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Journal of Integrative Agriculture  2024, Vol. 23 Issue (12): 3966-3982    DOI: 10.1016/j.jia.2023.09.010
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Mapping and identification of QTLs for seed fatty acids in soybean (Glycine max L.)

Yiwang Zhong1, 2, 6*, Xingang Li1, 2*, Shasha Wang1, 2, Sansan Li1, 2, Yuhong Zeng1, 2, Yanbo Cheng1, 2, Qibin Ma1, 2, Yanyan Wang3, Yuanting Pang4, 5, Hai Nian1, 2, 4#, Ke Wen1, 2, 3, 4, 6#

1 State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, Guangzhou 510642, China

2 Guangdong Sub-center of the National Center for Soybean Improvement/College of Agriculture, South China Agricultural University, Guangzhou 510642, China

3 Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

4 Hainan Seed Industry Laboratory, Sanya 572025, China

5 Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops/Department of Vegetable Science, College of Horticulture, China Agricultural University, Beijing 100193, China 

6 Key Laboratory of Genetic Resources Evaluation and Utilization of Tropical Fmuits and Vegetables, Co-construction by Ministry of Agriculture and Rural Affairs and Hainan Province/Key Laboratory of Vegetable Biology of Hainan Province/Vegetable Research Institute, Hainan Academy of Agricultural Sciences, Haikou 570228, China

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摘要  

大豆是世界上最重要的植物油来源之一。油分含量和脂肪酸比例因其对豆油产品的保质期和消费者健康的影响而受到广泛关注。本研究利用桂早 1 号和巴西 13 杂交构建的重组自交系群体的高密度遗传图谱,鉴定棕榈酸(PA)、硬脂酸(SA)、油酸(OA)、亚油酸(LA)、亚麻酸(LNA)和含油量的数量性状位点(QTL)。在遗传图谱连锁分析中共检测到 54 个QTL。在这些性状定位结果共享的 6 个染色体 bin 区间中,13 号染色体上的 bin 区间(bin106 - bin118 和 bin123 - bin125)在多种环境下被检测为稳定的新 QTL,与 OA、LA 和 LNA 相关。通过亲本重测序、生物信息学和 RNA 测序数据的联合分析,确定这些共享区间内的 8 个差异表达基因(DEGs)为候选基因。本研究结果将有助于培育脂肪酸比例理想的适宜食用的大豆,并为挖掘与大豆脂肪酸和油脂含量相关的基因提供遗传信息基础。



Abstract  
Soybean is one of the most important sources of vegetable oil.  The oil content and fatty acid ratio have attracted significant attention due to their impacts on the shelf-life of soybean oil products and consumer health.  In this study, a high-density genetic map derived from Guizao 1 and Brazil 13 was used to analyze the quantitative trait loci of palmitic acid (PA), stearic acid (SA), oleic acid (OA), linoleic acid (LA), linolenic acid (LNA), and oil content (OC).  A total of 54 stable QTLs were detected in the genetic map linkage analysis, which shared six bin intervals.  Among them, the bin interval on chromosome 13 (bin106–bin118 and bin123–bin125) was found to include stable QTLs in multiple environments that were linked to OA, LA, and LNA.  Eight differentially expressed genes (DEGs) within these QTL intervals were determined as candidate genes according to the combination of parental resequencing, bioinformatics and RNA sequencing data.  All these results are conducive to breeding soybean with the ideal fatty acid ratio for food, and provide the genetic basis for mining genes related to the fatty acid and oil content traits in soybean.
Keywords:  soybean        oil        fatty acids        QTL        gene  
Received: 14 April 2023   Accepted: 19 July 2023
Fund: 
This research was supported by funding from the Seed Industry Revitalization Plan of Guangdong Province, China (2022-NPY-00-007), the Hainan Seed Industry Laboratory, China (B21HJ0901 and B23C1000416), the Key-Area Research and Development Program of Guangdong Province, China (2020B020220008), the National Natural Science Foundation of China (31971966 and 31971965), the China Agricultural Research System (CARS-04-PS09), the National Key Research and Development Projects, China (2018YFE0116900-06), Guangdong Agricultural Science and Technology Innovation and Promotion Project, China (2019KJ136-03), and the Sanya Science and Technology Innovation Special Project, China (2022KJCX11). 
About author:  #Correspondence Hai Nian, Tel: +86-20-85288024, E-mail: hnian@scau.edu.cn; Ke Wen, Mobile: +86-13544332296, E-mail: wenke@hnaas.org.cn * These authors contributed equally to this study.

