Skip to main content
SpringerLink
Log in

Accumulation of mannitol in the cytoplasm and vacuole during the expansion of sepal cells associated with flower opening in Delphinium × belladonna cv. Bellamosum

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The role of mannitol differs from that of glucose, fructose and sucrose in sepal cell expansion associated with flower opening in Delphinium × belladonna.

Sepals of Delphinium × belladonna are colored and much larger than the petals. To determine whether the role of mannitol in sepal growth associated with flower opening differs from those of ubiquitous metabolic sugars including glucose, fructose and sucrose, we investigated changes in cell number, subcellular concentrations of soluble carbohydrates, and osmotic potential in sepals during flower opening in Delphinium × belladonna cv. Bellamosum. The number of epidermal cells in the sepals did not increase from the stage when sepal pigmentation started, whereas the cell area increased during flower opening, indicating that petal growth during flower opening depends on cell expansion. Mannitol concentrations in the vacuole at three different stages were approximately 100 mM, which were much higher than the other carbohydrate concentrations, but they decreased slightly at open stage. In contrast, mannitol concentration in the cytoplasm was 56 mM at bud stage, but it increased to 104 mM at open stage. Glucose and fructose concentrations in the vacuole at open stage increased to 45 and 56 mM, respectively. Total osmotic potential in apoplast and symplast, which was partially due to soluble carbohydrates, was almost constant during flower opening. Therefore, mannitol may be acting constitutively as the main osmoticum in the vacuole where it may contribute to the maintenance of the osmotic balance between the cytoplasm and vacuole in open flowers. The role of mannitol differs from those of glucose, fructose, and sucrose in sepal cell expansion in Delphinium × belladonna.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

DW:

Dry weight

FW:

Fresh weight

HPLC:

High-performance liquid chromatography

References

  • Beauzamy L, Nakayama N, Boudaoud A (2014) Flowers under pressure: ins and outs of turgor regulation in development. Ann Bot 114:1517–1533

    Article  PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bieleski RL, Elgar HJ, Heyes JA (2000) Mechanical aspects of rapid flower opening in Asiatic lily. Ann Bot 86:1175–1183

    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 

  • Boyer JS, Cavalieri AJ, Schulze E-D (1985) Control of the rate of cell enlargement: excision, wall relaxation, and growth-induced water potentials. Planta 163:527–543

    Article  CAS  PubMed  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  PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH (1994) Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiol 106:281–292

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fellman JK, Loescher WH (1987) Comparative studies of sucrose and mannitol utilization in celery (Apium graveolens). Physiol Plant 69:337–341

    Article  CAS  Google Scholar 

  • Hanaichi T, Sato T, Iwamoto T, Malavasi-Yamashiro J, Hoshino M, Mizuno N (1986) A stable lead by modification of Sato’s method. J Electron Microsc 35:304–306

    CAS  Google Scholar 

  • Harada T, Torii Y, Morita S, Masumura T, Satoh S (2010) Differential expression of genes identified by suppression subtractive hybridization in petals of opening carnation. J Exp Bot 61:2345–2354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ichimura K, Kohata K, Koketsu M, Shimamura M, Ito A (1998) Identification of pinitol as a main sugar constituent and changes in its content during flower bud development in carnation (Dianthus caryophyllus L.). J Plant Physiol 152:363–367

    Article  CAS  Google Scholar 

  • Ichimura K, Kohata K, Goto R (2000a) Soluble carbohydrates in Delphinium and their influence on sepal abscission in cut flowers. Physiol Plant 108:307–313

    Article  CAS  Google Scholar 

  • Ichimura K, Kohata K, Yamaguchi Y, Douzono M, Ikeda H, Koketsu M (2000b) Identification of l-inositol and scyllytol and their distribution in various organs in chrysanthemum. Biosci Biotechnol Biochem 64:865–868

    Article  CAS  PubMed  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 Hort Sci 72:292–298

    Article  CAS  Google Scholar 

  • Keller F, Matile P (1989) Storage of sugars and mannitol in petioles of celery leaves. New Phytol 113:291–299

