Published August 30, 2018 RESEARCH Genetic Analysis of Sugar Composition and Its Relationship with Protein, Oil, and Fiber in Soybean Guo-Liang Jiang,* Pengyin Chen, Jiaoping Zhang, Liliana Florez-Palacios, Ailan Zeng, Xianzhi Wang, Ronald A. Bowen, Amanda Miller, and Haley Berry G.-L. Jiang, R.A. Bowen, A. Miller, and H. Berry, Agricultural Research ABSTRACT Station, Virginia State Univ., PO Box 9061, Petersburg, VA 23806; P. Soybean [Glycine max (L.) Merr.] is one of the Chen, Dep. of Crop, Soil and Environmental Sciences, Univ. of Arkansas, most important crops in the world. It is a major Fayetteville, AR 72701, current address, Univ. of Missouri, Fisher Delta source of vegetable oil for consumption and Research Center, Portville, MO 63873; J. Zhang, Plant Science Dep., protein meal for animal feeds and has also been South Dakota State Univ., Brookings, SD 57007, current address, Dep. widely used in human food industries because of Agronomy, Iowa State Univ., Ames, IA; L. Florez-Palacios and A. of its nutritive and health benefits. To provide Zeng, Dep. of Crop, Soil and Environmental Sciences, Univ. of Arkansas, useful information for soybean quality improve- Fayetteville, AR 72701; X. Wang, Plant Science Dep., South Dakota State ment, seed individual sugars, total sugar, Univ., Brookings, SD 57007, current address, College of Agriculture, protein, oil, and dietary fiber were genetically Yunnan Univ., Kunming, China. Received 11 Mar. 2018. Accepted 10 analyzed in replicated trials with 323 germplasm July 2018. *Corresponding author ([email protected], gljiang99@yahoo. lines grown in South Dakota and 137 cultivars com). Assigned to Associate Editor Owen Hoekenga. and breeding lines grown in Virginia. The results Abbreviations: HPAEC-PAD, high-performance anion-exchange indicated significant differences among the chromatography coupled with pulsed amperometric detection; HPLC, genotypes for all traits investigated. Environment high-performance liquid chromatography; NIFA, National Institute effect and genotype ´ environment interaction of Food and Agriculture; NIR, near-infrared; PI, plant introduction; were also significant in most cases. Heritability RIL, recombinant inbred line. estimates were high (94.45–97.79%) for all traits in the germplasm population, and higher in the population of breeding lines for most traits. High oybean [Glycine max (L.) Merr.] is a leading crop grown world- genotypic correlation existed between sucrose Swide for production of vegetable oil for human consumption and and total sugar, which helps improvement of provision of protein meal for animal feeds. It has also been widely digestible sugars and sweetness in soybean used in human food industries because more and more people food. However, attention should be paid to the have become aware of its health benefits. In general, soybean seeds lines with higher sucrose but lower oligosaccha- consist of approximately 40% protein, 20% oil, 35% carbohydrate, rides, since stachyose was positively associated and 5% ashes (Liu, 1999; Karr-Lilienthal et al., 2005). Soybean with total sugar. Genotypic correlations between as a dietary protein source contains 18 amino acids, including all seed sugars and protein were insignificant or essential amino acids that cannot be synthesized in human body very low in most cases, implying that altera- and conditionally essential amino acids except glutamine, the tion of seed sugars might not necessarily affect synthesis of which can be limited under given conditions. Soybean protein. In some cases, however, there might be negative correlations between seed sugars and oil is composed of five fatty acids: palmitic, stearic, oleic, linoleic, oil or dietary fiber in soybean. This study also and linolenic acids. Of the carbohydrates in soybean, important identified some unique germplasm lines with components include dietary fiber (or nonstarch polysaccharides) a desired level of a specific seed composition: one with high sucrose, five with low raffinose, Published in Crop Sci. 58:2413–2421 (2018). 15 with high total sugar, seven with high protein, doi: 10.2135/cropsci2018.03.0173 and four high in both sucrose and total sugar. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA This is an open access article distributed under the CC BY license (https:// creativecommons.org/licenses/by/4.0/). CROP SCIENCE, VOL. 58, NOVEMBER–DECEMBER 2018 WWW.CROPS.ORG 2413 and sugars such as sucrose, raffinose, and stachyose (Choct was positively associated with protein (Hymowitz et al., et al., 2010). The proportion of seed composition deter- 1972). Wilcox and Shibles (2001) reported that concentra- mines the uses of soybean. For instance, cultivars high in tions of carbohydrates were not associated with seed yield, oil are preferred by vegetable oil and soy-diesel industries, but increased protein was coupled with decreases in oil, whereas soy food products usually need lower oil but higher total carbohydrates, and sucrose. In an evaluation of 23 protein and sugar contents. conventional and food-grade cultivars, Geater and Fehr Soybean seed protein and oil contents have been (2000) suggested that total sugar was highly correlated extensively investigated, particularly in plant breeding with the sum of protein and oil. In a study with 30 vege- and genetics from quantitative genetics to molecular table soybean genotypes, negative correlations were found mapping and candidate gene identification (Wang et al., between protein and total sugar (r = −0.52) or sucrose (r = 2014; Hwang et al., 2014; Zhang et al., 2018). Relatively, −0.43), whereas no significant correlations were detected studies on sugar and fiber content in soybean are less between oil and total sugar or sucrose (Li et al., 2012). Yu reported. Sucrose, a disaccharide and the most important et al. (2016) evaluated 35 soybean germplasm lines (mostly component of total sugar in soybean, is a free or digestible from China) for five individual and total sugars, as well as sugar and is very important for food soybean (Kumar et protein. They found that protein content was positively al., 2010; Song et al., 2013). Similarly, monosaccharides correlated with total sugar and sucrose contents but nega- glucose and fructose are also easily digested, and thus they tively correlated with fructose and glucose contents. should be worthy of exploring, in particular for food use There have historically been fewer carbohydrate- of soybeans like edamame (Song et al., 2013). However, focused studies than studies focused on protein and/ two oligosaccharides, raffinose and stachyose, cannot be or oil content, and the studies that considered all prox- digested in monogastric animals and cause flatulence imate nutrients including sugars, protein, oil, and fiber (Choct et al., 2010). A decreased concentration of both were even more limited. In most of the previous studies raffinose and stachyose is preferred in soy food industries on seed sugar content in soybean, the number of geno- such as soymilk and tofu production (Kumar et al., 2010; types used was relatively small compared with the studies Saldivar et al., 2011). on protein and oil research. Inconsistencies between the Using high-performance anion-exchange chroma- studies existed to some extent. In addition, there is lack tography coupled with pulsed amperometric detection of understanding of genetic variability of fiber content (HPAEC-PAD), Bainy et al. (2008) reported varietal in soybean, although it is an important trait in vegetable differences in carbohydrates in defatted soybean flour and soybeans that are consumed directly for fresh market and soy protein isolate byproducts among 12 soybean lines. other food-grade soybeans that are used by food product Hou et al. (2009) analyzed five individual sugars and manufacturers (Redondo-Cuenca et al., 2007). Genotypic total sugar in 241 germplasm accessions of three maturity correlation between sugars and other traits has rarely been groups using high-performance liquid chromatography discussed. Therefore, there is a need to further investigate (HPLC). They identified some plant introductions (PIs) the genetic feature of sugars and their relationships with considerably low or high in individual sugars. Cicek et other seed composition in soybean. To provide useful al. (2006) reported a high heritability for sucrose content, information for quality improvement and related research, but relatively low heritabilities for stachyose and raffinose using two populations, one consisting of 323 soybean contents in a recombinant inbred line (RIL) population germplasm accessions grown in South Dakota and one of derived from an interspecific cross. Quantitative trait loci 137 cultivars and breeding lines grown in Virginia, we associated with sucrose and oligosaccharide contents were characterized seed individual sugar, total sugar, protein, also explored (Maughan et al., 2000; Kim et al., 2005). oil, and dietary fiber content in the present study. We also Strong correlations between sugars were previously analyzed the genotypic correlations between the traits. reported (Cicek et al., 2006; Hou et al., 2009). In the study by Hou et al. (2009), the absolute values of simple MATERIALS AND METHODS correlation coefficients among individual sugar and total Genotypes and Field Trials sugar contents varied from 0.59 to 0.999, except between Experiment 1 total sugar and glucose (r = −0.27) or fructose (r = −0.24). In total, 323 soybean germplasm accessions or PIs were obtained Hymowitz et al.