Diversity of the Composition and Content of Soluble Carbohydrates in Seeds of the Genus Vicia (Leguminosae)

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Diversity of the Composition and Content of Soluble Carbohydrates in Seeds of the Genus Vicia (Leguminosae) Genet Resour Crop Evol (2018) 65:541–554 https://doi.org/10.1007/s10722-017-0552-y RESEARCH ARTICLE Diversity of the composition and content of soluble carbohydrates in seeds of the genus Vicia (Leguminosae) Lesław Bernard Lahuta . Monika Ciak . Wojciech Rybin´ski . Jan Bocianowski . Andreas Bo¨rner Received: 15 March 2017 / Accepted: 14 August 2017 / Published online: 30 August 2017 Ó The Author(s) 2017. This article is an open access publication Abstract Low molecular weight carbohydrates of and its a-D-galactosides—in V. articulata, V. monantha seeds of 10 species of Vicia, namely: V. angustifolia, and V. pannonica or D-ononitol and its galactoside—in V. articulata, V. cordata, V. ervilia, V. johannis, V. V. ervilia). Among the species containing in seeds RFOs macrocarpa, V. monantha, V. narbonensis, V. pan- as the main a-D-galactosides (V. angustifolia, V. nonica and V. sativa were analyzed by the high cordata, V. johanensis, V. macrocarpa, V. narbonensis resolution gas chromatography method. Seeds of the and V. sativa), an additional subgroup can be separated, investigated species contain common (glucose, fruc- which contains a set of unknown compounds (found in tose, myo-inositol, sucrose, galactinol, di-galactosyl V. angustifolia, V. cordata and V. macrocarpa). More- myo-inositol and raffinose family oligosaccharides— over, several other unidentified carbohydrate-containing RFOs) and species-specific carbohydrates (D-pinitol compounds were detected exclusively in seeds of V. ervilia. The concentrations of total soluble carbohy- drates (TSCs), including sugars, RFOs, cyclitols and Electronic supplementary material The online version of galactosyl cyclitols and unknown compounds, in seeds this article (doi:10.1007/s10722-017-0552-y) contains supple- mentary material, which is available to authorized users. differ significantly (P \ 0.05) among the species. RFOs and sucrose are the main fractions in TSCs, with the L. B. Lahuta (&) Á M. Ciak exception of V. pannonica seeds, containing more Department of Plant Physiology, Genetics and galactosyl pinitols, and V. ervilia, in which unknown Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego Street 1A/103, 10-719 Olsztyn, compounds account for 50% of TSCs. In V. ervilia -1 Poland RFOs occur at the lowest concentration (9.32 mg g e-mail: [email protected] seeds), and the concentration of DGMI (di-galactosyl myo-inositol) is comparable with that of RFOs, which is W. Rybin´ski Department of Genomics, Institute of Plant Genetics unusual among all the investigated Vicia species. Polish Academy of Science, Strzeszyn´ska 34, 60-101 Poznan, Poland Keywords Vicia Á Seeds Á Chemotaxonomy Á Carbohydrate Á Raffinose oligosaccharides Á Pinitol J. Bocianowski Department of Mathematical and Statistical Methods, Poznan´ University of Life Sciences, Wojska Polskiego 28, 60-637 Poznan, Poland Introduction A. Bo¨rner Leibniz Institute of Plant Genetics and Crop Plant The genus Vicia L. comprises about 160 annual and Research, 06466 Gatersleben, Germany perennial species, which are distributed in Europe, 123 542 Genet Resour Crop Evol (2018) 65:541–554 Asia, Americas and tropical East Africa (Schaefer that of RFOs (up to 12%, in lupin, Gulewicz et al. et al. 2012). A few important annual species, such as V. 2014). Galactosyl pinitols (ciceritol and galactopinitol narbonensis L. (narbon vetch), V. sativa L. subsp. A) predominate among GalCs (Obendorf et al. 2012). sativa (common vetch), V. ervilia (L.) Willd. (bitter Infrageneric variation of RFOs and GalCs in seeds vetch) and V. villosa Roth subsp. dasycarpa (hairy- of Vicia genus was characterized by Yasui et al. pod vetch) are grown for livestock feed in non-tropical (1987). In the chemotaxonomic studies, these authors dry areas. The grains of these vetches can be used as analyzed 29 species, including 19 accessions of less costly sources of proteins and energy for rumi- common vetch and 3 accessions of narbon vetch. In nants and non-ruminants. However, seeds of some the seeds of the two latter species, RFOs are the only Vicia species contain also toxins and antinutritional a-D-galactosides, and verbascose was the predominant compounds, restricting their use as food and feed oligosaccharide (1.2–2.0% of dry mass). Verbascose is (Enneking and Wink 2000). Moreover, the presence of also a major oligosaccharide in bitter vetch (Muzquiz raffinose family oligosaccharides (RFOs: including et al. 2012). Seeds of few other Vicia species raffinose, stachyose, verbascose, ajugose), ubiquitous accumulate considerable amounts of D-pinitol and its for seeds of all legumes (Obendorf and Go´recki 2012), galactosides (Yasui et al. 1987; Lahuta