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Determination of subcellular concentrations of soluble carbohydrates in rose petals during opening by nonaqueous fractionation method combined with infiltration–centrifugation method

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Abstract

Petal growth associated with flower opening depends on cell expansion. To understand the role of soluble carbohydrates in petal cell expansion during flower opening, changes in soluble carbohydrate concentrations in vacuole, cytoplasm and apoplast of petal cells during flower opening in rose (Rosa hybrida L.) were investigated. We determined the subcellular distribution of soluble carbohydrates by combining nonaqueous fractionation method and infiltration–centrifugation method. During petal growth, fructose and glucose rapidly accumulated in the vacuole, reaching a maximum when petals almost reflected. Transmission electron microscopy showed that the volume of vacuole and air space drastically increased with petal growth. Carbohydrate concentration was calculated for each compartment of the petal cells and in petals that almost reflected, glucose and fructose concentrations increased to higher than 100 mM in the vacuole. Osmotic pressure increased in apoplast and symplast during flower opening, and this increase was mainly attributed to increases in fructose and glucose concentrations. No large difference in osmotic pressure due to soluble carbohydrates was observed between the apoplast and symplast before flower opening, but total osmotic pressure was much higher in the symplast than in the apoplast, a difference that was partially attributed to inorganic ions. An increase in osmotic pressure due to the continued accumulation of glucose and fructose in the symplast may facilitate water influx into cells, contributing to cell expansion associated with flower opening under conditions where osmotic pressure is higher in the symplast than in the apoplast.

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Abbreviations

DW:

Dry weight

FW:

Fresh weight

NAD-GA3PDH:

NAD-glyceraldehyde-3-phosphate dehydrogenase

References

  • Bieleski RL (1993) Fructan hydrolysis drives petal expansion in the ephemeral daylily flower. Plant Physiol 103:213–219

    CAS  PubMed  Google Scholar 

  • Biran M, Robinson M, Halevy AH (1974) Factors determining petal color of Baccara roses. II. The effect of pigment concentration. J Exp Bot 87:624–631

    Article  Google Scholar 

  • Bird IF, Cornelius MJ, Keys AJ, Whittingham CP (1974) Intracellular site of sucrose synthesis in leaves. Phytochemistry 13:59–64

    Article  CAS  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ, Cleland RE (1983) Solutes in the free space of growing stem tissues. Plant Physiol 72:326–331

    Article  CAS  PubMed  Google Scholar 

  • Cram WJ (1976) Negative feedback regulation of transport in cells. The maintenance of turgor, volume and nutrient supply. In: Lüttge U, Pitman MG (eds) Encyclopedia of plant physiology, N.S., vol 2: transport in plants II, part A. Springer, Berlin, pp 284–316

    Google Scholar 

  • Damon S, Hewitt J, Nieder M, Bennett A (1988) Sink metabolism in tomato fruit. II. Phloem unloading and sugar uptake. Plant Physiol 87:731–736

    Article  CAS  PubMed  Google Scholar 

  • Evans RY, Reid MS (1988) Changes in carbohydrates and osmotic potential during rhythmic expansion of rose petals. J Am Soc Hortic Sci 113:884–888

    CAS  Google Scholar 

  • Faragher JD, Mayak S, Tirosh T, Halevy AH (1984) Cold storage of rose flowers: effects of cold storage and water loss on opening and vase life of ‘Mercedes’ roses. Sci Hortic 24:369–378

    Article  Google Scholar 

  • Gerhardt R, Heldt HW (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in nonaqueous media. Plant Physiol 75:542–547

    Article  PubMed  Google Scholar 

  • Ho LC, Nichols R (1977) Translocation of 14C-sucrose in relation to changes in carbohydrate content in rose corollas cut at different stages of development. Ann Bot 41:227–242

    Google Scholar 

  • Ichimura K, Kohata K, Koketsu M, Yamaguchi Y, Yamaguchi H, Suto K (1997) Identification of methyl glucopyranoside and xylose as soluble sugar constituents in roses (Rosa hybrida L.). Biosci Biotechnol Biochem 61:1734–1735

    Article  CAS  Google Scholar 

  • Ichimura K, Ueyama S, Goto R (1999) Possible roles of soluble carbohydrate constituents in cut rose flowers. J Jpn Soc Hortic Sci 68:534–539