Cite this article: 

Yiwang Zhong, Xingang Li, Shasha Wang, Sansan Li, Yuhong Zeng, Yanbo Cheng, Qibin Ma, Yanyan Wang, Yuanting Pang, Hai Nian, Ke Wen. 2024. Mapping and identification of QTLs for seed fatty acids in soybean (Glycine max L.). Journal of Integrative Agriculture, 23(12): 3966-3982.

Agarwal M, Shrivastava N, Padh H. 2008. Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Reports, 27, 617–631.

Aghoram K, Wilson R F, Burton J W, Dewey R E. 2006. A mutation in a 3-keto-acyl-acp synthase II gene is associated with elevated palmitic acid levels in soybean seeds. Crop Science, 46, 2453–2459.

Akond M, Liu S, Boney M, Kantartzi S K, Meksem K, Bellaloui N, Lightfoot D A, Kassem M A. 2014. Identification of quantitative trait loci (QTL) underlying protein, oil, and five major fatty acids’ contents in soybean. American Journal of Plant Sciences, 5, 158–167.

Andre C, Benning C. 2007. Arabidopsis seedlings deficient in a plastidic pyruvate kinase are unable to utilize seed storage compounds for germination and establishment. Plant Physiology, 145, 1670–1680.

Andre C, Froehlich J E, Moll M R, Benning C. 2007. A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. The Plant Cell, 19, 2006–2022.

Andreu V, Lagunas B, Collados R, Picorel R, Alfonso M. 2010. The GmFAD7 gene family from soybean: Identification of novel genes and tissue-specific conformations of the FAD7 enzyme involved in desaturase activity. Journal of Experimental Botany, 61, 3371–3384.

Ash M, Dohlman E. 2017. Oil Crops Outlook. Economic Research Service, Situation and Outlook Report, United States Department of Agriculture, USA.

Avise J C. 1993. Molecular Markers, Natural History and Evolution. Springer, New York, NY.

Bachlava E, Dewey R E, Burton J W, Cardinal A J. 2009. Mapping and comparison of quantitative trait loci for oleic acid seed content in two segregating soybean populations. Crop Science, 49, 433–442.

Baud S, Wuillème S, Dubreucq B, de Almeida A, Vuagnat C, Lepiniec L, Miquel M, Rochat C. 2007. Function of plastidial pyruvate kinases in seeds of Arabidopsis thaliana. Plant Journal, 52, 405–419.

Bilyeu K D, Palavalli L H, Sleper D A, Beuselinck P R. 2003. Three microsomal omega-3 fatty-acid desaturase genes contribute to soybean linolenic acid levels. Crop Science, 43, 1833–1838.

Biswas N, Cheow Y L, Tan C P, Siow L F. 2017. Physical, rheological and sensorial properties, and bloom formation of dark chocolate made with cocoa butter substitute (CBS). LWT-Food Science and Technology, 82, 420–428.

Cahoon E B. 2003. Genetic enhancement of soybean oil for industrial uses: prospects and challenges. Agbioforum, 6, 11–13.

Cardinal A J, Burton J W, Camacho-Roger A M I A, Yang J H, Wilson R F, Dewey R E. 2007. Molecular analysis of soybean lines with low palmitic acid content in the seed oil. Crop Science, 47, 304–310.

Cheng K, Pan Y F, Liu L M, Zhang H Q, Zhang Y M. 2021. Integrated transcriptomic and bioinformatics analyses reveal the molecular mechanisms for the differences in seed oil and starch content between Glycine max and Cicer arietinum. Frontiers in Plant Science, 12, 743680.

Cherry J H, Bishop L, Hasegawa P M, Lefflert H R. 1985. Differences in the fatty acid composition of soybean seed produced in northern and southern areas of the USA. Phytochemistry, 24, 237–241.

