Skip to main content
Log in

Cyclitols affect accumulation of α-d-galactosides in developing Vicia seeds

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The mechanism preferentially regulating accumulation of raffinose family oligosaccharides (RFOs) or galactosyl cyclitols in legume seeds still remains unknown. The broad range of raffinose family oligosaccharides and galactosyl pinitols in the composition of seeds of Vicia genus gives researchers an exceptional opportunity for investigations on relationships in biosynthesis of both types of α-d-galactosides. Feeding explants of Vicia species radically different in the composition of RFOs and galactosyl pinitols with basic galactose acceptors, sucrose (for RFOs) or cyclitols (for galactosyl cyclitols) can be a helpful method for assessment of their regulatory role in accumulation of α-d-galactosides in seeds. Garden vetch (Vicia sativa L.) seeds, naturally accumulating RFOs, demonstrated an ability to take up and use exogenously applied d-pinitol and d-chiro-inositol for synthesis of their mono-, di- and tri-galactosides. Together with the accumulation of new galactosides, the concentration of RFOs decreased. In fine-leaved (Vicia tenuifolia Roth.) vetch seeds such a remarkably high concentration of galactosyl pinitols (GPs) was discovered that they nearly replaced RFOs, which is unique among legumes. If the accumulation of both types of galactosides is correlated with concentration of galactose acceptors, elevated levels of sucrose or myo-inositol should promote accumulation of RFOs, instead of GPs. Unexpectedly, feeding fine-leaved vetch raceme explants with myo-inositol or sucrose promoted accumulation of GPs, but not of RFOs. Our comparison of accumulation and biosynthesis of both types of galactosides (RFOs and GPs) throughout development and maturation of seeds from fine-leaved vetch has indicated that preferential accumulation of GPs is associated with the drying of seeds during maturation. Different patterns in activities of enzymes engaged in RFOs’ biosynthetic pathway and galactosyltransferases involved in biosynthesis of GPs indicated that distinct forms of enzymes can operate in both pathways. The feeding of explants with d-chiro-inositol causes accumulation of fagopyritols B1 in seeds of both Vicia species, which suggests presence of the same or a similar form of galactinol synthase. Accumulation of fagopyritols in fine-leaved vetch seeds did not affect accumulation of RFOs or galactosyl pinitols.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

RFOs:

Raffinose family oligosaccharides

GPs:

α-d-Galactosides of d-pinitol

Fag B1:

Galactosyl d-chiro-inositol (fagopyritol B1)

Fag B2:

Di-galactosyl d-chiro-inositol (fagopyritol B2)

GPA:

Galactosyl pinitol A

GPB:

Galactosyl pinitol B

DGPA:

Di-galactosyl pinitol A (ciceritol)

TGPA:

Tri-galactosyl pinitol A

tetraGPA:

Tetra-galactosyl pinitol A

GolS:

Galactinol synthase

RS:

Raffinose synthase

STS:

Stachyose synthase

VS:

Verbascose synthase

GPAS:

GPA synthase

CICS:

Ciceritol synthase

TGPAS:

TGPA synthase

DAP:

Day after pollination

FW:

Fresh weight

DW:

Dry weight

References

  • Chiera JM, Streeter JG, Finer JJ (2006) Ononitol and pinitol production in transgenic soybean containing the inositol methyl transferase gene from Mesembryanthemum crystallinum. Plant Sci 171:647–654

    Article  CAS  Google Scholar 

  • Frias J, Bakhsh A, Jones DA, Arthur AE, Vidal-Valverde C, Rhodes MJC, Hedley CL (1999) Genetic analysis of the raffinose oligosaccharide pathway in lentil seeds. J Exp Bot 50:469–476

    Article  CAS  Google Scholar 

  • Gomes CI, Obendorf RL, Horbowicz M (2005) myo-Inositol, d-chiro-inositol, and d-pinitol synthesis, transport, and galactoside formation in soybean explants. Crop Sci 45(2):1312–1319

    Article  CAS  Google Scholar 

  • Górecki RJ, Piotrowicz-Cieślak AI, Lahuta LB, Obendorf RL (1997) Soluble carbohydrates in desiccation tolerance of yellow lupin seeds during maturation and germination. Seed Sci Res 7:107–115

