20 ppm) and B (0.2 ppm) were added from November 8. After November 17 the composition of the culture solution was as follows (rag/liter): NH~NOa, 17.1; Ca(NO3)2"4H20, 76.0; CaCI2.2H~O,
4 Behavior of Carbohydrates in Tulip Bulbs ; Na2HPO4-12H20, 30.2; K2SO4, 33.5; MgSO4-7H,O, 76.1; FeSO~.7H20, EDTA.2Na, 13.32; HsBO4, 1.14; CuSO4.5H20, 0.012; ZnSO4.7H20, 0.022; MnSO4. 5H20, 0.219; (NH~)6MoTO24.4H20, The culture solution was intermittently aerated, and changed frequently. Defloration treatment was carried out on April 27, in which the flower was removed by conventional method. Tulip plants were harvested periodically during their development, and the mother bulb scales or an innermost bulblet were cut into two symmetrical pieces, half of which were immediately extracted with 80~/o ethanol and the carbohydrate contents were measured, the other halfs being dried and used for the measurement of DW. After the mother bulb scales or bulblets were extracted with 80~ ethanol, the residues were washed twice with 80~ ethanol, and the extract and washings were combined together. The residue was freeze-dried and ground into a fine powder. Then 50 mg of the residue was further extracted with a DMSO-HCI solution. Starch content was analyzed using an enzymatic method (B6ehringer Mannheim F-Kit Starch). The content of 80~ ethanol insoluble fructan (inulin) was measured by the resorcin- HC1 method using the DMSO-HC1 extract prepared for the starch analysis. Total amount of Glc and Frc including the combined forms in the ethanol extract was calculated from the data based on two colorimetric analyses usiqg the resorcin-hcl and of phenol-h2so4 methods. The content of mono- and disaccharides was determined by gas chromatography in the form of trimethylsilyl derivatives. The fructosylsucroses (DP~<5) were analyzed by high performance liquid chromatography. The analytical details were the same as those described in the previous paper (OHYAMA et al. 1986). Morphological observations of the shape of the starch granules were performed on the basis of secondary electron scanning images using an electron probe X-ray microanalyzer (Shimadzu ARL EMX-SM). RESULTS AND DISCUSSION Figure 1 shows the changes in the DW of each part of the tulip plant. The DW of the mother bulb scales decreased gradually after planting to half of the initial value at the time of sprouting. Thereafter the DW declined rapidly until anthesis occurred. The FW of the mother bulb scales which had remained almost constant before the bolting stage decreased rapidly. As a result, the DW/FW ratio decreased linearly from 37 to 11~. Roots developed rapidly just after planting, showing a maximum DW value o11 February 21, and then the development declined slightly. After sprouting on March 9, the leaves, stem, and flower grew rapidly, in this sequence. Following defloration, the bulblets grew very rapidly, and the harvested bulblets accounted for about 20 g DW, which was 7 times higher than the value recorded in the mother bulb. The FW of the bulblets increased linearly after the bolting stage (March 30), whereas the rapid increase in DW started one month later (April 27). The DW/FW ~ in the bulblets was low (less than 10~% on March 30) at the beginning of their development,
5 408 T. OHYAMA, T. IKARASHI, T. MATSUBARA, and A. BABA g C)3 C~ O'~ c'- 5 t" -.~ c".-.- o 20 c S ~ " o o ~ / 0a ~3 ~, m ~ d' :D l/x,> 's c~ -"%.1 I / I month day D a t e Fig. 1. Changes in DW of various parts of tulip plant. I, mother bulb scales; O, bulblets; A, roots; A, basal plate; ~, shoot; ~, leaves; I, stem; O, flower. The DW of the bulblets (dotted line) is indicated by a vertical line on the right hand side. and then increased to 34.5~,o until maturity. This indicates that reserve substrates had accumulated in the bulblets especially after defloration, though the size of the bulblets had been considerably large at the time of flowering. Figure 2 shows the changes in the content of total, insoluble and soluble carbohydrates in the mother bulb scales. At the time of planting the total carbohydrate content was about 2 g/plant accounting for 78~ of the dry matter. Total carbohydrates were constantly consumed during winter and only 44~/o of the reserve carbohydrates remained in the bulb scales at the time of sprouting. The decrease in the total carbohydrate content was accelerated after sprouting, and became constant after April. The major part of the 80}, o ethanol insoluble carbohydrates was represented by starch, though ethanomnsoluble oligofructan accounted for a small portion of less than 1~. The starch