Chu S, Li H, Zhang X, Yu K, Chao M, Han S, Zhang D. 2018. Physiological and proteomics analyses reveal low-phosphorus stress affected the regulation of photosynthesis in soybean. International Journal of Molecular Sciences, 19, 1688.

Chung J, Babka H L, Graef G L, Staswick P E, Lee D J, Cregan P B, Shoemaker R C, Specht J E. 2003. The seed protein, oil, and yield QTL on soybean linkage group I. Crop Science, 43, 1053–1067.

Clemente T E, Cahoon E B. 2009. Soybean oil: Genetic approaches for modification of functionality and total content. Plant Physiology, 151, 1030–1040.

Collados R, Andreu V, Picorel R, Alfonso M. 2006. A light-sensitive mechanism differently regulates transcription and transcript stability of ω3 fatty-acid desaturases (FAD3, FAD7 and FAD8) in soybean photosynthetic cell suspensions. FEBs Letters, 580, 4934–4940.

Das U N. 2006. Essential fatty acids: Biochemistry, physiology and pathology. Biotechnology Journal, 1, 420–439.

Depree J A, Savage G P. 2001. Physical and flavour stability of mayonnaise. Trends in Food Science & Technology, 12, 157–163.

Diers B W, Keim P, Fehr W R, Shoemaker R C. 1992. RFLP analysis of soybean seed protein and oil content. Theoretical and Applied Genetics, 83, 608–612.

Do P T, Nguyen C X, Bui H T, Tran L T N, Stacey G, Gillman J D, Zhang Z J, Stacey M G. 2019. Demonstration of highly efficient dual gRNA CRISPR/Cas9 editing of the homeologous GmFAD2-1A and GmFAD2-1B genes to yield a high oleic, low linoleic and α-linolenic acid phenotype in soybean. BMC Plant Biology, 19, 311.

Dornbos D L, Mullen R E. 1992. Soybean seed protein and oil contents and fatty acid composition adjustments by drought and temperature. Journal of the American Oil Chemists Society, 69, 228–231.

Drexler H, Spiekermann P, Meyer A, Domergue F, Zank T, Sperling P, Abbadi A, Heinz E. 2003. Metabolic engineering of fatty acids for breeding of new oilseed crops: strategies, problems and first results. Journal of Plant Physiology, 160, 779–802.

Eskandari M, Cober E R, Rajcan I. 2013a. Genetic control of soybean seed oil: I. QTL and genes associated with seed oil concentration in RIL populations derived from crossing moderately high-oil parents. Theoretical and Applied Genetics, 126, 483–495.

Eskandari M, Cober E R, Rajcan I. 2013b. Genetic control of soybean seed oil: II. QTL and genes that increase oil concentration without decreasing protein or with increased seed yield. Theoretical and Applied Genetics, 126, 1677–1687.

Fan S, Li B, Yu F, Han F, Yan S, Wang L, Sun J. 2015. Analysis of additive and epistatic quantitative trait loci underlying fatty acid concentrations in soybean seeds across multiple environments. Euphytica, 206, 689–700.

Fehr W R, Caviness C E. 1977. Stages of Soybean Development. Extension and Experiment Station Publications, Holland.

Ghassemi-Golezani K, Farhangi-Abriz S. 2018. Changes in oil accumulation and fatty acid composition of soybean seeds under salt stress in response to salicylic acid and jasmonic acid. Russian Journal of Plant Physiology, 65, 229–236.

Grant D, Nelson R T, Cannon S B, Shoemaker R C. 2010. Soybase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Research, 38, D843–D846.

Ha B, Kim H, Velusamy V, Vuong T D, Nguyen H T, Shannon J G, Lee J. 2014. Identification of quantitative trait loci controlling linolenic acid concentration in PI483463 (Glycine soja). Theoretical and Applied Genetics, 127, 1501–1512.

Hammond E G, Fehr W R, Snyder H E. 1972. Improving soybean quality by plant breeding. Journal of the American Oil Chemists’ Society, 49, 33–35.

Hammond E G, Johnson L A, Su C. 2005. In: Shahidi F, ed., Soybean Oil. Bailey’s Industrial Oil and Fat Products. USA.

Hanway J, Thompson H. 1971. How a Soybean Plant Develops. Iowa State University of Science and Technology, USA.