    Google Scholar 

  • Haab CI, Keller F (2002) Purification and characterization of the raffinose oligosaccharide chain elongation enzyme, galactan:galactan galactosyltransferase (GGT), from Ajuga reptans leaves. Physiol Plant 114:361–371

    Article  CAS  PubMed  Google Scholar 

  • Hoch G, Peterbauer T, Richter A (1999) Purification and characterization of stachyose synthase from lentil (Lens culinaris) seeds: galactopinitol and stachyose synthesis. Arch Biochem Biophys 366(1):75–81

    Article  CAS  PubMed  Google Scholar 

  • Horbowicz M, Obendorf RL, McKersie BD, Viands DR (1995) Soluble saccharides and cyclitols in alfalfa (Medicago sativa L.) somatic embryos, leaflets, and mature seeds. Plant Sci 109:191–198

    Article  CAS  Google Scholar 

  • Horbowicz M, Brenac P, Obendorf RL (1998) Fagopyritol B1, O-α-d-galactopyranosyl-(1-2)-d-chiro-inositol, a galactosyl cyclitol in maturing buckwheat seeds associated with desiccation tolerance. Planta 205:1–11

    Article  CAS  PubMed  Google Scholar 

  • Jaaska V (2005) Isozyme variation and phylogenetic relationships in Vicia subgenus Cracca (Fabaceae). Ann Bot 96:1085–1096

    Article  CAS  PubMed  Google Scholar 

  • Lahuta LB (2006) Biosynthesis of raffinose family oligosaccharides and galactosyl pinitols in developing and maturing seeds of winter vetch (Vicia villosa Roth.). Acta Soc Bot Pol 75(3):219–227

    CAS  Google Scholar 

  • Lahuta LB, Górecki RJ, Hołdyński C, Horbowicz M (2001) The seeds of genus Vicia (Leguminosae) as an object for study on metabolism of raffinose series of oligosaccharides and galactosyl cyclitols. In: AEP (ed) 4th European Conference on Grain Legumes, Cracow, Poland. pp 366–367

  • Lahuta LB, Horbowicz M, Gojło E, Goszczyńska J, Górecki RJ (2005a) Exogenously applied d-pinitol and d-chiro-inositol modifies the accumulation of α-d-D-galactosides in developing tiny vetch (Vicia hirsuta [L.] S.F. Gray) seeds. Acta Soc Bot Pol 74(4):287–296

  • Lahuta LB, Górecki RJ, Gojło E, Horbowicz M (2005b) Differences in accumulation of soluble α-d-galactosides during seed maturation of several Vicia species. Acta Physiol Plant 27(2):163–171

    Article  CAS  Google Scholar 

  • Lahuta LB, Górecki RJ, Horbowicz M (2005b) High concentrations of d-pinitol or d-chiro-inositol inhibit the biosynthesis of raffinose family oligosaccharides in maturing smooth tare (Vicia tetrasperma [L.] Schreb.) seeds. Acta Physiol Plant 27(4A):505–513

    Google Scholar 

  • Ma JM, Horbowicz M, Obendorf RL (2005) Cyclitols galactosides in embryos of buckwheat stem-leaf-seed explants fed d-chiro-inositol, myo-inositol or d-pinitol. Seed Sci Res 15:329–338

    Article  CAS  Google Scholar 

  • Obendorf RL (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Sci Res 7:63–74

    Article  CAS  Google Scholar 

  • Obendorf RL, Horbowicz M, Dickerman AM, Brenac P, Smith ME (1998) Soluble oligosaccharides and galactosyl cyclitols in maturing soybean seeds in planta and in vitro. Crop Sci 38:78–84

    Article  CAS  Google Scholar 

  • Obendorf RL, Odorcic S, Ueda T, Coseo MP, Vasallo E (2004) Soybean galactinol synthase forms fagopyritol B1 but not galactosyl pinitols: substrate feeding of isolated embryos and heterologous expression. Seed Sci Res 14:321–333

    Article  CAS  Google Scholar 

  • Obendorf RL, McInnis CE, Horbowicz M, Keresztes I, Lahuta LB (2005) Molecular structure of lathyritol, a galactosyl bornesitol from Lathyrus odoratus seeds by NMR. Carbohydr Res 340:1441–1446

    Article  CAS  PubMed  Google Scholar 

  • Obendorf RL, Zimmerman AD, Zhang Q, Castillo A, Kosina SM, Bryant EG, Sensenig EM, Wu J, Schnebly SR (2009) Accumulation of soluble carbohydrates during seed development and maturation of low-raffinose, low-stachyose soybean. Crop Sci 49:329–341