content decreased continuously during the first three months, but the decrease almost ended from January 13 to March 9. Then the degradation resumed and the content of starch was almost completely depleted on April 11. On the other hand, the inulin content which increased slightly after planting until December 13, decreased constantly and was depleted at the time of sprouting. The content of soluble Frc and Glc which increased after planting, remained relatively constant until March 9, and then decreased linearly The fluctuations in the content of mono- to tetra-saccharides in the tulip bulb scales are shown in Fig. 3. The Suc content increased markedly after planting, showing maximum values on January 13. It decreased gradually until sprouting and then the
6 Behavior of Carbohydrates in Tulip Bulbs 409 c r v (3. c ~- 0,3 f, u 1 (D t~.2 o -13 s "\ \ o ~ e,,.... ~ x\ o.- " ---o ~ \ o c O, 2 / u m 0 o I~-~-'" ~ month day Date Fig, month day Fig. 3. Fig. 2. Changes in reserve carbohydrate content in mother bulb scales. -- total carbohydrates; --@--, starch (80~ ethanol-insoluble Glc); --O--, inulin (80~ ethanol-insoluble Frc); ~ ethanol-soluble Glc;... O..., 80%0 ethanol-soluble Frc. Fig. 3. Changes in content of sugars in mother bulb scales, x, Glc; 9 Suc; R, G F..: A, GF3; A, GF4. consumption was accelerated toward to anthesis. Frc and Glc were detected in the ethanol extract of bulb scales, and the content increased slowly during winter. The content of the monosaccharides was highest at the time of sprouting and then it declined. On the other hand, the content of GF2, GF3, and GF4 decreased after sprouting, and the content of these carbohydrates was almost completely depleted at the time of flowering (April 27). Figure 4 shows the soluble and insoluble carbohydrate content in the main bulblet. Starch was the predominant reserve carbohydrate. The accumulation started after sprouting, and increased after defloration. Due to the defloration treatment, the bulblets became the main sink of photosynthates. On the other hand, the content of soluble carbohydrates remained relatively constant after May 12. Figures 5 and 6 show the fluctuations in the concentration (Fig. 5) and content (Fig. 6) of the carbohydrate constituents in the bulblets. The Glc and Frc concentration which was initially high on March 30, decreased thereafter (Fig. 5). On the other hand, the Suc concentration increased, reached maximum values on May 12, and decreased thereafter. It is interesting to note that the concentration of fructosylsucrose (GF2-GF4) which was very low at the beginning on March 30, increased and
7 410 T. OHYAMA, T. IKARASHI, T. MATSUBARA, and A. BABA - - it 30 c" LI- U1 O_,,~ 10 0J Un E v c- O 2C,% O t.j c <D ID N 5 k- C- O 2D k. C0 0 r ' mooth 9. - = _" day Date Fig. 4. UD month day Date Fig. 4. Changes in reserve carbohydrate content in bulblet. Fig. 5. Symbols are the same as in Fig. 2. The innermost bulblet was analyzed. Generally only the innermost bulblet becomes a large flowering bulb, whereas some of the other bulblets are small and do not flower in the next season. Fig. 5. Changes in sugar concentration in bulblet. Symbols are the same as in Fig. 3. fluctuated in a pattern similar to that of Suc. As shown in Fig. 6 the Suc content in the bulblets gradually increased before anthesis, and the accumulation of Suc was accelerated showing maximum values on May 26. Thereafter the Suc content decreased9 It is interesting to note that the GF2 content in the bulblets was significantly high, and the fluctuation pattern was very similar to that of Suc. The accumulation of GF 3 and GF4 was slightly delayed compared with that of Suc and GF~. Figure 7 shows the changes in the content ratio of each carbohydrate in which the content of each constituent in the mother bulb scales (a) or bulblet (b) periodically sampled was divided by the corresponding content in the mother bulb at the time of planting (a) or in the mature bulblets (b) at harvest, respectively. The starch content of the mother bulb scales decreased initially among the constituents analyzed. Following starch, inulin and GF4 tended to decrease after the early stage. The content of GF3 remained constant before sprouting and decreased thereafter, whereas the content of Suc and GF2 rose in the early stage, and decreased after sprouting. The content of monosaccharides, Glc and Frc which increased logarithmically until the bolting stage, decreased thereafter. These results suggest that the decomposition of high DP carbohydrates tended to start earlier than that of the low DP saccharides.
