Published in Crop Sci. 44:2101-2106 (2004).
© 2004 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
CROP PHYSIOLOGY & METABOLISM
Quantitative Trait Loci Associated with Cell Wall Polysaccharides in Soybean Seed
S. K. Stombaugha,
J. H. Orfa,
H. G. Jungb,
K. Chasec,
K. G. Larkc and
D. A. Somersa,*
a Dep. of Agronomy and Plant Genetics, 1991 Upper Buford Circle, Univ. of Minnesota, St. Paul, MN 55108
b USDA-ARS, Plant Sciences Research Unit, and Dep. of Agronomy and Plant Genetics, 1991 Upper Buford Circle, Univ. of Minnesota, St. Paul, MN 55108
c Dep. of Biology, Univ. of Utah, Salt Lake City, UT 84112
* Corresponding author (somers{at}biosci.cbs.umn.edu)
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ABSTRACT
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Seed cell wall polysaccharides (CWPs) represent a significant portion of seed dry matter (DM) in soybean [Glycine max (L.) Merr.]. Quantitative trait locus (QTL) analysis is a step toward identifying genes controlling CWP concentration and composition of soybean seed. The objectives of this study were to identify QTLs associated with CWP variability and investigate the relationships between seed CWP, protein, and oil content. Whole soybean seed from ‘Minsoy’, ‘Archer’, and 108 Minsoy x Archer recombinant inbred (RI) lines were analyzed for CWP using the Uppsala total dietary fiber method. For a random subsample of 73 RI lines, embryos (seed with the seed coats removed) were analyzed. Three QTLs were observed on Linkage Groups U3 (ISU A2), U7 (ISU A1), and U24 (ISU K) that represented most of the variability in CWP content expressed on a DM basis in both whole seed and embryos. A QTL for fucose was detected on U3. Linkage Group U7 contained multiple QTLs mapping at the same location for galactose, the arabinose-to-galactose ratio (Ara/Gal), pectin, and CWP content. A QTL for arabinose was on U24. These same chromosomal regions also exhibited significant QTLs when the monosaccharide data were expressed on a CWP basis, suggesting that most of the variation in CWP was controlled by changes in the incorporation of galactose, arabinose, and fucose into CWP as total CWP concentration increased. Negative correlations of protein with oil, and the sum of protein and oil with most monosaccharides, pectin, and CWP were present within the RI population, indicating that decreasing seed CWP content will improve seed quality.
Abbreviations: Ara/Gal, arabinose-to-galactose ratio • CWP, cell wall polysaccharide • DM, dry matter • QTL, quantitative trait locus • RI, recombinant inbred
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INTRODUCTION
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THE CWPS CELLULOSE, pectin, and hemicellulose are synthesized from monosaccharide precursors such that their concentration and polymerization pattern determine CWP properties and function. In soybean seed, CWPs comprise a significant part of the total DM deposited during seed development. For example, CWPs averaged 165 g kg–1 DM in whole seed from a sample of 14 soybean genotypes from Maturity Groups 00 to I and exhibited significant genotypic and environmental variation (Stombaugh et al., 2000). The bulk of seed CWPs occurs in the cotyledons of a soybean embryo (seed without seed coats) and is composed of approximately 76% pectin and 24% cellulose plus hemicellulose (Daveby and Åman, 1993; Stombaugh et al., 2000). The CWP concentration is negatively correlated with the sum of protein and oil (protein + oil). These observations suggest that CWP synthesis, and specifically monosaccharide incorporation into pectin, diverts carbon away from protein and oil deposition in soybean seed (Stombaugh et al., 2000, 2003).
By studying genetically characterized populations of soybean that segregate for CWP, oil, and protein content, it should be possible to investigate the metabolic trade-offs between CWP, oil, and protein. Moreover, in such populations it becomes possible to identify the genetic determinants that regulate such trade-offs. In soybean, several linkage maps have been developed (Lee et al., 1996; Brummer et al., 1997) and consensus maps further defined (Cregan et al., 1999; Song et al., 2004). Quantitative trait locus (QTL) analysis can be used to provide insight into the genetic control of seed CWP concentration and composition. Furthermore, inferences may be drawn about simultaneous regulation when different traits map to similar loci. For instance, height, maturity, and yield are correlated in soybean and share some QTLs (Lee et al., 1996; Mansur et al., 1996). Monosaccharides comprising CWP are intercorrelated (Stombaugh et al., 2000, 2003), their formation is part of a multistep pathway, and some monosaccharides like glucose are found in the different CWP, thus there is potential for many QTLs controlling trait variability.