    Article  CAS  Google Scholar 

  • Keller M, Shrestha PM (2014) Solute accumulation differs in the vacuoles and apoplast of ripening grape berries. Planta 239:633–642

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi K, Kanahama K, Kanayama Y (2003) Changes in sugar-related enzymes during wilting of cut delphinium flowers. J Jpn Soc Hort Sci 72:37–42

    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 

  • Kornberg A, Horecker BL (1955) Glucose-6-phosphate dehydrogenase. Methods Enzymol 1:323–325

    Article  CAS  Google Scholar 

  • Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiol Plant 70:553–557

    Article  CAS  Google Scholar 

  • Moore BD, Palmquist DE, Seemann JR (1997) Influence of plant growth at high CO2 concentrations on leaf content of ribulose-1,5-bisphosphate carboxylase/oxygenase and intracellular distribution of soluble carbohydrates in tobacco, snapdragon, and parsley. Plant Physiol 115:241–248

    PubMed Central  CAS  PubMed  Google Scholar 

  • Norikoshi R, Imanishi H, Ichimura K (2013) Changes in cell number, osmotic potential and concentrations of carbohydrates and inorganic ions in Tweedia caerulea during flower opening. J Jpn Soc Hort Sci 82:51–56

    Article  CAS  Google Scholar 

  • Paul MJ, Cockborn W (1989) Pinitol, a compatible solute in Mesembryanthemum crystallinum L.? J Exp Bot 40:1093–1098

    Article  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  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stoop JMH, Pharr DM (1994) Mannitol metabolism in celery stressed by excess macronutrients. Plant Physiol 106:503–511

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tattini M, Gucci R, Romani A, Baldi A, Everard JD (1996) Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress. Physiol Plant 98:117–124

    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 Hort 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

    Article  CAS  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  PubMed Central  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamada K, Norikoshi R, Suzuki K, Imanishi H, Ichimura K (2009a) 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 Hort Sci 117:951–954

    CAS  Google Scholar 

  • Yamane K, Kawabata S, Sakiyama R (1991) Changes in water relations, carbohydrate contents, and acid invertase activity associated with perianth elongation during anthesis of cut gladiolus flowers. J Jpn Soc Hort Sci 60:421–428

    Article  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  PubMed Central  CAS  PubMed  Google Scholar 

  • Zimmermann MH (1960) Transport in the phloem. Annu Rev Plant Physiol 11:167–190

    Article  Google Scholar 

Download references

Acknowledgments

We thank Ms. R. Mori for her technical assistance. 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 KI).

Author information

Author notes

  1. Ryo Norikoshi

    Present address: School of Agriculture, Tokyo University of Agriculture, Funako, Atsugi, Kanagawa, 243-0034, Japan

  2. Kunio Yamada

    Present address: Chubu University, Matsumoto-cho, Kasugai, Aichi, 487-8501, Japan

Authors and Affiliations

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

    Ryo Norikoshi, Kunio Yamada, Tomoko Niki & Kazuo Ichimura

Authors
  1. Ryo Norikoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kunio Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomoko Niki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuo Ichimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazuo Ichimura.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2015_2385_MOESM1_ESM.pdf

Supplementary material 1 (PDF 7985 kb). Scanning electron micrographs of adaxial and abaxial epidermal cells in the sepals during flower opening. Adaxial epidermal cells at stage 1 (a), stage 2 (b) and stage 3 (c). Abaxial epidermal cells at stage 1 (d), stage 2 (e) and stage 3 (f). The scale bars represent 50 μm

Supplementary material 2 (DOCX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Norikoshi, R., Yamada, K., Niki, T. et al. Accumulation of mannitol in the cytoplasm and vacuole during the expansion of sepal cells associated with flower opening in Delphinium × belladonna cv. Bellamosum. Planta 242, 1467–1477 (2015). https://doi.org/10.1007/s00425-015-2385-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2385-2

Keywords

Search

Navigation