    Article  CAS  Google Scholar 

  • Ichimura K, Kawabata Y, Kishimoto M, Goto R, Yamada K (2003) Shortage of soluble carbohydrates is largely responsible for short vase life of cut Sonia rose flowers. J Jpn Soc Hortic Sci 72:292–298

    Article  CAS  Google Scholar 

  • Kanai R, Edwards GE (1973) Purification of enzymatically isolated mesophyll protoplasts from C3, C4 and crassulacean acid metabolism plants using an aqueous dextran–polyethylene glycol two-phase system. Plant Physiol 52:484–490

    Article  CAS  PubMed  Google Scholar 

  • Kenis JD, Silvents ST, Trippi VS (1985) Nitrogen metabolite and senescence-associated change during growth of carnation flowers. Physiol Plant 65:455–459

    Article  CAS  Google Scholar 

  • Koning RE (1984) The role of plant hormones in the growth of the corolla of Gaillardia grandiflora (Asteraceae) ray flowers. Am J Bot 71:1–8

    Article  CAS  Google Scholar 

  • Kumar N, Srivastava GC, Dixit K, Mahajan A, Pal M (2007) Role of carbohydrates in flower bud opening in rose (Rosa hybrida L.). J Hortic Sci Biotechnol 82:235–242

    CAS  Google Scholar 

  • Leigh RA, Tomos AD (1993) Ion distribution in cereal leaves: pathways and mechanisms. Phil Trans R Soc Lond B 341:75–86

    Article  CAS  Google Scholar 

  • Loewus FA, Dickinson DB (1982) Cyclitols. In: Loewus FA, Tanner W (eds) Encyclopedia of plant physiology, N.S., vol 13A: plant carbohydrates I. Springer, Berlin, pp 193–216

    Google Scholar 

  • MacDougall AJ, Parker R, Selvendran R (1995) Nonaqueous fractionation to assess the ionic composition of the apoplast during fruit ripening. Plant Physiol 108:1679–1689

    CAS  PubMed  Google Scholar 

  • McKenzie MJ, Greer LA, Heyes JA, Hurst PL (2004) Sugar metabolism and compartmentation in asparagus and broccoli during controlled atmosphere storage. Postharv Biol Technol 32:45–56

    Article  CAS  Google Scholar 

  • Meinzer FC, Moore PH (1988) Effect of apoplastic solutes on water potential in elongating sugarcane leaves. Plant Physiol 86:873–879

    Article  PubMed  Google Scholar 

  • Moore BD, Shrkey TD, Seemann JR (1995) Intracellular localization of CA1P and CA1P phosphatase activity in leaves of Phaseolus vulgaris L. Photosynth Res 45:219–224

    Article  CAS  Google Scholar 

  • Ofosu-Anim J, Yamaki S (1994) Sugar content and compartmentation in melon fruit and the restriction of sugar efflux from flesh tissue by ABA. J Jpn Soc Hortic Sci 63:685–692

    Article  CAS  Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1993) Microtuble organization, mesophyll cell morphogenesis, and intercellular space formation in Adiantum capillus veneris leaflets. Protoplasma 172:97–110

    Article  Google Scholar 

  • Patrick JW, Offler CE (1996) Post-sieve element transport of photoassimilates in sink regions. J Exp Bot 47:1165–1177

    CAS  Google Scholar 

  • Riens B, Lohaus G, Heineke D, Heldt HW (1991) Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol 97:227–233

    Article  CAS  PubMed  Google Scholar 

  • Schnabl H, Mayer I (1976) Dark fixation of CO2 by flowers of cut roses. Planta 131:51–55

    Article  CAS  Google Scholar 

  • Speer M, Kaiser WM (1991) Ion relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol 97:990–997

    Article  CAS  PubMed  Google Scholar 

  • Stitt M, Lilley RM, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Method Enzymol 174:518–550

    Article  CAS  Google Scholar 

  • Terasaki S, Sakurai N, Yamamoto R, Wada N, Nevins DJ (2001) Changes in cell wall polysacchrides of kiwifruit and the visco-elastic properties detected by a laser Doppler method. J Jpn Soc Hortic Sci 70:572–580

    Article  CAS  Google Scholar 

  • Thorpe MR, Minchin PEH, Williams JHH, Farrar JF, Tomos AD (1993) Carbon import into developing ovules of Pisum sativum: the role of the water relations of the seed coat. J Exp Bot 262:937–945