et al. 2005a). is an additional factor decreasing the use of vetch The higher concentration of galactosyl pinitols than seeds by monogastric animals and humans. RFOs are RFOs in seeds is a unique feature and has been found a-D-galactosides of sucrose, containing 1–4 units of only in the subgenus Cracca, in seeds of V. villosa galactose linked by a-1,6 linkages. They are not Roth, V. cracca L. (Yasui et al. 1987; Lahuta et al. digested in the upper part of the gastrointestinal tract, 2005a; Lahuta 2006) and V. tenuifolia Roth (Lahuta due to the absence of endogenous a-D-galactosidase, et al. 2010a). The characterization of low molecular and are therefore available for bacterial fermentation weight carbohydrates in seeds of legumes from in the colon, causing flatulence and digestive discom- different taxa allowed Yasui and Ohashi (1990)to fort (Martı´nez-Villaluenga et al. 2008). In seeds of conclude that the accumulation of RFOs is a primary some legumes, including several Vicia species, beside evolutionary attribute of legumes, whereas the syn- RFOs, a-D-galactosides of cyclitols (galactosyl cycli- thesis of myo-inositol methyl derivatives: D-ononitol, tols, GalCs) are present (Yasui and Ohashi 1990), D-pinitol and D-bornesitol and their a-D-galactosides, whose flatulent potential seems to be lower than RFOs. is a secondary trait. The confirmation of this hypoth- The physiological effects of GalCs are not known. esis can be found in catalytic properties of enzymes However, cyclitols (myo-inositol, D-chiro-inositol, D- engaged in RFOs biosynthetic pathway and the lack of pinitol), released during GalCs hydrolysis in the identification of enzymes responsible exclusively for digestive tract, indicate some health benefit properties the synthesis of galactosyl cyclitols (Peterbauer et al. (insulin-mimetic, antioxidative, anti-inflammatory 2003). The biosynthetic pathway of RFOs is deter- and anticancer activity) and can be used as diet mined by the activity of galactinol synthase (GolS), supplements with therapeutic properties (Croze and catalyzing the synthesis of galactinol from UDP- Soulage 2013). Thus, legume seeds can be used not galactose and myo-inositol. Galactinol is the main only as foodstuff, but also as a source of health- galactosyl donor for the synthesis of raffinose, promoting cyclitols. stachyose and verbascose (Peterbauer and Richter The content and composition of a-D-galactosides in 2001). Raffinose synthase (RS), transferring the seeds was characterized in detail in major legume galactosyl moiety from galactinol to sucrose (produc- crops: soybean (Glycine max [L.] Merr.), pea (Pisum ing raffinose), and stachyose synthase (STS), trans- sativum L.), bean (Phaseolus vulgaris L.), lentil (Lens ferring the galactosyl moiety from galactinol to culinaris L.) and chickpea (Cicer arietinum L.). The raffinose and stachyose (producing stachyose and concentration of RFOs is within the range of 2–12% of verbascose, respectively), indicate multifunctional dry matter and stachyose or verbascose are the properties. They are able to transfer galactose to D- prevalent oligosaccharides in seeds (Guillon and pinitol/D-ononitol and their galactosides (Peterbauer Champ 2002). The concentration of GalCs occurring et al. 2002a, b). Moreover, STS from pea indicates an in seeds of lentil, chickpea, soybean and lupin ability to catalyze the synthesis of verbascose from (Lupinus L.) is lower (up to 3–4%, in chickpea) than two molecules of stachyose (Peterbauer et al. 2003). 123 Genet Resour Crop Evol (2018) 65:541–554 543 The indirect confirmation of the synthesis of both establishment of the taxonomy of species of the genus RFOs and galactosyl pinitols by the same set of Vicia. enzymes was found in developing Vicia villosa seeds (Lahuta 2006). The profiles of enzyme activity and the accumulation of RFOs and galactosyl pinitols were Materials and methods very consistent. Additionally, in seeds of Vicia species naturally accumulating only myo-inositol and RFOs, Material and not D-pinitol/galactosyl pinitols, the activity directed towards the synthesis of ciceritol and tri- Seeds of 10 Vicia species were derived from Gene galactosyl pinitol A was found (Lahuta et al. 2010b). Bank in Gatersleben (Germany), whereas 17 cultivars The accumulation of higher amounts of galactosyl and breeding lines of Vicia sativa L. were derived pinitols in seeds may depend on D-pinitol (1D-3-O- from a collection of the Institute of Plant Genetics in methyl-chiro-inositol) at sufficiently high concentra- Poznan´ (Poland). The investigated Vicia species tions (Lahuta et al. 2005a, b, c, 2010a). This cyclitol is belong to subgenus Vicia, Cracca and Ervum. Seven synthesized from myo-inositol by myo-inositol methyl species from the sections: Vicia (V. angustifolia L., V. transferase (IMT), catalyzing the synthesis of D- cordata Wulfen ex Hoppe, V. macrocarpa
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