There are very few studies reporting QTL analysis of CWP concentration or composition in plants in general and especially in seed. Hazen et al. (2003) reported on QTLs affecting sugar composition of maize (Zea mays L.) pericarp cell walls. A QTL analysis of CWP concentration or composition of legume seed has not been reported. One reason for this paucity of CWP studies is that analytical procedures required to quantify CWP are relatively expensive, thereby limiting the numbers of individuals that can be used in a QTL analysis. Nevertheless, our previous research (Stombaugh et al., 2000, 2003) indicated that there were significant genotypic differences in soybean seed CWP. In an effort to further characterize the regulation of CWP deposition in soybean seed, we initiated a QTL analysis. The objectives of this study were to quantify variation in CWP monosaccharide concentration and composition in the Minsoy x Archer RI population, identify QTLs associated with these traits, and estimate the amount of variability accounted for by each QTL. We also investigated potential relationships between CWP and the seed traits, protein, oil, protein + oil, and seed weight in this population. The Minsoy x Archer RI population has been used to determine the map locations for a range of agronomic and seed composition QTLs (Mansur et al., 1993; Orf et al., 1999a, 1999b). Thus, mapping CWP QTLs in this population would likely provide additional information on relationships with other seed traits. The QTL analysis of seed CWP concentration may provide information that will lead to breeding and eventually genetic engineering strategies to reduce the flow of assimilates into CWP and thus increase the percentage of oil and protein, allowing the development of cultivars with higher quality and more valuable soybean seed.
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MATERIALS AND METHODS
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Minsoy, Archer, and 108 Minsoy x Archer RI lines (Mansur et al., 1993) were grown in Minnesota at Waseca in 1997 and Rosemount in 2000 in uniform field trials. The seed analyzed was sampled from small plot, combine-harvested two-row plots 3.7 m long which were end-trimmed at harvest to 2.5 m. The row spacing between plots was 75 cm and plots were planted at 375000 seed ha–1. The RI lines were divided into blocks based on maturity. Each block had two replications (plots) of each RI line using a randomized complete block design. In each year, seed harvested from the replicates were combined into a single sample for analysis. Whole seed were ground, defatted, and analyzed for CWP content using the Uppsala total dietary fiber method (Theander et al., 1995) as described by Stombaugh et al. (2000). Briefly, samples were digested with amylase and 
-amyloglucosidase to remove starch along with monosaccharides and oligosaccharides. The cell wall material was collected by precipitation in 80% ethanol and hydrolyzed by a two-stage sulfuric acid treatment. Neutral sugar residues were measured by GC-FID as alditol acetate derivatives. Uronic acids were measured colorimetrically using galacturonic acid as a reference standard (Ahmed and Labavitch, 1977). To determine embryo CWP concentration and composition, seed coats were removed from 73 RI lines grown at Waseca, MN, in 1997, and remaining cotyledons and embryonic axes were ground, defatted, and analyzed for total dietary fiber using the same method as for whole seed. The CWP was calculated as the sum of arabinose, fucose, galactose, glucose, mannose, rhamnose, xylose, and total uronic acid residues. Pectin was calculated as the sum of uronic acids, galactose, arabinose, rhamnose, and fucose based on previous reports of soybean pectin composition (Aspinall et al., 1967; Stombaugh et al., 2000). Monosaccharide data were expressed on the basis of seed concentration (g kg–1 seed DM) and CWP composition (g kg–1 CWP). Oil was chemically quantified by Soxhlet extraction. Monosaccharide and oil analyses were conducted in duplicate and averaged. Protein concentration was determined using near infrared reflectance spectroscopy (Orf et al., 1999b).