    Article  Google Scholar 

  • Tsurusaki K, Matsuda Y, Sakurai N (1997) Distribution of indole-3-acetic acid in the apoplast and symplast of squash (Cucurbita maxima) hypocotyls. Plant Cell Physiol 38:352–356

    CAS  Google Scholar 

  • van Doorn WG, Groenewegen G, van de Pol P, Berkholst EM (1991) Effects of carbohydrate and water status on flower opening of cut Madelon roses. Postharv Biol Technol 1:47–57

    Article  Google Scholar 

  • Vergauwen R, van den Ende W, van Laere A (2000) The role of fructan in flowering of Campanula rapunculoides. J Exp Bot 51:1261–1266

    Article  CAS  PubMed  Google Scholar 

  • Wagner GJ (1979) Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. Plant Physiol 64:88–93

    Article  CAS  PubMed  Google Scholar 

  • Welbaum GE, Meinzer FC (1990) Compartmentation of solutes and water in developing sugarcane stalk tissue. Plant Physiol 93:1147–1153

    Article  CAS  PubMed  Google Scholar 

  • Wermicke W, Günther P, Jung G (1993) Microtubles and cell shaping in the mesophyll of Nigella damascene L. Protoplasma 173:8–12

    Article  Google Scholar 

  • Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191:180–190

    Article  CAS  Google Scholar 

  • Yamada K, Ito M, Oyama T, Nakada M, Mesaka M, Yamaki S (2007) Analysis of sucrose metabolism during petal growth of cut roses. Postharv Biol Technol 43:174–177

    Article  CAS  Google Scholar 

  • Yamada K, Norikoshi R, Suzuki K, Nishijima T, Imanishi H, Ichimura K (2009) Cell division and expansion growth during rose petal development. J Jpn Soc Hortic Sci 78:356–362

    Article  Google Scholar 

  • Yamaki S (1984) Isolation of vacuoles from immatured apple fruit flesh and compartmentation of sugars, organic acids, phenolic compounds and amino acids. Plant Cell Physiol 25:151–166

    CAS  Google Scholar 

  • Yamaki S, Ino M (1992) Alteration of cellular compartmentation and membrane permeability to sugars in immature and mature apple fruit. J Am Soc Hortic Sci 117:951–954

    CAS  Google Scholar 

  • Yamaki S, Ishikawa K (1986) Role of four sorbitol related enzymes and invertase in the seasonal alteration of sugar metabolism in apple tissue. J Am Soc Hortic Sci 111:134–137

    CAS  Google Scholar 

  • Zhang LY, Peng YB, Pelleschi-Travier S, Fan Y, Lu YF, Lu YM, Gao XP, Shen YY, Delrot S, Zhang DP (2004) Evidence for apoplasmic phloem unloading in developing apple fruit. Plant Physiol 135:574–586

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. N. Sakurai (Hiroshima University) for his valuable comments. This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 15380030 to K.I.).

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Author notes

  1. Kunio Yamada

    Present address: Graduate School of Bioagricultural Sciences, Nagoya University, Furoh-cho, Chikusa, Nagoya, Aichi, 464-8601, Japan

Authors and Affiliations

  1. National Institute of Floricultural Science, Fujimoto, Tsukuba, Ibaraki, 305-8519, Japan

    Kunio Yamada & Kazuo Ichimura

  2. School of Agriculture, Tokyo University of Agriculture, Funako, Atsugi, Kanagawa, 243-0034, Japan

    Ryo Norikoshi & Hideo Imanishi

  3. National Institute of Vegetables and Tea Science, Minaminakane, Taketoyo, Aichi, 470-2351, Japan

    Katsumi Suzuki

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  1. Kunio Yamada
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  2. Ryo Norikoshi
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  3. Katsumi Suzuki
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  4. Hideo Imanishi
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  5. Kazuo Ichimura
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Correspondence to Kazuo Ichimura.

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Yamada, K., Norikoshi, R., Suzuki, K. et al. Determination of subcellular concentrations of soluble carbohydrates in rose petals during opening by nonaqueous fractionation method combined with infiltration–centrifugation method. Planta 230, 1115–1127 (2009). https://doi.org/10.1007/s00425-009-1011-6

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  • DOI: https://doi.org/10.1007/s00425-009-1011-6

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