Head K, Galos T, Fang Y, Hudson K. 2012. Mutations in the soybean 3-ketoacyl-acp synthase gene are correlated with high levels of seed palmitic acid. Molecular Breeding, 30, 1519–1523.

Hong M J, Jang Y E, Kim D G, Kim J M, Lee M K, Kim J B, Eom S H, Ha B K, Lyu J I, Kwon S J. 2019. Selection of mutants with high linolenic acid contents and characterization of fatty acid desaturase 2 and 3 genes during seed development in soybean (Glycine max). Journal of the Science of Food and Agriculture, 99, 5384–5391.

Huang J, Ma Q, Cai Z, Xia Q, Li S, Jia J, Chu L, Lian T, Nian H, Cheng Y. 2020. Identification and mapping of stable QTLs for seed oil and protein content in soybean [Glycine max (L.) Merr.]. Journal of Agricultural and Food Chemistry, 68, 6448–6460.

Hwang H, Singh M, Bakota E L, Winkler-Moser J K, Kim S, Liu S X. 2013. Margarine from organogels of plant wax and soybean oil. Journal of the American Oil Chemists’ Society, 90, 1705–1712.

Hyten D L, Pantalone V R, Sams C E, Saxton A M, Landau-Ellis D, Stefaniak T R, Schmidt M E. 2004. Seed quality QTL in a prominent soybean population. Theoretical and Applied Genetics, 109, 552–561.

Innis S M. 1991. Essential fatty acids in growth and development. Progress in Lipid Research, 30, 39–103.

Ivanov S, Lević J D, Sredanović S A. 2011. Fatty acid composition of various soybean products. Food & Feed Research, 37, 65–70.

Jiang B, Li M, Cheng Y, Cai Z, Ma Q, Jiang Z, Ma R, Xia Q, Zhang G, Nian H. 2019. Genetic mapping of powdery mildew resistance genes in soybean by high-throughput genome-wide sequencing. Theoretical and Applied Genetics, 132, 1833–1845.

Kanobe C, Mccarville M T, O’Neal M E, Tylka G L, Macintosh G C. 2015. Soybean aphid infestation induces changes in fatty acid metabolism in soybean. PLoS ONE, 10, e145660.

Kim H K, Im M, Choung M. 2008. Analysis of quantitative trait loci (QTLs) for unsaturated fatty acid contents in soybean seed using recombinant inbred lines. Journal of Life Science, 18, 1665–1670.

Kim M Y, Van K, Lestari P, Moon J K, Lee S H. 2005. SNP identification and SNAP marker development for a GmNARK gene controlling supernodulation in soybean. Theoretical and Applied Genetics, 110, 1003–1010.

Kinney A J, Knowlton S. 1998. Designer oils: The high oleic acid soybean. In: Roller S, Harlander S, eds., Genetic Modification in the Food Industry: A Strategy for Food Quality Improvement. Springer US, Boston, MA. pp. 193–213.

Lee Y, Jeong N, Kim J H, Lee K, Kim K, Pirani A, Ha B, Kang S, Park B, Moon J, Kim N, Jeong S. 2015. Development, validation and genetic analysis of a large soybean SNP genotyping array. The Plant Journal, 81, 625–636.

Li H, Zhao T, Wang Y, Yu D, Chen S, Zhou R, Gai J. 2011. Genetic structure composed of additive QTL, epistatic QTL pairs and collective unmapped minor QTL conferring oil content and fatty acid components of soybeans. Euphytica, 182, 117–132.

Li Y H, Reif J C, Hong H L, Li H H, Liu Z X, Ma Y S, Li J, Tian Y, Li Y F, Li W B, Qiu L J. 2018. Genome-wide association mapping of QTL underlying seed oil and protein contents of a diverse panel of soybean accessions. Plant Science, 266, 95–101.

Mansur L M, Orf J H, Chase K D, Jarvik T, Cregan P B, Lark K G. 1996. Genetic mapping of agronomic traits using recombinant inbred lines of soybean. Crop Science, 36, 1327–1336.

Mao X, Chen W, Huyan Z, Sherazi S, Yu X. 2020. Impact of linolenic acid on oxidative stability of rapeseed oils. Journal of Food Science and Technology (Mysore), 57, 3184–3192.