    Article  CAS  Google Scholar 

  • Peterbauer T, Richter A (1998) Galactosyl ononitol and stachyose synthesis in seeds of adzuki bean. Purification and characterization of stachyose synthase. Plant Physiol 117:165–172

    Article  CAS  PubMed  Google Scholar 

  • Peterbauer T, Richter A (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Sci Res 11:185–197

    CAS  Google Scholar 

  • Peterbauer T, Lahuta LB, Blöchl A, Mucha J, Jones DA, Hedley CL, Górecki RJ, Richter A (2001) Analysis of the raffinose family oligosaccharide pathway in pea seeds with contrasting carbohydrate composition. Plant Physiol 127:1764–1772

    Article  CAS  PubMed  Google Scholar 

  • Peterbauer T, Mucha J, Mach L, Richter A (2002a) Chain elongation of raffinose in pea seeds. Isolation, characterization, and molecular cloning of a multifunctional enzyme catalyzing the synthesis of stachyose and verbascose. J Biol Chem 277:194–200

    Article  CAS  PubMed  Google Scholar 

  • Peterbauer T, Mach L, Mucha J, Richter A (2002b) Functional expression of a cDNA encoding pea (Pisum sativum L.) raffinose synthase, partial purification of the enzyme from maturing seeds and steady-state kinetic analysis of raffinose synthesis. Planta 215:839–846

    Article  CAS  PubMed  Google Scholar 

  • Peterbauer T, Brereton I, Richter A (2003a) Identification of a digalactosyl ononitol from seeds of adzuki bean (Vigna angularis). Carbohydr Res 338:2017–2019

    Article  CAS  PubMed  Google Scholar 

  • Peterbauer T, Karner U, Mucha J, Mach L, Jones DA, Hedley CL, Richter A (2003b) Enzymatic control of the accumulation of verbascose in pea seeds. Plant Cell Environ 26:1385–1391

    Article  CAS  Google Scholar 

  • Quemener B, Brillouet JM (1983) Ciceritol, a pinitol digalactoside from seeds of chickpea, lentil and white lupin. Phytochemistry 22:1745–1751

    Article  CAS  Google Scholar 

  • Schweizer TF, Horman I (1981) Purification and structure determination of three α-d-galactopyranosylcyclitols from soya beans. Carbohydrate Res 95:61–71

    Article  CAS  Google Scholar 

  • Szczeciński P, Gryff-Keller A, Horbowicz M, Lahuta LB (2000) Galactosylpinitols isolated from vetch (Vicia villosa Roth.) seeds. J Agric Food Chem 48:2717–2720

    Article  PubMed  CAS  Google Scholar 

  • Tapernoux-Lüthi EM, Böhm A, Keller F (2004) Cloning, functional expression, and characterization of the raffinose oligosaccharide chain elongation enzyme, galactan:galactan galactosyltransferase, from common bugle leaves. Plant Physiol 134:1377–1387

    Article  PubMed  CAS  Google Scholar 

  • Ueda T, Coseo MP, Harrell TJ, Obendorf RL (2005) A multifunctional galactinol synthase catalyzes the synthesis of fagopyritol A1 and fagopyritol B1 in buckwheat seed. Plant Sci 168:681–690

    Article  CAS  Google Scholar 

  • Wanek W, Richter A (1995) Purification and characterization of myo-inositol 6-O-methyltransferase from Vigna umbellata Ohwi et Ohashi. Planta 197:427–434

    Article  CAS  Google Scholar 

  • Yasui T, Endo Y, Ohashi H (1987) Infrageneric variation of the low molecular weight carbohydrate composition of the seeds of genus Vicia (Leguminosae). Bot Mag Tokyo 100:255–272

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by grant No N30312532/4015 obtained from Ministry of Science and Higher Education of Poland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lesław B. Lahuta.

Additional information

Communicated by F. Corbineau.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lahuta, L.B., Goszczyńska, J., Horbowicz, M. et al. Cyclitols affect accumulation of α-d-galactosides in developing Vicia seeds. Acta Physiol Plant 32, 933–942 (2010). https://doi.org/10.1007/s11738-010-0481-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-010-0481-2

Keywords

Navigation