The data for the RI lines were analyzed as a randomized complete block design using years (1997 and 2000) as blocks in Statistix 7 (Analytical Software, Tallahassee, FL). Heritability estimates were computed and the sample interval mapping feature of PLABQTL was used to detect QTLs as described by Orf et al. (1999b). Markers, assay methods, and linkage group designations were previously described in Orf et al. (1999b). For whole seed, QTLs were determined for each year and for both years combined. A LOD score of 3.2 was designated as the threshold to identify significant QTLs.
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RESULTS
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Phenotypic Variation and Correlations
The average concentration of monosaccharides, CWP, oil, and protein in whole seed of Minsoy and Archer, and in whole seed and embryos (seeds without seed coats) of the Minsoy x Archer RI lines are shown in Table 1. Although whole seed of Minsoy and Archer and the RI population had similar average contents of each monosaccharide (Table 1), the extremes in the RI population significantly exceeded (P < 0.05) the monosaccharide contents of the parental lines, indicating transgressive segregation for the majority of monosaccharides. The averages and range of monosaccharide content in embryos (Table 1) indicated that the monosaccharides incorporated into pectin were mostly found in the embryo. Average concentrations of pectin, CWP, oil, protein, and the sum of protein + oil also exhibited transgressive segregation in the RI population (Table 1).
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Table 1. Cell wall polysaccharide (CWP) concentration and composition, and content of protein and oil in whole seed, seed weight (SDWT), and heritability (h2) of ‘Minsoy’, ‘Archer’, and 108 Minsoy x Archer recombinant inbred (RI) lines grown in 1997 and 2000, and of embryos from 73 RI lines grown in 1997.
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Monosaccharide concentrations were positively correlated with each other in the RI population (Table 2). Significant negative correlations were observed for seed weight, oil, and the sum of protein + oil with rhamnose, arabinose, galactose, pectin, and CWP. Seed weight was negatively correlated with xylose, glucose, and mannose (Table 2).
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Table 2. Correlations among seed traits in whole seed of 108 ‘Minsoy’ x ‘Archer’ recombinant inbred lines. Averaged data from 1997 and 2000 were used in the analysis.
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Genetic Control of Cell Wall Polysaccharide in Whole Seed
Fucose, arabinose, and galactose content of whole seed exhibited relatively high heritability in the RI population compared with the other monosaccharides (Table 1). Whole seed data were analyzed for QTLs separately for the 2 yr and across the 2 yr (Table 3). Significant QTLs were detected for fucose, glucose, galactose, arabinose, Ara/Gal, pectin, CWP, protein, and seed weight of whole seeds of the RI population averaged across the 2 yr (Table 3). A major QTL located on U3 explained 37.8% of the variation in fucose content. The QTLs located in the same region of U7 (Satt174-Satt211) were observed for galactose, Ara/Gal, pectin, and CWP, and explained 27, 19.5, 22.3, and 16.5% of the phenotypic variation, respectively. A minor QTL for glucose content on U21 explained 13% of the variation. Seed weight exhibited a QTL on U14 that accounted for 13% of the variation. Protein exhibited a minor QTL on U22 in 1997 and the 2-yr average, but there was no QTL detected for oil. A QTL located on U24 represented 45.2% of arabinose variation.
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Table 3. Quantitative trait loci (LOD  3.2) for cell wall carbohydrates, protein, and oil content in whole seed of 108 recombinant inbred lines grown in 1997 and 2000.
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While the same QTLs were identified in all three analyses (1997, 2000, and the 2-yr average) for some traits, such as fucose, galactose, and arabinose concentration, most traits were not this consistent (Table 3). The same QTL was detected for pectin in all three analyses, but an additional QTL was located using year 2000 data. Glucose was the only monosaccharide for which a QTL was detected for the 2-yr average data, but not for either individual year (Table 3). Significant QTLs for fucose, galactose, and arabinose composition of CWP were detected in the same locations as determined for the concentration of these monosaccharides expressed on a seed DM basis (U3, U7, and U24). The QTL for glucose content expressed on a DM basis on U21 was not observed when glucose was expressed on a per-CWP basis (data not shown).