8 Behavior of Carbohydrates in Tulip Bulbs 411 0,6 C'c 0,5 rg ~0,4 v 0,3 0 u 0,2 zo,1 U month day Date Fig. 6. Changes in sugar content in bulblet. Symbols are the same as in Fig. 3. Cn g & 10 ~ 0,1 (a) Mother bulb 10 crq "' '", / 1 ~.-...,, 'if, i{! i,il x (b) Bu[blet,~--%/'X Fig. 7. Relative content of carbohydrates in the mother bulb scales and bulblet, x, Glc; 9 Frc; 0, Suc; C], GF.; GF3; A, GF4; II, starch; O, inulin. In the case of the mother bulb, the content of each of the constituents in the planting bulb was represented by 1. On the other hand in the bulblet the content in the harvested bulb on June 13 was represented by 1.
9 412 T. OHYAMA, T. IKARASHI, T. MATSUBARA, and A. BABA Fig. 8. Cut surface of mother bulb scales (a d) and bulblet (e-h) observed by scanning electron microscopy, a, October 26 (planting); b, December 3; c, February 21; d, March 30; e, April
10 Behavior of Carbohydrates in Tulip Bulbs (flowering); f, May 12; g, May 26; h, June 13 (harvest).
11 414 T. OHYAMA, T. IKARASHI, T. MATSUBARA, and A. BABA The accumulation of GF2 during winter indicates that isokestose as well as Suc may be temporary storage carbohydrates before sprouting. The ratio of Suc and GF2 in the bulblet (b) increased initially, followed by GFz, GF~, inulin, and starch, in this sequence. These results suggest that Suc which translocated from the leaves to the bulblets was initially stored in this form or after being converted to low DP fructosylsucroses in the bulblets until the onset of starch synthesis. As maturation proceeded, accumulated Suc and fructosylsucroses were actively converted to starch. Therefore, the fructosylsucroses formed in the bulblets may act as temporary storage sugars for the development to maturity and not as reserve carbohydrates for underground life after planting. Figure 8 shows secondary electron scanning images of the mother bulb scales (a-d) and main bulblet (e-h), respectively. At the time of planting on October 26 (a), the scale cells were filled with two types of granules, one which consisted of large granules, ym in diameter with a thin lenticular shape and the other which consisted of small granules, < 10 ~m in diameter with a spherical shape. Immediately after planting, the small granules disappeared until December 3, whereas the numbers and size of the large granules remained unchanged. After December 3, the starch granules were embedded in a cementing matter (c). Thereafter the number of large granules decreased markedly until March 30 (d). In the case of the bulblet, the small granules were already detected on April 27 (e). They became larger and showing a lenticular shape on and after May 12 (f, g). Just before harvest (h) the small starch granules appeared as shown in the planting bulb (a). This observation suggests that the small granules in the bulblets were synthesized in the late period, just before maturation, and that they were preferentially utilized just after planting in autumn. Comparison of a and h showed that the density of the small granules increased from harvest until planting. Therefore the formation of the small granules continued during the post-harvest storage period. The morphological features of the starch granules in the tulip bulb scales resembled those of the endosperm of barley (KIRIBUCHI and NAKAMURA 1973), in which large lenticular and small spherical granules are observed. In the case of barley the small granules also underwent degradation earlier than the large ones. The authors attributed this fact to the difference in the surface structure of the granules. Further studies on the structure and function of the tulip starch granules should be carried out. Based on the results obtained, the changes in the carbohydrates in tulip bulb scales during development can be summarized as follows. Starch