Monteros M J, Burton J W, Boerma H R. 2008. Molecular mapping and confirmation of QTLs associated with oleic acid content in N00-3350 soybean. Crop Science, 48, 2223–2234.

Moongkanna J, Nakasathien S, Novitzky W P, Kwanyuen P, Sinchaisri P, Srinives P. 2011. SSR markers linking to seed traits and total oil content in soybean. Thai Journal of Agricultural Science, 44, 233–241.

Nguyen Q T, Kisiala A, Andreas P, Neil E R, Narine S. 2016. Soybean seed development: Fatty acid and phytohormone metabolism and their interactions. Current Genomics, 17, 241–260.

O’Brien R D. 1995. Chapter 20 - Soybean oil products utilization: Shortenings. In: Erickson D R, ed., Practical Handbook of Soybean Processing and Utilization. AOCS Press, United Soybean Board, England. pp. 363–379.

Okuley J, Lightner J, Feldmann K, Yadav N, Lark E, Browse J. 1994. Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell, 6, 147–158.

Oliva M L, Shannon J G, Sleper D A, Ellersieck M R, Cardinal A J, Paris R L, Lee J. 2006. Stability of fatty acid profile in soybean genotypes with modified seed oil composition. Crop Science, 46, 2069–2075.

Otyama P I, Chamberlin K, Ozias-Akins P, Graham M A, Cannon E K S, Cannon S B, Macdonald G E, Anglin N L. 2022. Genome-wide approaches delineate the additive, epistatic, and pleiotropic nature of variants controlling fatty acid composition in peanut (Arachis hypogaea L.). G3 Genes|Genomes|Genetics, 12, jkab382.

Panthee D R, Pantalone V R, Saxton A M. 2006. Modifier QTL for fatty acid composition in soybean oil. Euphytica, 152, 67–73.

Parker P G, Snow A A, Schug M D, Booton G C, Fuerst P A. 1998. What molecules can tell us about populations: choosing and using a molecular marker. Ecology, 79, 361–382.

Pathan S M, Vuong T D, Clark K M, Lee J, Shannon J G, Roberts C A, Ellersieck M R, Burton J W, Cregan P B, Hyten D L, Nguyen H T, Sleper D A. 2013. Genetic mapping and confirmation of quantitative trait loci for seed protein and oil contents and seed weight in soybean. Crop Science, 53, 765–774.

Peng L, Qian L, Wang M, Liu W, Song X, Cheng H, Yuan F, Zhao M. 2021. Comparative transcriptome analysis during seeds development between two soybean cultivars. PeerJ, 9, e10772.

Pham A, Lee J, Shannon J G, Bilyeu K D. 2010. Mutant alleles of FAD2-1A and FAD2-1B combine to produce soybeans with the high oleic acid seed oil trait. BMC Plant Biology, 10, 195.

Pham A, Lee J, Shannon J G, Bilyeu K D. 2011. A novel FAD2-1A allele in a soybean plant introduction offers an alternate means to produce soybean seed oil with 85% oleic acid content. Theoretical and Applied Genetics, 123, 793–802.

Pham A T, Shannon J G, Bilyeu K D. 2012. Combinations of mutant FAD2 and FAD3 genes to produce high oleic acid and low linolenic acid soybean oil. Theoretical and Applied Genetics, 125, 503–515.

Priolli R H G, Campos J B, Stabellini N S, Pinheiro J B, Vello N A. 2015. Association mapping of oil content and fatty acid components in soybean. Euphytica, 203, 83–96.

Priolli R H G, Carvalho C R L, Bajay M M, Pinheiro J B, Vello N A. 2019. Genome analysis to identify SNPs associated with oil content and fatty acid components in soybean. Euphytica, 215, 54.

Qi Z, Wu Q, Han X, Sun Y, Du X, Liu C, Jiang H, Hu G, Chen Q. 2011. Soybean oil content QTL mapping and integrating with meta-analysis method for mining genes. Euphytica, 179, 499–514.

Rahman S M M, Kinoshita T, Anai T, Takagi Y. 2001. Combining ability in loci for high oleic and low linolenic acids in soybean. Crop Science, 41, 26–29.