Embryo Cell Wall Polysaccharide
Comparing the embryo QTLs with QTLs from whole seed in 1997, more QTLs were observed after removal of the seed coat; however, most of these were marginally significant (Table 4). Some QTLs were specific to embryo tissue. The fucose QTLs on U14 and U19 were unique to this tissue, as were the arabinose QTL on U12, glucose QTL on U19, and xylose QTL on U9. In embryos, galactose, rhamnose, glucose, and CWP QTLs were observed on U7 near the location determined in whole seed. While the location with the highest LOD score for QTLs on U7 varied between whole seed and embryos, the U7 QTLs all exhibited a similar pattern across the linkage group (data not shown).
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Table 4. Quantitative trait loci (LOD 3.2) for cell wall carbohydrate content in soybean embryos of 73 recombinant inbred lines grown in 1997.
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DISCUSSION
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This is the first report of QTL analysis of soybean seed CWPs. The relationships between the monosaccharides, pectin, CWP, protein, oil, the sum of protein + oil, and seed weight in the RI lines were generally the same as previously reported for whole seed of 14 soybean genotypes from Maturity Groups 00 to 1 grown at four locations in Minnesota (Stombaugh et al., 2000, 2003). Specifically, there were significant negative correlations for the sum of protein and oil with pectin, CWP, rhamnose, arabinose, and galactose (Table 2). These results indicated that the Minsoy x Archer RI population would be useful for dissecting these relationships and that the QTL analysis is likely representative of the genetic control of these seed constituents in soybean cultivars. The negative relationship between the sum of protein and oil with CWP concentration suggests that synthesis of the monosaccharides and their incorporation into CWP diverts carbon away from protein and oil deposition (Stombaugh et al., 2000, 2003). The QTLs for specific monosaccharides at three different genomic locations were detected across both years of the study. The numbers of lines per year was restricted to 108 because of the expense of CWP analysis. Although this population size provides reliable identification of QTLs, estimates of the magnitude of their effects can be overestimated (Beavis, 1998). Thus, we regard these estimates as simply informational at this point. Certainly, larger populations with more replication will need to be evaluated to accurately determine the impacts of these QTLs. This will require development of more economical analytical methods for quantifying monosaccharides.
The CWP traits in whole soybean seeds must be interpreted with some caution because two different plant parts (seed coat and embryo) are combined. Soybean seed coat cell walls are primarily composed of hemicellulose and cellulose (Stombaugh et al., 2000). The negative correlations of xylose, glucose, and mannose (the major monosaccharides of hemicellulose and cellulose) with seed weight may reflect the simple observation that smaller soybean seeds tend to have higher seed coat-to-embryo DM ratios compared with large seed. The major QTLs at U3, U7, and U24 observed in whole seed were present at or near the same loci in embryos with similar LOD scores, indicating that the variation giving rise to these QTLs was derived from the embryo and not the seed coat. This conclusion is consistent with the observation that the bulk of these monosaccharides are in the embryo (Stombaugh et al., 2000).
A region of U7 exhibited QTLs for galactose concentration and composition, and the Ara/Gal, which was previously shown to be negatively correlated with yield and maturity, pectin, and CWP content (Stombaugh et al., 2003). The pattern of QTLs on U7 in whole seed and embryos were very similar, with the exception of detecting significant QTLs for glucose and rhamnose in embryos compared with the whole seed, indicating that seed coat CWP content obscured these QTL in whole seed analysis. The number of QTLs in the U7 region is unclear. There appears to be more than one. However, this region of Linkage Group U7 is not well saturated with markers, making it difficult to discern how many QTLs are at this location.