consumption, especially the degradation of the small granules occurred immediately after planting. As in the case of starch, high DP oligofructans were also immediately utilized during the winter season. These high DP fructans in the scales represent long-term storage carbohydrates like starch, though their content is comparatively very low. Most of the starch was converted to mobile sugars especially Suc until sprouting occurred, and these sugars were used for the growth of the roots and for nutrient absorption especially N (OHYAMA et al. 1985b), or accumulated in the bulb scales. In addition, GF2
12 Behavior of Carbohydrates in Tulip Bulbs 415 (isokestose) also may play a role as an intermediate form of carbohydrates between easily metabolized and stored ones as well as Suc. The accumulation of Suc and fructosylsucroses may account for the frost tolerance during winter associated with increasing osmotic pressure. Moreover, the large accumulation of Suc and kestose may be important for the rapid growth of the shoots after sprouting, by providing a large amount of carbon sources for the initial development of the shoots. After defloration, photosynthetically produced carbohydrate is translocated mainly to the bulblets. Suc and low DP fructosylsucroses, especially isokestose, accumulated in the bulblets, where they acted as short-term storage sugars in the bulblets until they were converted to the starch. It may be concluded that low DP fructosylsucroses, especially isokestose are temporary storage sugars present either in the mother bulb scales or bulblet scales. The conversion between Suc and isokestose can easily occur by one step reaction, if the reaction is catalyzed by the sucrose-sucrose 1-fructosyltransferase or 1-fructanohydrase enzyme as shown in Helianthus tuberosus (EDELMAN and JEFFORD 1968; KANDLER and HOPE 1980). REFERENCES AUNG, L.H., TOGNONI, F., and DE HERTOGH, A.A. 1973: Changes in the carbohydrates of tulip bulbs during development. Hortic. Sci., 8, AUNG, L.H., WRIGHT, R.D., and HERTOGH, A.A. 1976: Carbohydrate and dry matter changes in organs of Tulipa gesneriana L. during low temperature treatment. Hortic. Sci., 11, DAVIES, J.N. and KEMPTON, R.J. 1975: Carbohydrate changes in tulip bulbs during storage and forcing. Acta hrortic., 47, EDELIvlAN, J. and JEFFORD, T.G. 1968: The mechanism of fructan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol., 67, HAALAND, E. and W~CKS'rROM, A. 1975: The effect of storage temperature on carbohydrate interconversion in tulip bulbs. Acta Hortic., 47, HAMMER, H. 1969: The trisaccharide fraction of the bulbs of some liliaceous species. Acta Chem. Scand., 23, I(ANDLER, O. and HOPE, H. 1980: Occurrence, metabolism and function of oligosaccharides, bl The Biochemistry of Plants, Vol. 3, p , Academic Press, London, New York KIRIBUCHI, S. and NAKAMURA, M. 1973: Studies on the germination of barley seeds (Part 4). Scanning electron microscopic observation of the endosperm of barley during germination. J. Jpn. Soc. Starch Sci., 20, MOE, R. and WICKSTROM, A. 1973: The effect of storage temperature on shoot growth, flowering, and carbohydrate metabolism in tulip bulbs. Physiol. Plant., 28, MOE, R. and WICKSTROM, A. 1979: Effect of precooling at 5 or --1~ on shoot growth flowering and carbohydrate metabolism in tulip bulbs. Sci. Hortic., 10, OHYAMA, Z., IKARASHI, T., and BABA, A. 1985a: Determination of the structure of oligofructan in the tulip bulb. Soil Sci. Plant Nutr., 31, OHYAMA, T., IKARASHI, T., and BABA, A. 1985b: Nitrogen accumulation in the roots of tulip plants (Tulipa gesneriana). Soil Sci. Plant Nutr., 31, OHYAMA, T., IKARASHI, T., and BABA, A. 1986: Analysis of the reserve carbohydrate in bulb scales of autumn planting bulb plant. Jpn. J. Soil Sci. Plant Nutr., 57,
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