Abstract
Soybean is an utterly important crop for high-quality meal protein and vegetative oil. Soybean seed protein content has become a key factor in nutrients for livestock feed as well as human dietary consumption. Genetic improvement of soybean seed protein is highly desired to meet the demands of rapidly growing world population. Molecular mapping and genomic analysis in soybean have identified many quantitative trait loci (QTL) underlying seed protein content control. Exploring the mechanisms of seed storage protein regulation will be helpful to achieve the improvement of protein content. However, the practice of breeding higher protein soybean is challenging because soybean seed protein is negatively correlated with seed oil content and yield. To overcome the limitation of such inverse relationship, deeper insights into the property and genetic control of seed protein are required. Recent advances of soybean genomics have strongly enhanced the understandings for molecular mechanisms of soybean with better seed quality. Here, we review the research progress in the genetic characteristics of soybean storage protein, and up-to-date advances of molecular mappings and genomics of soybean protein. The key factors underlying the mechanisms of the negative correlation between protein and oil in soybean seeds are elaborated. We also briefly discuss the future prospects of breaking the bottleneck of the negative correlation to develop high protein soybean without penalty of oil and yield.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Adachi M, Kanamori J, Masuda T, Yagasaki K, Kitamura K, Mikami B, Utsumi S (2003) Crystal structure of soybean 11S globulin: glycinin A3B4 homohexamer. Proc Natl Acad of Sci U S A 100(12):7395–7400. https://doi.org/10.1073/pnas.0832158100
Akond M, Liu S, Boney M, Kantartzi SK, Meksem K, Bellaloui N, Lightfoot DA, Kassem MA (2014) Identification of quantitative trait loci (QTL) underlying protein, oil, and five major fatty acids’ contents in soybean. Am J of Plant Sci 05(01):158–167. https://doi.org/10.4236/ajps.2014.51021
Al Amin N, Ahmad N, Wu N, Pu X, Ma T, Du Y, Bo X, Wang N, Sharif R, Wang P (2019) CRISPR-Cas9 mediated targeted disruption of FAD2-2 microsomal omega-6 desaturase in soybean (Glycine max. L). BMC Biotechnol 19(1):9. https://doi.org/10.1186/s12896-019-0501-2
Allen DK, Young JD (2013) Carbon and nitrogen provisions alter the metabolic flux in developing soybean embryos. Plant Physiol 161(3):1458–1475. https://doi.org/10.1104/pp.112.203299
Allen DK, Ohlrogge JB, Shachar-Hill Y (2009) The role of light in soybean seed filling metabolism. Plant J 58(2):220–234. https://doi.org/10.1111/j.1365-313X.2008.03771.x
Alonso AP, Goffman FD, Ohlrogge JB, Shachar-Hill Y (2007) Carbon conversion efficiency and central metabolic fluxes in developing sunflower (Helianthus annuus L.) embryos. Plant J 52(2):296–308. https://doi.org/10.1111/j.1365-313X.2007.03235.x
Anai T (2012) Potential of a mutant-based reverse genetic approach for functional genomics and molecular breeding in soybean. Breed Sci 61(5):462–467. https://doi.org/10.1270/jsbbs.61.462
Anderson EJ, Ali ML, Beavis WD, Chen P, Clemente TE, Diers BW, Graef GL, Grassini P, Hyten DL, McHale LK, Nelson RL, Parrott WA, Patil GB, Stupar RM, Tilmon KJ (2019) Soybean [Glycine max (L.) Merr.] breeding: history, improvement, production and future opportunities. In: Advances In Plant Breeding Strategies: Legumes. Springer, pp 431–516. https://doi.org/10.1007/978-3-030-23400-3_12
Asakura T, Tamura T, Terauchi K, Narikawa T, Yagasaki K, Ishimaru Y, Abe K (2012) Global gene expression profiles in developing soybean seeds. Plant Physiol Biochem 52:147–153. https://doi.org/10.1016/j.plaphy.2011.12.007
Bai M, Yuan J, Kuang H, Gong P, Li S, Zhang Z, Liu B, Sun J, Yang M, Yang L, Wang D, Song S, Guan Y (2020) Generation of a multiplex mutagenesis population via pooled CRISPR-Cas9 in soya bean. Plant Biotechnol J 18(3):721–731. https://doi.org/10.1111/pbi.13239
Bandillo N, Jarquin D, Song Q, Nelson R, Cregan P, Specht J, Lorenz A (2015) A population structure and genome-wide association analysis on the USDA soybean germplasm collection. Plant. Genome 8:20040024. https://doi.org/10.3835/plantgenome2015.04.0024
Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L (2008) Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. Arabidopsis Book 6:e0113. https://doi.org/10.1199/tab.0113
Beilinson V, Chen Z, Shoemaker C, Fischer L, Goldberg B, Nielsen C (2002) Genomic organization of glycinin genes in soybean. Theor Appl Genet 104(6-7):1132–1140. https://doi.org/10.1007/s00122-002-0884-6
Bennett JO, Krishnan AH, Wiebold WJ, Krishnan HB (2003) Positional effect on protein and oil content and composition of soybeans. J Agric Food Chem 51(23):6882–6886. https://doi.org/10.1021/jf034371l
Bolon YT, Joseph B, Cannon SB, Graham MA, Diers BW, Farmer AD, May GD, Muehlbauer GJ, Specht JE, Tu ZJ, Weeks N, Xu WW, Shoemaker RC, Vance CP (2010) Complementary genetic and genomic approaches help characterize the linkage group I seed protein QTL in soybean. BMC Plant Biol 10:41. https://doi.org/10.1186/1471-2229-10-41
Bolon YT, Haun WJ, Xu WW, Grant D, Stacey MG, Nelson RT, Gerhardt DJ, Jeddeloh JA, Stacey G, Muehlbauer GJ, Orf JH, Naeve SL, Stupar RM, Vance CP (2011) Phenotypic and genomic analyses of a fast neutron mutant population resource in soybean. Plant Physiol 156(1):240–253. https://doi.org/10.1104/pp.110.170811
Bolon YT, Stec AO, Michno JM, Roessler J, Bhaskar PB, Ries L, Dobbels AA, Campbell BW, Young NP, Anderson JE, Grant DM, Orf JH, Naeve SL, Muehlbauer GJ, Vance CP, Stupar RM (2014) Genome resilience and prevalence of segmental duplications following fast neutron irradiation of soybean. Genetics 198(3):967–981. https://doi.org/10.1534/genetics.114.170340