The region of U7 that exhibited the CWP QTLs has also been shown to be important for oil and protein content in other populations and studies. A QTL for protein content has been reported in this region of U7 in a Minsoy x Noir RI population; however, no protein QTL was detected in our study or has been reported on U7 in the Minsoy x Archer RI population (Orf et al., 1999b), suggesting lack of polymorphism for alleles of this protein QTL in the population. A significant oil QTL was reported at this location on U7 in the Minsoy x Archer RI population (Orf et al., 1999b). Although we did not detect this oil QTL on U7, these results suggest that genes in this region of the genome are involved in determining the deposition of oil, protein, and CWP in soybean seed. The QTLs for protein and oil are present in duplicated soybean genomic regions described by Shoemaker et al. (1996). Only the fucose U3 QTL and the multitrait U7 locus were in these duplicated regions (Tables 3 and 4). Thus, it is possible that with QTL mapping of seed CWP monosaccharides in different RI populations, similar relationships among the duplicated regions of the soybean genome will emerge, and that these genomic regions may control the content of multiple monosaccharides.
Interpreting the soybean QTL data in relation to the synthesis of CWP is a major challenge. There are no similar studies analyzing seed CWP in soybean or other dicots, including Arabidopsis thaliana (L.) Heynh. A recent study in maize described QTLs controlling the monosaccharide content of the pericarp (Hazen et al., 2003). Two QTLs on maize chromosome 3, one for arabinose + galactose and one for arabinose, were aligned with a syntenic region of the rice (Oryza sativa L.) genome. Hazen et al. (2003) observed that among numerous genes linked to these QTLs, two encoded putative glycosyltransferases. Unfortunately, physical mapping resources for soybean are not sufficiently developed to pursue a similar analysis. Moreover, the wide divergence of dicot and monocot genomes precludes a comparison of the soybean and maize data.
The same QTLs were detected when the data were calculated as either monosaccharide concentration on a DM basis or on a CWP basis. Thus, it appears that the variation in CWP concentration is primarily associated with changes in CWP composition. Whether the QTLs detected in soybean are controlled by genes involved in synthesis of the monosaccharide precursors of the CWP or their incorporation into CWP is more difficult to ascertain. Synthesis of monosaccharides incorporated into CWP occurs via complex pathways consisting of multiple enzymatic steps (Reiter and Vanzin, 2001; Seifert, 2004). Likewise, incorporation of the monosaccharides into CWP is complex and poorly elucidated. The QTLs were detected for fucose, galactose, and arabinose in our study; these monosaccharides with rhamnose and the uronic acids are primarily incorporated into pectic polysaccharides. This family of complex polysaccharides requires a large number of biosynthetic steps for monosaccharide precursor synthesis and incorporation into the cell wall (Ridley et al., 2001). The complex structure of pectin suggests that several control points may be resolved as QTLs. The absence of QTLs for multiple monosaccharides at the same genomic locations in soybean (Tables 3 and 4) may reflect variation in the regulation of the synthesis of the various monosaccharides, which in turn are incorporated into pectin at ratios reflecting their synthesis rates.
Soybean pectin is composed of rhamnogalacturonic acid backbones, with rhamnose being used as branch points for galactose and arabinose homo- and heteropolymer side chains (Aspinall et al., 1967; Huisman et al., 1999, 2001). As such, regulation of rhamnose and galacturonic acid incorporation into polysaccharides may vary the amount of galactose and arabinose incorporated. However, the soybean monosaccharide data for the RI population we studied indicated that there were no QTLs detected for total uronic acids, and only one at U7 for rhamnose in embryos. This observation suggests that most of the variation in pectin and CWPs was caused by increases in galactose and arabinose concentration of the CWP. This suggests that at the enzymatic level, pectin formation may be regulated by transferases that control the frequency and length of galactose- and arabinose-containing side chains added to the rhamnogalacturonic acid backbones. Further investigations will be required to test this hypothesis. A number of genes coding for enzymes involved in CWP synthesis have been identified as a result of extensive efforts to elucidate plant cell wall biosynthesis and of plant genomics efforts. Mapping these genes in RI populations to determine their relationships with QTLs identified in this study will be a useful approach to further investigating the genes controlling the CWP QTLs.
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NOTES
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Contribution of the Minnesota Agric. Exp. Stn. Supported in part by grants from the Minnesota Soybean Research and Promotion Council and USDA-NRICGP, grant number 2001-35301-10546.
Received for publication December 10, 2003.
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ABSTRACT
INTRODUCTION