Ravelombola W, Qin J, Shi A, Song Q, Yuan J, Wang F, Chen P, Yan L, Feng Y, Zhao T, Meng Y, Guan K, Yang C, Zhang M. 2021. Genome-wide association study and genomic selection for yield and related traits in soybean. PLoS ONE, 16, e255761.

Roesler K, Shen B, Bermudez E, Li C, Hunt J, Damude H G, Ripp K G, Everard J D, Booth J R A, Castaneda L, Feng L, Meyer K. 2016. An improved variant of soybean type I diacylglycerol acyltransferase increases the oil content and decreases the soluble carbohydrate content of soybeans. Plant Physiology, 171, 878–893.

Rong H, Yang W, Xie T, Wang Y, Wang X, Jiang J, Wang Y. 2022. Transcriptional profiling between yellow- and black-seeded Brassica napus reveals molecular modulations on flavonoid and fatty acid content. Journal of Integrative Agriculture, 21, 2211–2226.

Rubel A C, Rinne R W, Canvin D T. 1972. Protein, oil, and fatty acid in developing soybean seeds. Crop Science, 12, 739–741.

Schlueter J A, Vasylenko-Sanders I F, Deshpande S, Yi J, Siegfried M, Roe B A, Schlueter S D, Scheffler B E, Shoemaker R C. 2007. The FAD2 gene family of soybean: Insights into the structural and functional divergence of a paleopolyploid genome. Crop Science, 47, 14–26.

Schnebly S R, Fehr W R. 1993. Effect of years and planting dates on fatty acid composition of soybean genotypes. Crop Science, 33, 716–719.

Sehgal D, Singh R, Rajpal V R. 2016. Quantitative trait loci mapping in plants: Concepts and approaches. In: Rajpal V R, Rao S R, Raina S N, eds., Molecular Breeding for Sustainable Crop Improvement. vol. 2. Springer International Publishing, Cham. pp. 31–59.

Semagn K, Bjornstad A S, Ndjiondjop M. 2006. An overview of molecular marker methods for plants. African Journal of Biotechnology, 5, 2540–2568.

Sharma M, Gupta S K, Mondal A K. 2021. Production and trade of major world oil crops. In: Gupta S K, ed., Technological Innovations in Major World Oil Crops. vol. 1: Breeding. Springer New York, New York, NY. pp. 1–15.

Shen Y, Liu J, Geng H, Zhang J, Liu Y, Zhang H, Xing S, Du J, Ma S, Tian Z. 2018. De novo assembly of a Chinese soybean genome. Science China Life Sciences, 61, 871–884.

Shi Z, Liu S, Noe J, Arelli P, Meksem K, Li Z. 2015. SNP identification and marker assay development for high-throughput selection of soybean cyst nematode resistance. BMC Genomics, 16, 314.

Talukdar A, Shivakumar M, Chandra S. 2019. Recent advances in breeding for modified fatty acid profile in soybean oil. In: Qureshi A M I, Dar Z A, Wani S H, eds., Quality Breeding in Field Crops. Springer International Publishing, Cham. pp. 159–172.

Torabi S, Sukumaran A, Dhaubhadel S, Johnson S E, Lafayette P, Parrott W A, Rajcan I, Eskandari M. 2021. Effects of type I Diacylglycerol O-acyltransferase (DGAT1) genes on soybean (Glycine max L.) Seed composition. Scientific Reports, 11, 2556.

Van K, Mchale L K. 2017. Meta-analyses of QTLs associated with protein and oil contents and compositions in soybean [Glycine max (L.) Merr.] seed. International Journal of Molecular Sciences, 18, 1180.

Vieira C C, Chen P. 2021. The numbers game of soybean breeding in the United States. Crop Breeding and Applied Biotechnology, 21, e387521S10.

Vollmann J, Rajcan I. 2010. Oil crop breeding and genetics. In: Vollmann J, Rajcan I, eds., Oil Crops. Springer New York, New York, NY. pp. 1–30.

De Vries B D, Fehr W R, Welke G A, Dewey R E. 2011. Molecular characterization of the mutant fap3 (A22) allele for reduced palmitate concentration in soybean. Crop Science, 51, 1611–1616.