Borek S, Pukacka S, Michalski K, Ratajczak L (2009) Lipid and protein accumulation in developing seeds of three lupine species: Lupinus luteus L., Lupinus albus L., and Lupinus mutabilis Sweet. J Exp Bot 60(12):3453–3466. https://doi.org/10.1093/jxb/erp186
Borisjuk L, Nguyen TH, Neuberger T, Rutten T, Tschiersch H, Claus B, Feussner I, Webb AG, Jakob P, Weber H, Wobus U, Rolletschek H (2005) Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. New Phytol 167(3):761–776. https://doi.org/10.1111/j.1469-8137.2005.01474.x
Bray EA, Beachy RN (1985) Regulation by ABA of beta-conglycinin expression in cultured developing soybean cotyledons. Plant Physiol 79(3):746–750. https://doi.org/10.1104/pp.79.3.746
Brim CA, Burton JW (1979) Recurrent selection in soybeans. II. Selection for increased percent protein in seeds 1. Crop Sci 19(4):494–498. https://doi.org/10.2135/cropsci1979.0011183X001900040016x
Brummer EC, Graef GL, Orf J, Wilcox JR, Shoemaker RC (1997) Mapping QTL for seed protein and oil content in eight soybean populations. Crop Sci 37(2):370–378. https://doi.org/10.2135/cropsci1997.0011183X003700020011x
Brzostowski LF, Pruski TI, Specht JE, Diers BW (2017) Impact of seed protein alleles from three soybean sources on seed composition and agronomic traits. Theor Appl Genet 130(11):2315–2326. https://doi.org/10.1007/s00122-017-2961-x
Burton JW, Brim CA (1981) Recurrent selection in soybeans. III. Selection for increased percent oil in seeds. Crop Sci 21(1):31–34. https://doi.org/10.2135/cropsci1981.0011183X002100010009x
Campbell BW, Stupar RM (2016) Soybean (Glycine max) mutant and germplasm resources: current status and future prospects. Curr Protoc Plant Biol 1(2):307–327. https://doi.org/10.1002/cppb.20015
Cao Y, Li S, Wang Z, Chang F, Kong J, Gai J, Zhao T (2017) Identification of major quantitative trait loci for seed oil content in soybeans by combining linkage and genome-wide association mapping. Front Plant Sci 8:1222. https://doi.org/10.3389/fpls.2017.01222
Carter AM, Tegeder M (2016) Increasing nitrogen fixation and seed development in soybean requires complex adjustments of nodule nitrogen metabolism and partitioning processes. Curr Biol 26(15):2044–2051. https://doi.org/10.1016/j.cub.2016.06.003
Carter TE, Hymowitz T, Nelson RL. (2004). Biogeography, Local Adaptation, Vavilov, and Genetic Diversity in Soybean. In: Werner, D. (eds) Biological Resources and Migration. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-06083-4_5
Chaudhary J, Patil GB, Sonah H, Deshmukh RK, Vuong TD, Valliyodan B, Nguyen HT (2015) Expanding omics resources for improvement of soybean seed composition traits. Front Plant Sci 6:1021. https://doi.org/10.3389/fpls.2015.01021
Chauffour F, Bailly M, Perreau F, Cueff G, Suzuki H, Collet B, Frey A, Clement G, Soubigou-Taconnat L, Balliau T, Krieger-Liszkay A, Rajjou L, Marion-Poll A (2019) Multi-omics analysis reveals sequential roles for ABA during seed maturation. Plant Physiol 180(2):1198–1218. https://doi.org/10.1104/pp.19.00338
Chen Q-s, Zhang Z-c, Liu C-y, Xin D-w, Qiu H-m, Shan D-p, C-y S, Hu G-h (2007) QTL analysis of major agronomic traits in soybean. Agri Sci China 6(4):399–405. https://doi.org/10.1016/S1671-2927(07)60062-5
Chen K, Li G-J, Bressan RA, Song C-P, Zhu J-K, Zhao Y (2020) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62(1):25–54. https://doi.org/10.1111/jipb.12899
Cheng L, Yuan HY, Ren R, Zhao SQ, Han YP, Zhou QY, Ke DX, Wang YX, Wang L (2016) Genome-wide identification, classification, and expression analysis of amino acid transporter gene family in Glycine max. Front Plant Sci 7:515. https://doi.org/10.3389/fpls.2016.00515
Chung J, Babka HL, Graef GL, Staswick PE, Lee DJ, Cregan PB, Shoemaker RC, Specht JE (2003) The seed protein, oil, and yield QTL on soybean linkage group I. Crop Sci 43(3):1053–1067. https://doi.org/10.2135/cropsci2003.1053
Clemente TE, Cahoon EB (2009) Soybean oil: genetic approaches for modification of functionality and total content. Plant Physiol 151(3):1030–1040. https://doi.org/10.1104/pp.109.146282
Cober ER, Voldeng HD (2000) Developing high-protein, high-yield soybean populations and lines. Crop Sci 40:39–42
Cooper JL, Till BJ, Laport RG, Darlow MC, Kleffner JM, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, Bilyeu KD, Meksem K, Comai L, Henikoff S (2008) TILLING to detect induced mutations in soybean. BMC Plant Biol 8:9. https://doi.org/10.1186/1471-2229-8-9
Csanádi G, Vollmann J, Stift G, Lelley T (2001) Seed quality QTLs identified in a molecular map of early maturing soybean. Theor Appl Genet 103(6):912–919. https://doi.org/10.1007/s001220100621
Delisle AJ, Crouch ML (1989) Seed storage protein transcription and mRNA levels in Brassica napus during development and in response to exogenous abscisic acid. Plant Physiol 91(2):617–623. https://doi.org/10.1104/pp.91.2.617
Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JG, McCourt P, Samuel MA (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proc Natl Acad Sci U S A 110(40):E3888–E3894. https://doi.org/10.1073/pnas.1308114110
Derbyshire E, Wright DJ, Boulter D (1976) Legumin and vicilin, storage proteins of legume seeds. Phytochemistry 15(1):3–24. https://doi.org/10.1016/S0031-9422(00)89046-9
Dierking EC, Bilyeu KD (2009) New sources of soybean seed meal and oil composition traits identified through TILLING. BMC Plant Biol 9:89. https://doi.org/10.1186/1471-2229-9-89
Diers BW, Keim P, Fehr WR, Shoemaker RC (1992) RFLP analysis of soybean seed protein and oil content. Theor Appl Genet 83(5):608–612. https://doi.org/10.1007/bf00226905
Dobbels AA, Michno JM, Campbell BW, Virdi KS, Stec AO, Muehlbauer GJ, Naeve SL, Stupar RM (2017) An induced chromosomal translocation in soybean disrupts a KASI ortholog and is associated with a high-sucrose and low-oil seed phenotype. G3 7(4):1215–1223. https://doi.org/10.1534/g3.116.038596
Dornbos DL, Mullen RE (1992) Soybean seed protein and oil contents and fatty acid composition adjustments by drought and temperature. J Am Oil Chem Soc 69(3):228–231. https://doi.org/10.1007/BF02635891
Duan Z, Zhang M, Zhang Z, Liang S, Fan L, Yang X, Yuan Y, Pan Y, Zhou G, Liu S, Tian Z (2022) Natural allelic variation of GmST05 controlling seed size and quality in soybean. Plant Biotechnol J 20(9):1807–1818. https://doi.org/10.1111/pbi.13865
Eisenberg AJ, Mascarenhas JP (1985) Abscisic acid and the regulation of synthesis of specific seed proteins and their messenger RNAs during culture of soybean embryos. Planta 166(4):505–514. https://doi.org/10.1007/bf00391275
Eskandari M, Cober ER, Rajcan I (2013) 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. Theor Appl Genet 126(2):483–495. https://doi.org/10.1007/s00122-012-1995-3
Fang C, Ma Y, Wu S, Liu Z, Wang Z, Yang R, Hu G, Zhou Z, Yu H, Zhang M, Pan Y, Zhou G, Ren H, Du W, Yan H, Wang Y, Han D, Shen Y, Liu S et al (2017) Genome-wide association studies dissect the genetic networks underlying agronomical traits in soybean. Genome Biol 18(1):161. https://doi.org/10.1186/s13059-017-1289-9
Fasoula VA, Harris DK, Boerma HR (2004) Validation and designation of quantitative trait loci for seed protein, seed oil, and seed weight from two soybean populations. Crop Sci 44(4):1218–1225. https://doi.org/10.2135/cropsci2004.1218
Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23(2):701–715. https://doi.org/10.1105/tpc.110.080788
Filho MM, Destro D, Miranda LA, Spinosa WA, Carrão-Panizzi MC, Montalván R (2001) Relationships among oil content, protein content and seed size in soybeans. Braz Arch Biol Technol 44:23–32
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45. https://doi.org/10.1105/tpc.010441
Fischer RL, Goldberg RB (1982) Structure and flanking regions of soybean seed protein genes. Cell 29(2):651–660. https://doi.org/10.1016/0092-8674(82)90181-7
Fliege CE, Ward RA, Vogel P, Nguyen H, Quach T, Guo M, Viana JPG, Dos Santos LB, Specht JE, Clemente TE, Hudson ME, Diers BW (2022) Fine mapping and cloning of the major seed protein quantitative trait loci on soybean chromosome 20. Plant J 110(1):114–128. https://doi.org/10.1111/tpj.15658
Gacek K, Bartkowiak-Broda I, Batley J (2018) Genetic and molecular regulation of seed storage proteins (SSPs) to improve protein nutritional value of oilseed rape (Brassica napus L.) seeds. Front Plant Sci 9:890. https://doi.org/10.3389/fpls.2018.00890
Gao C, Qi S, Liu K, Li D, Jin C, Li Z, Huang G, Hai J, Zhang M, Chen M (2016) MYC2, MYC3, and MYC4 function redundantly in seed storage protein accumulation in Arabidopsis. Plant Physiol Biochem 108:63–70. https://doi.org/10.1016/j.plaphy.2016.07.004
Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7(3):373–385. https://doi.org/10.1016/j.devcel.2004.06.017
Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4(10):1251–1261. https://doi.org/10.1105/tpc.4.10.1251
Goettel W, Zhang H, Li Y, Qiao Z, Jiang H, Hou D, Song Q, Pantalone VR, Song BH, Yu D, An YC (2022) POWR1 is a domestication gene pleiotropically regulating seed quality and yield in soybean. Nat Commun 13(1):3051. https://doi.org/10.1038/s41467-022-30314-7
Yazdi-Samadi B, Rinne RW, Seif RD (1977) Components of developing soybean seeds: oil, protein, sugars, starch, organic acids, and amino acids. Agron J 69(3):481–486. https://doi.org/10.2134/agronj1977.00021962006900030037x
Zhang H, Goettel W, Song Q, Jiang H, Hu Z, Wang ML, An YC (2020) Selection of GmSWEET39 for oil and protein improvement in soybean. PLoS Genet 16(11):e1009114. https://doi.org/10.1371/journal.pgen.1009114
Yoshino M, Kanazawa A, Tsutsumi K-i, Nakamura I, Takahashi K, Shimamoto Y (2002) Structural variation around the gene encoding the α subunit of soybean β-conglycinin and correlation with the expression of the α subunit. Breed Sci 52:285–292
Zhuang Y, Li X, Hu J, Xu R, Zhang D (2022) Expanding the gene pool for soybean improvement with its wild relatives. Abiotech 3(2):115–125. https://doi.org/10.1007/s42994-022-00072-7
Zhang S, Hao D, Zhang S, Zhang D, Wang H, Du H, Kan G, Yu D (2021) Genome-wide association mapping for protein, oil and water-soluble protein contents in soybean. Mol Genet Genomics 296(1):91–102. https://doi.org/10.1007/s00438-020-01704-7
Guo B, Sun L, Ren H, Sun R, Wei Z, Hong H, Luan X, JunWang WX, Xu D, Li W, Qiu L-J (2022) Soybean genetic resources contributing to sustainable protein production. Theor Appl Genet. https://doi.org/10.1007/s00122-022-04222-9
Gupta SK, Manjaya JG (2022) Advances in improvement of soybean seed composition traits using genetic, genomic and biotechnological approaches. Euphytica 218(7). https://doi.org/10.1007/s10681-022-03046-4
Gupta M, Bhaskar PB, Sriram S, Wang PH (2017) Integration of omics approaches to understand oil/protein content during seed development in oilseed crops. Plant Cell Rep 36(5):637–652. https://doi.org/10.1007/s00299-016-2064-1
Han Y, Teng W, Wang Y, Zhao X, Wu L, Li D, Li W (2015) Unconditional and conditional QTL underlying the genetic interrelationships between soybean seed isoflavone, and protein or oil contents. Plant Breeding 134(3):300–309. https://doi.org/10.1111/pbr.12259
Hanson WD (1991) Seed protein content and delivery of assimilates to soybean seed embryos. Crop Sci 31(6):1600. https://doi.org/10.2135/cropsci1991.0011183X003100060044x
Harada JJ, Barker SJ, Goldberg RB (1989) Soybean beta-conglycinin genes are clustered in several DNA regions and are regulated by transcriptional and posttranscriptional processes. Plant cell 1(4):415–425. https://doi.org/10.1105/tpc.1.4.415
Hayati R, Egli DB, Crafts-Brandner SJ (1995) Carbon and nitrogen supply during seed filling and leaf senescence in soybean. Crop Sci 35(4):1063. https://doi.org/10.2135/cropsci1995.0011183X003500040024x
Hayati R, Egli DB, Crafts-Brandner SJ (1996) Independence of nitrogen supply and seed growth in soybean: studies using an in vitro culture system. J Exp Bot 47(1):33–40. https://doi.org/10.1093/jxb/47.1.33
Herman EM, Larkins BA (1999) Protein storage bodies and vacuoles. Plant Cell 11(4):601–613. https://doi.org/10.1105/tpc.11.4.601
Hernandez-Sebastia C, Marsolais F, Saravitz C, Israel D, Dewey RE, Huber SC (2005) Free amino acid profiles suggest a possible role for asparagine in the control of storage-product accumulation in developing seeds of low- and high-protein soybean lines. J Exp Bot 56(417):1951–1963. https://doi.org/10.1093/jxb/eri191
Hoshino T, Watanabe S, Takagi Y, Anai T (2014) A novel GmFAD3-2a mutant allele developed through TILLING reduces α-linolenic acid content in soybean seed oil. Breed Sci 64(4):371–377. https://doi.org/10.1270/jsbbs.64.371
Hu Y, Zhou L, Yang Y, Zhang W, Chen Z, Li X, Qian Q, Kong F, Li Y, Liu X, Hou X (2021) The gibberellin signaling negative regulator RGA-LIKE3 promotes seed storage protein accumulation. Plant Physiol 185(4):1697–1707. https://doi.org/10.1093/plphys/kiaa114
Huang Y, Wang H, Zhu Y, Huang X, Li S, Wu X, Zhao Y, Bao Z, Qin L, Jin Y, Cui Y, Ma G, Xiao Q, Wang Q, Wang J, Yang X, Liu H, Lu X, Larkins BA, Wang W, Wu Y (2022) THP9 enhances seed protein content and nitrogen-use efficiency in maize. Nature 16:1–9. https://doi.org/10.1038/s41586-022-05441-2
Huber SC, Li K, Nelson R, Ulanov A, DeMuro CM, Baxter I (2016) Canopy position has a profound effect on soybean seed composition. PeerJ 4:e2452. https://doi.org/10.7717/peerj.2452
Hwang E-Y, Song Q, Jia G, Specht JE, Hyten DL, Costa J, Cregan PB (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15(1):1. https://doi.org/10.1186/1471-2164-15-1
Hymowitz T, Collins FI, Panczner J, Walker WM (1972) Relationship between the content of oil, protein, and sugar in soybean seed. Agron J 64(5):613–616. https://doi.org/10.2134/agronj1972.00021962006400050019x
Hyten DL, Pantalone VR, Sams CE, Saxton AM, Landau-Ellis D, Stefaniak TR, Schmidt ME (2004) Seed quality QTL in a prominent soybean population. Theor Appl Genet 109(3):552–561. https://doi.org/10.1007/s00122-004-1661-5
Imoto Y, Yamada T, Kitamura K, Kanazawa A (2008) Spatial and temporal control of transcription of the soybean beta-conglycinin alpha subunit gene is conferred by its proximal promoter region and accounts for the unequal distribution of the protein during embryogenesis. Genes Genet Syst 83(6):469–476. https://doi.org/10.1266/ggs.83.469
Islam N, Stupar RM, Qijian S, Luthria DL, Garrett W, Stec AO, Roessler J, Natarajan SS (2019) Genomic changes and biochemical alterations of seed protein and oil content in a subset of fast neutron induced soybean mutants. BMC Plant Biol 19(1):420. https://doi.org/10.1186/s12870-019-1981-x
Jarquin D, Specht J, Lorenz A (2016) Prospects of genomic prediction in the USDA soybean germplasm collection: historical data creates robust models for enhancing selection of accessions. G3 6(8):2329–2341. https://doi.org/10.1534/g3.116.031443
Jo L, Pelletier JM, Hsu S-W, Baden R, Goldberg RB, Harada JJ (2019) Combinatorial interactions of the LEC1 transcription factor specify diverse developmental programs during soybean seed development. Proc Natl Acad of Sci U S A 117(2):1223–1232. https://doi.org/10.1073/pnas.1918441117
Joaquim PIL, Molinari MDC, Marin SRR, Barbosa DA, Viana AJC, Rech EL, Henning FA, Nepomuceno AL, Mertz-Henning LM (2022) Nitrogen compounds transporters: candidates to increase the protein content in soybean seeds. J Plant Interact 17(1):309–318. https://doi.org/10.1080/17429145.2022.2039791
Johnson HW, Robinson HF, Comstock RE (1955) Genotypic and phenotypic correlations in soybeans and their implications in selection. Agron J 47(10):477–483. https://doi.org/10.2134/agronj1955.00021962004700100008x
Zhang D, Kan G, Hu Z, Cheng H, Zhang Y, Wang Q, Wang H, Yang Y, Li H, Hao D, Yu D (2014) Use of single nucleotide polymorphisms and haplotypes to identify genomic regions associated with protein content and water-soluble protein content in soybean. Theor Appl Genet 127(9):1905–1915. https://doi.org/10.1007/s00122-014-2348-1
Zhang D, Sun L, Li S, Wang W, Ding Y, Swarm SA, Li L, Wang X, Tang X, Zhang Z, Tian Z, Brown PJ, Cai C, Nelson RL, Ma J (2018a) Elevation of soybean seed oil content through selection for seed coat shininess. Nat Plants 4(1):30–35. https://doi.org/10.1038/s41477-017-0084-7
Jun T-H, Van K, Kim MY, Lee S-H, Walker DR (2007) Association analysis using SSR markers to find QTL for seed protein content in soybean. Euphytica 162(2):179–191. https://doi.org/10.1007/s10681-007-9491-6
Kabelka EA, Diers BW, Fehr WR, LeRoy AR, Baianu IC, You T, Neece DJ, Nelson RL (2004) Putative alleles for increased yield from soybean plant introductions. Crop Sci 44(3):784–791. https://doi.org/10.2135/cropsci2004.7840
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 et al (2015) Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol 33(4):408–414. https://doi.org/10.1038/nbt.3096
Kagawa H, Yamauchi F, Hirano H (1987) Soybean basic 7 S globulin represents a protein widely distributed in legume species. FEBS Lett 226(1):145–149. https://doi.org/10.1016/0014-5793(87)80568-9
Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005a) Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46(2):300–311. https://doi.org/10.1093/pcp/pci031
Kambhampati S, Aznar-Moreno JA, Bailey SR, Arp JJ, Chu KL, Bilyeu KD, Durrett TP, Allen DK (2021) Temporal changes in metabolism late in seed development affect biomass composition. Plant Physiol. https://doi.org/10.1093/plphys/kiab116
Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005b) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46(3):399–406. https://doi.org/10.1093/pcp/pci048
Kastoori Ramamurthy R, Jedlicka J, Graef GL, Waters BM (2014) Identification of new QTLs for seed mineral, cysteine, and methionine concentrations in soybean [Glycine max (L.) Merr]. Mol Breed 34(2):431–445. https://doi.org/10.1007/s11032-014-0045-z
Ke X, Xiao H, Peng Y, Wang J, Lv Q, Wang X (2022) Phosphoenolpyruvate reallocation links nitrogen fixation rates to root nodule energy state. Science 378(6623):971–977. https://doi.org/10.1126/science.abq8591
Kenworthy WJ, Brim CA (1979) Recurrent selection in soybeans. I. Seed yield. Crop Sci 19(3):315. https://doi.org/10.2135/cropsci1979.0011183X001900030009x
Kim H, Fujiwara T, Hayashi H, Chino M (1997) Effects of exogenous ABA application on sulfate and OAS concentrations, and on composition of seed storage proteins in in vitro cultured soybean immature cotyledons (Reprinted from Plant nutrition for sustainable food production and environment, 1997). Soil Sci Plant Nutr 43:1119–1123. https://doi.org/10.1080/00380768.1997.11863728
Kim MY, Lee S, Van K, Kim TH, Jeong SC, Choi IY, Kim DS, Lee YS, Park D, Ma J, Kim WY, Kim BC, Park S, Lee KA, Kim DH, Kim KH, Shin JH, Jang YE, Kim KD et al (2010) Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci U S A 107(51):22032–22037. https://doi.org/10.1073/pnas.1009526107
Kim M, Schultz S, Nelson RL, Diers BW (2016) Identification and fine mapping of a soybean seed protein QTL from PI 407788A on chromosome 15. Crop Sci 56(1):219–225. https://doi.org/10.2135/cropsci2015.06.0340
Kim MS, Lozano R, Kim JH, Bae DN, Kim ST, Park JH, Choi MS, Kim J, Ok HC, Park SK, Gore MA, Moon JK, Jeong SC (2021) The patterns of deleterious mutations during the domestication of soybean. Nat Commun 12(1):97. https://doi.org/10.1038/s41467-020-20337-3
Kofsky J, Zhang H, Song BH (2018) The untapped genetic reservoir: the past, current, and future applications of the wild soybean (Glycine soja). Front Plant Sci 9:949. https://doi.org/10.3389/fpls.2018.00949
Koley S, Chu KL, Mukherjee T, Morley SA, Klebanovych A, Czymmek KJ, Allen DK (2022) Metabolic synergy in Camelina reproductive tissues for seed development. Sci Adv 8(43):eabo7683. https://doi.org/10.1126/sciadv.abo7683
Krishnan HB (2001) Biochemistry and molecular biology of soybean seed storage proteins. J New Seeds 2(3):1–25. https://doi.org/10.1300/J153v02n03_01
Krishnan HB, Jez JM (2018) Review: the promise and limits for enhancing sulfur-containing amino acid content of soybean seed. Plant Sci 272:14–21. https://doi.org/10.1016/j.plantsci.2018.03.030
Kroj T, Savino G, Valon C, Giraudat J, Parcy F (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130(24):6065–6073. https://doi.org/10.1242/dev.00814
Lawrence MC, Izard T, Beuchat M, Blagrove RJ, Colman PM (1994) Structure of phaseolin at 2·2 Å resolution: implications for a common vicilin/legumin structure and the genetic engineering of seed storage proteins. J Mol Biol 238(5):748–776. https://doi.org/10.1006/jmbi.1994.1333
Lee SH, Bailey MA, Mian MA, Carter TE Jr, Shipe ER, Ashley DA, Parrott WA, Hussey RS, Boerma HR (1996) RFLP loci associated with soybean seed protein and oil content across populations and locations. Theor Appl Genet 93(5-6):649–657. https://doi.org/10.1007/bf00224058
Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci U S A 100(4):2152–2156. https://doi.org/10.1073/pnas.0437909100
Leffel RC (1989) Breeding soybeans for the economic values of seed oil and protein. J Prod Agric 2(4):338–343. https://doi.org/10.2134/jpa1989.0338
Leprince O, Pellizzaro A, Berriri S, Buitink J (2017) Late seed maturation: drying without dying. J Exp Bot 68(4):827–841. https://doi.org/10.1093/jxb/erw363
Lestari P, Van K, Lee J, Kang YJ, Lee SH (2013) Gene divergence of homeologous regions associated with a major seed protein content QTL in soybean. Front Plant Sci 4:176. https://doi.org/10.3389/fpls.2013.00176
Li L, Wurtele ES (2015) The QQS orphan gene of Arabidopsis modulates carbon and nitrogen allocation in soybean. Plant Biotechnol J 13(2):177–187. https://doi.org/10.1111/pbi.12238
Li Y-h, Zhou G, Ma J, Jiang W, Jin L-g, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, Zhang S-s, Zuo Q, Shi X-h, Li Y-f, Zhang W-k, Hu Y, Kong G, Hong H-l, Tan B, Song J, Liu Z-x, Wang Y, Ruan H, Yeung CKL, Liu J, Wang H, Zhang L-j, Guan R-x, Wang K-j, Li W-b, Chen S-y, Chang R-z, Jiang Z, Jackson SA, Li R, Qiu L-j (2014) De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol 32(10):1045–1052. https://doi.org/10.1038/nbt.2979
Li L, Zheng W, Zhu Y, Ye H, Tang B, Arendsee ZW, Jones D, Li R, Ortiz D, Zhao X, Du C, Nettleton D, Scott MP, Salas-Fernandez MG, Yin Y, Wurtele ES (2015) QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions. Proc Natl Acad Sci U S A 112(47):14734–14739. https://doi.org/10.1073/pnas.1514670112
Li YH, Reif JC, Hong HL, Li HH, Liu ZX, Ma YS, Li J, Tian Y, Li YF, Li WB, Qiu LJ (2018) Genome-wide association mapping of QTL underlying seed oil and protein contents of a diverse panel of soybean accessions. Plant Sci 266:95–101. https://doi.org/10.1016/j.plantsci.2017.04.013
Li C, Nguyen V, Liu J, Fu W, Chen C, Yu K, Cui Y (2019) Mutagenesis of seed storage protein genes in soybean using CRISPR/Cas9. BMC Res Notes 12(1):176. https://doi.org/10.1186/s13104-019-4207-2
Li J, Zhang Y, Ma R, Huang W, Hou J, Fang C, Wang L, Yuan Z, Sun Q, Dong X, Hou Y, Wang Y, Kong F, Sun L (2022) Identification of ST1 reveals a selection involving hitchhiking of seed morphology and oil content during soybean domestication. Plant Biotechnol J 20(6):1110–1121. https://doi.org/10.1111/pbi.13791
Liang H-z, Yu Y-l, Wang S-f, Lian Y, Wang T-f, Wei Y-l, Gong P-t, Liu X-y, Fang X-j, Zhang M-c (2010) QTL mapping of isoflavone, oil and protein contents in soybean (Glycine max L. Merr.). Agri Sci in China 9(8):1108–1116. https://doi.org/10.1016/S1671-2927(09)60197-8
Liu S, Wang D, Mei Y, Xia T, Xu W, Zhang Y, You X, Zhang X, Li L, Wang NN (2020a) Overexpression of GmAAP6a enhances tolerance to low nitrogen and improves seed nitrogen status by optimizing amino acid partitioning in soybean. Plant Biotechnol J 18(8):1749–1762. https://doi.org/10.1111/pbi.13338
Liu S, Zhang M, Feng F, Tian Z (2020b) Toward a “Green Revolution” for soybean. Mol Plant 13(5):688–697. https://doi.org/10.1016/j.molp.2020.03.002
Liu Y, Du H, Li P, Shen Y, Peng H, Liu S, Zhou GA, Zhang H, Liu Z, Shi M, Huang X, Li Y, Zhang M, Wang Z, Zhu B, Han B, Liang C, Tian Z (2020c) Pan-genome of wild and cultivated soybeans. Cell 182(1):162–176 e113. https://doi.org/10.1016/j.cell.2020.05.023
Lu C, Napier JA, Clemente TE, Cahoon EB (2011) New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications. Curr Opin Biotechnol 22(2):252–259. https://doi.org/10.1016/j.copbio.2010.11.006
Lu W, Wen Z, Li H, Yuan D, Li J, Zhang H, Huang Z, Cui S, Du W (2013) Identification of the quantitative trait loci (QTL) underlying water soluble protein content in soybean. Theor Appl Genet 126(2):425–433. https://doi.org/10.1007/s00122-012-1990-8
Luerssen H, Kirik V, Herrmann P, Miséra S (1998) FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15(6):755–764. https://doi.org/10.1046/j.1365-313x.1998.00259.x
Manan S, Ahmad MZ, Zhang G, Chen B, Haq BU, Yang J, Zhao J (2017) Soybean LEC2 regulates subsets of genes involved in controlling the biosynthesis and catabolism of seed storage substances and seed development. Front Plant Sci 8:1604. https://doi.org/10.3389/fpls.2017.01604
Mao T, Jiang Z, Han Y, Teng W, Zhao X, Li W, Morris B (2013) Identification of quantitative trait loci underlying seed protein and oil contents of soybean across multi-genetic backgrounds and environments. Plant Breed 132(6):630–641. https://doi.org/10.1111/pbr.12091
Maruyama N, Mun LC, Tatsuhara M, Sawada M, Ishimoto M, Utsumi S (2006) Multiple vacuolar sorting determinants exist in soybean 11S globulin. Plant Cell 18(5):1253–1273. https://doi.org/10.1105/tpc.105.036376
Maruyama N, Matsuoka Y, Yokoyama K, Takagi K, Yamada T, Hasegawa H, Terakawa T, Ishimoto M (2018) A vacuolar sorting receptor-independent sorting mechanism for storage vacuoles in soybean seeds. Sci Rep 8(1):1108. https://doi.org/10.1038/s41598-017-18697-w
Matsuoka K, Neuhaus JM (1999) Cis-elements of protein transport to the plant vacuoles. J Exp Bot 50:165–174. https://doi.org/10.1093/jxb/50.331.165
Meinke DW, Chen J, Beachy RN (1981) Expression of storage-protein genes during soybean seed development. Planta 153(2):130–139. https://doi.org/10.1007/BF00384094
Meyer K, Stecca KL, Ewell-Hicks K, Allen SM, Everard JD (2012) Oil and protein accumulation in developing seeds is influenced by the expression of a cytosolic pyrophosphatase in Arabidopsis. Plant Physiol 159(3):1221–1234. https://doi.org/10.1104/pp.112.198309
Miao L, Yang S, Zhang K, He J, Wu C, Ren Y, Gai J, Li Y (2020) Natural variation and selection in GmSWEET39 affect soybean seed oil content. New Phytol 225(4):1651–1666. https://doi.org/10.1111/nph.16250
Müntz K (1998) Deposition of storage proteins. Plant Mol Biol 38(1-2):77–99
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol 56:165–185. https://doi.org/10.1146/annurev.arplant.56.032604.144046
Neuberger T, Sreenivasulu N, Rokitta M, Rolletschek H, Göbel C, Rutten T, Radchuk V, Feussner I, Wobus U, Jakob P, Webb A, Borisjuk L (2007) Quantitative imaging of oil storage in developing crop seeds. Plant Biotechnol J 6:31–45. https://doi.org/10.1111/j.1467-7652.2007.00294.x
Nichols DM, Glover KD, Carlson SR, Specht JE, Diers BW (2006) Fine mapping of a seed protein QTL on soybean linkage group I and its correlated effects on agronomic traits. Crop Sci 46(2):834–839. https://doi.org/10.2135/cropsci2005.05-0168
Nielsen NC, Dickinson CD, Cho TJ, Thanh VH, Scallon BJ, Fischer RL, Sims TL, Drews GN, Goldberg RB (1989) Characterization of the glycinin gene family in soybean. Plant Cell 1(3):313–328. https://doi.org/10.1105/tpc.1.3.313
Nishizawa K, Maruyama N, Satoh R, Fuchikami Y, Higasa T, Utsumi S (2003) A C-terminal sequence of soybean beta-conglycinin alpha’ subunit acts as a vacuolar sorting determinant in seed cells. Plant J 34(5):647–659. https://doi.org/10.1046/j.1365-313x.2003.01754.x
Nishizawa K, Maruyama N, Utsumi S (2006) The C-terminal region of alpha’ subunit of soybean beta-conglycinin contains two types of vacuolar sorting determinants. Plant Mol Biol 62(1-2):111–125. https://doi.org/10.1007/s11103-006-9007-0
Nonogaki H (2019) ABA responses during seed development and germination. In: Abscisic acid in plants. Advances in Botanical Research. Academic Press, pp 171–217. https://doi.org/10.1016/bs.abr.2019.04.005
Orf JH, Chase K, Jarvik T, Mansur LM, Cregan PB, Adler FR, Lark KG (1999) Genetics of soybean agronomic traits: I. Comparison of three related recombinant inbred populations. Crop Sci 39(6):1642–1651. https://doi.org/10.2135/cropsci1999.3961642x
Paek NC, Imsande J, Shoemaker RC, Shibles R (1997) Nutritional control of soybean seed storage protein. Crop Sci 37(2):498–503. https://doi.org/10.2135/cropsci1997.0011183X003700020031x
Palomeque L, Li-Jun L, Li W, Hedges B, Cober ER, Rajcan I (2009) QTL in mega-environments: II. Agronomic trait QTL co-localized with seed yield QTL detected in a population derived from a cross of high-yielding adapted x high-yielding exotic soybean lines. Theor Appl Genet 119(3):429–436. https://doi.org/10.1007/s00122-009-1048-8
Pandurangan S, Pajak A, Molnar SJ, Cober ER, Dhaubhadel S, Hernández-Sebastià C, Kaiser WM, Nelson RL, Huber SC, Marsolais F (2012) Relationship between asparagine metabolism and protein concentration in soybean seed. J Exp Bot 63(8):3173–3184. https://doi.org/10.1093/jxb/ers039
Panthee DR, Pantalone VR, West DR, Saxton AM, Sams CE (2005) Quantitative trait loci for seed protein and oil concentration, and seed size in soybean. Crop Sci 45(5):2015–2022. https://doi.org/10.2135/cropsci2004.0720
Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6(11):1567–1582. https://doi.org/10.1105/tpc.6.11.1567
Pathan SM, Vuong T, Clark K, Lee J-D, Shannon JG, Roberts CA, Ellersieck MR, Burton JW, Cregan PB, Hyten DL, Nguyen HT, Sleper DA (2013) Genetic mapping and confirmation of quantitative trait loci for seed protein and oil contents and seed weight in soybean. Crop Sci 53(3):765–774. https://doi.org/10.2135/cropsci2012.03.0153
Patil G, Chaudhary J, Vuong TD, Jenkins B, Qiu D, Kadam S, Shannon GJ, Nguyen HT (2017) Development of SNP genotyping assays for seed composition traits in soybean. Int J Plant Genomics 2017:6572969. https://doi.org/10.1155/2017/6572969
Patil G, Mian R, Vuong T, Pantalone V, Song Q, Chen P, Shannon GJ, Carter TC, Nguyen HT (2017b) Molecular mapping and genomics of soybean seed protein: a review and perspective for the future. Theor Appl Genet 130(10):1975–1991. https://doi.org/10.1007/s00122-017-2955-8
Patil G, Vuong TD, Kale S, Valliyodan B, Deshmukh R, Zhu C, Wu X, Bai Y, Yungbluth D, Lu F, Kumpatla S, Shannon JG, Varshney RK, Nguyen HT (2018) Dissecting genomic hotspots underlying seed protein, oil, and sucrose content in an interspecific mapping population of soybean using high-density linkage mapping. Plant Biotechnol J 16(11):1939–1953. https://doi.org/10.1111/pbi.12929
Patrick JW, Offler CE (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52(356):551–564
Pelletier JM, Kwong RW, Park S, Le BH, Baden R, Cagliari A, Hashimoto M, Munoz MD, Fischer RL, Goldberg RB, Harada JJ (2017) LEC1 sequentially regulates the transcription of genes involved in diverse developmental processes during seed development. Proc Natl Acad Sci U S A 114(32):E6710–E6719. https://doi.org/10.1073/pnas.1707957114
Perez-Grau L, Goldberg RB (1989) Soybean seed protein genes are regulated spatially during embryogenesis. Plant Cell 1(11):1095–1109. https://doi.org/10.1105/tpc.1.11.1095
Phansak P, Soonsuwon W, Hyten DL, Song Q, Cregan PB, Graef GL, Specht JE (2016) Multi-population selective genotyping to identify soybean [Glycine max (L.) Merr.] seed protein and oil QTLs. G3 6(6):1635–1648. https://doi.org/10.1534/g3.116.027656
Zhang F, Batley J (2020) Exploring the application of wild species for crop improvement in a changing climate. Curr Opin Plant Biol 56:218–222. https://doi.org/10.1016/j.pbi.2019.12.013
Phillips J, Artsaenko O, Fiedler U, Horstmann C, Mock HP, Müntz K, Conrad U (1997) Seed-specific immunomodulation of abscisic acid activity induces a developmental switch. EMBO J 16(15):4489–4496. https://doi.org/10.1093/emboj/16.15.4489
Pipolo AE, Sinclair TR, Camara GMS (2004) Effects of temperature on oil and protein concentration in soybean seeds cultured in vitro. Ann Appl Biol 144(1):71–76. https://doi.org/10.1111/j.1744-7348.2004.tb00318.x
Zhang J, Wang X, Lu Y, Bhusal SJ, Song Q, Cregan PB, Yen Y, Brown M, Jiang GL (2018b) Genome-wide scan for seed composition provides insights into soybean quality improvement and the impacts of domestication and breeding. Mol Plant 11(3):460–472. https://doi.org/10.1016/j.molp.2017.12.016
Prenger EM, Ostezan A, Mian MAR, Stupar RM, Glenn T, Li Z (2019) Identification and characterization of a fast-neutron-induced mutant with elevated seed protein content in soybean. Theor Appl Genet 132(11):2965–2983. https://doi.org/10.1007/s00122-019-03399-w
Zhang M, Liu S, Wang Z, Yuan Y, Zhang Z, Liang Q, Yang X, Duan Z, Liu Y, Kong F, Liu B, Ren B, Tian Z (2022) Progress in soybean functional genomics over the past decade. Plant Biotechnol J 20(2):256–282. https://doi.org/10.1111/pbi.13682
Qi ZM, Han X, Sun Y-n, Wu Q, Shan D-p, Du X-y, Liu C-y, Jiang H-w, Hu G-h, Chen Q-s (2011) An integrated quantitative trait locus map of oil content in soybean, Glycine max (L.) Merr., generated using a meta-analysis method for mining genes. Agri Sci China 10(11):1681–1692. https://doi.org/10.1016/S1671-2927(11)60166-1
Qin J, Wang F, Zhao Q, Shi A, Zhao T, Song Q, Ravelombola W, An H, Yan L, Yang C, Zhang M (2022) Identification of candidate genes and genomic selection for seed protein in soybean breeding pipeline. Front Plant Sci 13:882732. https://doi.org/10.3389/fpls.2022.882732
Rizzo G, Baroni L (2018) Soy, soy foods and their role in vegetarian diets. Nutrients 10(1). https://doi.org/10.3390/nu10010043
Qiu BX, Arelli PR, Sleper DA (1999) RFLP markers associated with soybean cyst nematode resistance and seed composition in a ‘Peking’בEssex’ population. Theor Appl Genet 98(3):356–364. https://doi.org/10.1007/s001220051080
Hudson KA (2010) The circadian clock-controlled transcriptome of developing soybean seeds. Plant Genome 3(1). https://doi.org/10.3835/plantgenome2009.08.0025
Reinprecht Y, Poysa VW, Yu K, Rajcan I, Ablett GR, Pauls KP (2006) Seed and agronomic QTL in low linolenic acid, lipoxygenase-free soybean (Glycine max (L.) Merrill) germplasm. Genome 49(12):1510–1527. https://doi.org/10.1139/g06-112
Ren C, Bilyeu KD, Beuselinck PR (2009) Composition, vigor, and proteome of mature soybean seeds developed under high temperature. Crop Sci 49(3):1010–1022. https://doi.org/10.2135/cropsci2008.05.0247
Rincker K, Nelson R, Specht J, Sleper D, Cary T, Cianzio SR, Casteel S, Conley S, Chen P, Davis V, Fox C, Graef G, Godsey C, Holshouser D, Jiang G-L, Kantartzi SK, Kenworthy W, Lee C, Mian R et al (2014) Genetic improvement of U.S. soybean in maturity groups II, III, and IV. Crop Sci 54(4):1419–1432. https://doi.org/10.2135/cropsci2013.10.0665
Rolletschek H, Radchuk R, Klukas C, Schreiber F, Wobus U, Borisjuk L (2005) Evidence of a key role for photosynthetic oxygen release in oil storage in developing soybean seeds. New Phytol 167(3):777–786. https://doi.org/10.1111/j.1469-8137.2005.01473.x
Rotundo JL, Borrás L, Westgate ME, Orf JH (2009) Relationship between assimilate supply per seed during seed filling and soybean seed composition. Field Crops Research 112(1):90–96. https://doi.org/10.1016/j.fcr.2009.02.004
Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54(4):608–620. https://doi.org/10.1111/j.1365-313X.2008.03461.x
Scallon B, Thanh VH, Floener LA, Nielsen NC (1985) Identification and characterization of DNA clones encoding group-II glycinin subunits. Theor Appl Genet 70(5):510–519. https://doi.org/10.1007/BF00305984
Schmidt MA, Parrott WA, Hildebrand DF, Berg RH, Cooksey A, Pendarvis K, He Y, McCarthy F, Herman EM (2015) Transgenic soya bean seeds accumulating beta-carotene exhibit the collateral enhancements of oleate and protein content traits. Plant Biotechnol J 13(4):590–600. https://doi.org/10.1111/pbi.12286
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183. https://doi.org/10.1038/nature08670
Schussler JR, Brenner ML, Brun WA (1984) Abscisic acid and its relationship to seed filling in soybeans. Plant Physiol 76(2):301–306. https://doi.org/10.1104/pp.76.2.301
Schwender J, Ohlrogge JB (2002) Probing in vivo metabolism by stable isotope labeling of storage lipids and proteins in developing Brassica napus embryos. Plant Physiol 130(1):347–361. https://doi.org/10.1104/pp.004275
Sebolt AM, Shoemaker RC, Diers BW (2000) Analysis of a quantitative trait locus allele from wild soybean that increases seed protein concentration in soybean. Crop Sci 40(5):1438–1444. https://doi.org/10.2135/cropsci2000.4051438x
Sedivy EJ, Wu F, Hanzawa Y (2017) Soybean domestication: the origin, genetic architecture and molecular bases. New Phytol 214(2):539–553. https://doi.org/10.1111/nph.14418
Seo J-H, Kim K-S, Ko J-M, Choi M-S, Kang B-K, Kwon S-W, Jun T-H (2019) Quantitative trait locus analysis for soybean (Glycine max) seed protein and oil concentrations using selected breeding populations. Plant Breed 138(1):95–104. https://doi.org/10.1111/pbr.12659
Zhang Y, Li W, Lin Y, Zhang L, Wang C, Xu R (2018c) Construction of a high-density genetic map and mapping of QTLs for soybean (Glycine max) agronomic and seed quality traits by specific length amplified fragment sequencing. BMC Genomics 19(1):641. https://doi.org/10.1186/s12864-018-5035-9
Shannon JG, Wilcox JR, Probst AH (1972) Estimated gains from selection for protein and yield in the f4 generation of six soybean populations. Crop Sci 12(6):824. https://doi.org/10.2135/cropsci1972.0011183X001200060032x
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. Sci China Life Sci 61(8):871–884. https://doi.org/10.1007/s11427-018-9360-0
Shen B, Schmidt MA, Collet KH, Liu ZB, Coy M, Abbitt S, Molloy L, Frank M, Everard JD, Booth R, Samadar PP, He Y, Kinney A, Herman EM (2022) RNAi and CRISPR-Cas silencing E3-ring ubiquitin ligase AIP2 enhances soybean seed protein content. J Exp Bot 73(22):7285. https://doi.org/10.1093/jxb/erac376
Shewry PR (2016) The protein chemistry of dicotyledonous grains. In: Wrigley C, Corke H, Seetharaman K, Faubion J (eds) Encyclopedia of food grains, 2nd edn. Academic Press, Oxford, pp 109–114. https://doi.org/10.1016/B978-0-12-394437-5.00105-4
Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7(7):945–956. https://doi.org/10.1105/tpc.7.7.945
Shook JM, Zhang J, Jones SE, Singh A, Diers BW, Singh AK (2021) Meta-GWAS for quantitative trait loci identification in soybean. G3 (7):11, jkab117. https://doi.org/10.1093/g3journal/jkab117
Shibata M, Takayama K, Ujiie A, Yamada T, Abe J, Kitamura K (2008) Genetic relationship between lipid content and linolenic acid concentration in soybean seeds. Breed Sci 58(4):361–366. https://doi.org/10.1270/jsbbs.58.361
Shutov AD, Baumlein H, Blattner FR, Muntz K (2003) Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution. J Exp Bot 54(388):1645–1654. https://doi.org/10.1093/jxb/erg165
Singh A, Meena M, Kumar D, Dubey AK, Hassan MI (2015) Structural and functional analysis of various globulin proteins from soy seed. Crit Rev Food Sci and Nutr 55(11):1491–1502. https://doi.org/10.1080/10408398.2012.700340
Zhang D, Zhang H, Hu Z, Chu S, Yu K, Lv L, Yang Y, Zhang X, Chen X, Kan G, Tang Y, An YC, Yu D (2019) Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication. PLoS Genet 15(7):e1008267. https://doi.org/10.1371/journal.pgen.1008267
Sonah H, O’Donoughue L, Cober E, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13(2):211–221. https://doi.org/10.1111/pbi.12249
Song W, Yang R, Wu T, Wu C, Sun S, Zhang S, Jiang B, Tian S, Liu X, Han T (2016) Analyzing the effects of climate factors on soybean protein, oil contents, and composition by extensive and high-density sampling in China. J Agric Food Chem 64(20):4121–4130. https://doi.org/10.1021/acs.jafc.6b00008
Specht JE, Chase K, Macrander M, Graef GL, Chung J, Markwell JP, Germann M, Orf JH, Lark KG (2001) Soybean response to water: a QTL analysis of drought tolerance. Crop Sci 41(2):493–509. https://doi.org/10.2135/cropsci2001.412493x
Springmann M, Clark M, Mason-D’Croz D, Wiebe K, Bodirsky BL, Lassaletta L, de Vries W, Vermeulen SJ, Herrero M, Carlson KM, Jonell M, Troell M, DeClerck F, Gordon LJ, Zurayk R, Scarborough P, Rayner M, Loken B, Fanzo J et al (2018) Options for keeping the food system within environmental limits. