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Comparison of Post-Germination Mobilization of Cell Wall

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Comparison of Post-Germination Mobilization of Cell Wall Short Communication Received: 13 December 2008 Revised: 22 April 2009 Accepted: 30 April 2009 Published online in Wiley Interscience: 23 June 2009 (www.interscience.wiley.com) DOI 10.1002/jsfa.3665 Comparison of post-germination mobilization of cell wall polysaccharides and non-cell wall carbohydrates in soybean (Glycine max L.) cotyledons John W Gronwald,a,b∗ Hans-Joachim G Jung,a,b Lynn A Littererb† and David A Somersb‡ Abstract BACKGROUND: In previous research, we demonstrated that cell wall polysaccharide (CWP) levels of soybean (Glycine max L.) cotyledons are negatively correlated with the sum of seed oil and protein content. Although the results suggest that reducing cotyledon CWP levels would be desirable, it is not known whether CWP are mobilized during early seedling growth and, if so, to what extent mobilization contributes to seed reserves. RESULTS: Ungerminated (dry) seeds contained equivalent amounts [approximately 20 mg (cotyledon pair)−1] of non-cell wall carbohydrates (NCWC) and CWP. Galactose and arabinose accounted for 47% of total CWP in cotyledons of dry seeds. Measured 14 days after planting (DAP), the levels of NCWC and CWP were reduced 98% and 34%, respectively, in cotyledons of seedlings grown under a 16-h photoperiod. Measured 14 DAP, greater than 85% of cotyledon cell wall galactose plus arabinose was mobilized. The transformation of the cotyledon to a photosynthetic organ was associated with restructuring of the cell wall involving increases in uronic acids, glucose and rhamnose. CONCLUSION: CWP of soybean cotyledons are modified during early seedling growth due to mobilization and cell wall restructuring triggered by light. The amount of carbon mobilized makes only a small contribution to total cotyledon reserves. Published 2009 by John Wiley & Sons, Ltd. Keywords: cell wall; cotyledon; galactose; Glycine max; pectin; soybean INTRODUCTION roles of the high-pectin cell walls of soybean cotyledons have The cotyledons of soybean (Glycinemax L.) seeds contain relatively not been defined. In the case of lupin (Lupin angustifolius L.), high levels of cell wall polysaccharides (CWP); approximately another legume with epigeal cotyledons, CWP, primarily β(1 → 4) 12% on a dry weight basis.1,2 The typical primary cell wall of galactans attached to RG-I, are mobilized during early seedling dicots consists of approximately 35% pectin, 30% cellulose and growth.10–15 The galactose mobilized from the cotyledon cell wall 30% hemicellulose on a dry weight basis.3 In contrast, soybean is considered to be a carbon reserve that contributes to early cotyledon cell walls contain approximately 76% pectin, and 24% seedling growth. cellulose plus hemicellulose on a dry weight basis.2 A major pectic The epigeal cotyledons of soybean have dual functions, serving polysaccharide in soybean cotyledons is rhamnogalacturonan as reserve storage and photosynthetic organs.16–18 The patterns (RG-I) which has galactose and arabinose homo- and hetero- of protein, lipid and oligosaccharide mobilization have been polymer side chains attached to the rhamnose residues.4–7 The predominant side chain is β(1 → 4) galactan with a chain length 7 of 43 to 47 residues. ∗ Correspondence to: John W Gronwald, USDA-ARS, Plant Science Research Unit, Recent research has shown that the amount of CWP in soybean St Paul, MN 55108, USA. E-mail: [email protected] seeds is negatively correlated with total seed oil and protein content.2,8,9 It was postulated that synthesis of CWP in developing † Current address: Promega Corp., 2800 Woods Hollow Rd., Madison, WI 53711, USA. cotyledons diverts carbon from protein and oil deposition, and that reducing CWP levels in soybean cotyledons may increase ‡ Current address: Monsanto Company, Agracetus Campus, Middleton, WI seed oil and/or protein.2,8,9 Assuming that diverting carbon from 53562, USA. CWP synthesis during cotyledon development would increase seed oil and/or protein, it is not clear whether reduced CWP would a USDA-ARS, Plant Science Research Unit, St Paul, MN 55108, USA adversely effect seed quality or early seedling growth. Other than b Department of Agronomy and Plant Genetics, University of Minnesota, St Paul, 1981 serving a compartmentation function, the structural/functional MN 55108, USA J Sci Food Agric 2009; 89: 1981–1986 www.soci.org This article is a US Government work and is in the public domain in the USA www.soci.org JW Gronwald et al. characterized in cotyledons of soybean seed during germination Pectin was estimated as the sum of arabinose, fucose, galactose, and early seedling growth.17,19–21 However, it is not known rhamnose and uronic acids based on previous reports of soybean whether structural carbon in the high-pectin cell walls of soybean pectin composition.2,8,9 cotyledons is mobilized during early seedling growth and, if so, to what extent it contributes to total carbon reserves. The objectives of this research were to: (1) characterize CWP Statistical analysis in cotyledons of soybean seedlings germinated under a 16-h Carbohydrate analyses were conducted in duplicate on each photoperiod compared to continuous darkness where seedlings sample, with each sample consisting of 20 cotyledon pairs. Data remain heterotrophic; and (2) compare changes in CWP with were statistically analyzed using a completely randomized design 27 patterns of mobilization of non-cell wall carbohydrates (NCWC) with 15 treatments. The treatments consisted of ungerminated (sucrose, raffinose, stachyose, starch). (dry) cotyledons and cotyledons collected at seven time intervals post-planting, grown under either light or dark conditions. Each treatment was replicated three times as described above. For those MATERIALS AND METHODS cotyledon traits where a significant (P < 0.05) analysis of variance Plant material result was observed, the F-protected least significant difference Soybean [Glycine max (L.) Merr. cv. Lambert] seed were planted [10 methodwasusedtocomparetreatmentmeans.Comparisonswere seeds (pot)−1]inpots[16cm(width)×15 cm (height)] containing Metro-mix200(SunGroHorticulture,Bellevue,WA,USA).Seedlings were grown in a growth chamber under a 16-h photoperiod or in continuous darkness. For growth under the 16-h photoperiod, ◦ day/night temperatures were 25/20 C, photosynthetically active radiation was 450 µmol m−2 s−1, and day/night relative humidity was 70% and 85%, respectively. For growth under continuous ◦ darkness, the temperature was 25 C and relative humidity was 90%. For seedlings grown in darkness, a ‘chimney’ made from pots with bottoms removed was attached to the upper rim of the pot at 4 days after planting (DAP). The chimney served to support the elongating hypocotyl and epicotyl. For both light- and dark-grown seedlings, pots were subirrigated as required with an alternating schedule of water or 1/4 × Hoagland’s containing 50 ppm N.22 For seedlings grown in either light or dark, cotyledons were harvested at 0, 1, 2, 3, 5, 7, 10 and 14 DAP. At each time point, seeds from six pots [10 seedlings (pot−1)] were harvested and the testa and embryonic axis were removed manually. Cotyledons [20 pairs (replicate)−1] were weighed, placed in 50 mL conical tubes, frozen ◦ in liquid nitrogen and stored at −80 C until analyzed. Sample preparation Cotyledon samples were lyophilized and their dry weight measured. Samples were then ground to a fine powder using three (10 s) bursts with a water-cooled Knifetec 1095 sample mill (Foss North America, Eden Prairie, MN, USA). Samples were defatted with petroleum ether following protocol AOAC 2003.06 for Soxhlet lipid extraction.23 Lipid content was calculated as the difference in dry weight before and after defatting. Defatted samples were ground using a mortar and pestle to ensure a fine ◦ texture and then dried at 50 C for 24 h prior to analysis. Determination of soluble sugars, starch and cell wall polysaccharides The defatted samples were analyzed for soluble sugars, starch and cellwallpolysaccharidesaspreviouslydescribed.2,24 Cotyledoncell wallpolysaccharides(CWP)werequantifiedusingtheUppsalatotal 25 2 dietary fiber method as described by Stombaugh et al. Briefly, Figure 1. Non-cell wall carbohydrates (NCWC) and cell wall polysaccharide starch-free, 80% ethanol-insoluble samples were acid hydrolyzed (CWP) levels in cotyledons grown under a 16-h photoperiod ()orin to monosaccharide subunits. Neutral sugars were acetylated and darkness (). (A) Non-cell wall carbohydrates are defined as the sum of the alditol acetate derivitives were quantified by GC–FID. Uronic stachyose, raffinose, sucrose and starch, (B) cell wall polysaccharides are acids were quantified colorimetrically by the method of Ahmed defined as the sum of arabinose, fucose, galactose, glucose, mannose, 26 rhamnose, xylose, and total uronic acid residues. Data points represent and Labavitch using galacturonic acid as a reference standard. mean ± SE (n = 3). SE bars not shown if smaller than symbol. ∗ 1982 CWP were calculated as the sum of arabinose, fucose, galactose, indicates significant differences between cotyledons grown under a 16-h glucose, mannose, rhamnose, xylose and total uronic acid residues. photoperiod compared to darkness at the P < 0.05 level. www.interscience.wiley.com/jsfa This article is a US Government work J Sci Food Agric 2009; 89: 1981–1986 and is in the public domain in the USA Cell wall polysaccharides in soybean cotyledons www.soci.org made for dry, ungerminated cotyledons and cotyledons harvested cotyledons grown under the 16-h photoperiod or in darkness was at each time interval,
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