Wang F, Das P, Pal N, Bhawal R, Zhang S, Bhattacharyya M K. 2022. A phosphoproteomics study of the soybean root necrosis 1 mutant revealed type II metacaspases involved in cell death pathway. Frontiers in Plant Science, 13, 882561.

Wang H, Jia J, Cai Z, Duan M, Jiang Z, Xia Q, Ma Q, Lian T, Nian H. 2022. Identification of quantitative trait loci (QTLs) and candidate genes of seed iron and zinc content in soybean [Glycine max (L.) Merr.]. BMC Genomics, 23, 146.

Wang X, Jiang G, Green M, Scott R A, Hyten D L, Cregan P B. 2012. Quantitative trait locus analysis of saturated fatty acids in a population of recombinant inbred lines of soybean. Molecular Breeding, 30, 1163–1179.

Wilcox J R, Cavins J F. 1992. Normal and low linolenic acid soybean strains: response to planting date. Crop Science, 32, 1248–1251.

Winter P, Kahl G. 1995. Molecular marker technologies for plant improvement. World Journal of Microbiology and Biotechnology, 11, 438–448.

Wolf R B, Cavins J F, Kleiman R, Black L T. 1982. Effect of temperature on soybean seed constituents: Oil, protein, moisture, fatty acids, amino acids and sugars. Journal of the American Oil Chemists’ Society, 59, 230–232.

Wu X, Ren C, Joshi T, Vuong T, Xu D, Nguyen H T. 2010. SNP discovery by high-throughput sequencing in soybean. BMC Genomics, 11, 469.

Wulfert S, Schilasky S, Krueger S. 2020. Transcriptional and biochemical characterization of cytosolic pyruvate kinases in Arabidopsis thaliana. Plants-Basel, 9, 353.

Xie D, Han Y, Zeng Y, Chang W, Teng W, Li W. 2012. SSR and SNP-related QTL underlying linolenic acid and other fatty acid contents in soybean seeds across multiple environments. Molecular Breeding, 30, 169–179.

Xie J, Cao Q, Wang W, Zhang H, Deng B. 2023. Understanding changes in volatile compounds and fatty acids of Jincheng orange peel oil at different growth stages using GC–MS. Journal of Integrative Agriculture, 22, 2282–2294.

Yang S, Miao L, He J, Zhang K, Li Y, Gai J. 2019. Dynamic transcriptome changes related to oil accumulation in developing soybean seeds. International Journal of Molecular Sciences, 20, 2202.

Yuan C, Bloch K. 1961. Conversion of oleic acid to linoleic acid. Journal of Biological Chemistry, 236, 1277–1279.

Zhang B, Xia P, Yu H, Li W, Chai W, Liang Z. 2021. Based on the whole genome clarified the evolution and expression process of fatty acid desaturase genes in three soybeans. International Journal of Biological Macromolecules, 182, 1966–1980.

Zhang G, Bahn S C, Wang G, Zhang Y, Chen B, Zhang Y, Wang X, Zhao J. 2019. PLD α1-knockdown soybean seeds display higher unsaturated glycerolipid contents and seed vigor in high temperature and humidity environments. Biotechnology for Biofuels, 12, 9.

Zhang H, Goettel W, Song Q, Jiang H, Hu Z, Wang M L, An Y C. 2020. Selection of GmSWEET39 for oil and protein improvement in soybean. PLoS Genetics, 16, e1009114.

Zhang J, Wang X, Lu Y, Bhusal S J, Song Q, Cregan P B, Yen Y, Brown M, Jiang G L. 2018. Genome-wide scan for seed composition provides insights into soybean quality improvement and the impacts of domestication and breeding. Molecular Plant, 11, 460–472.

Zhong Y, Wen K, Li X, Wang S, Li S, Zeng Y, Cheng Y, Ma Q, Nian H. 2023. Identification and mapping of QTLs for sulfur-containing amino acids in soybean (Glycine max L.). Journal of Agricultural and Food Chemistry, 71, 398–410.

Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, Yu Y, Shu L, Zhao Y, Ma Y, Fang C, Shen Y, Liu T, Li C, Li Q, Wu M, Wang M, Wu Y, Dong Y, Wan W, et al. 2015. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nature Biotechnology, 33, 408–414.

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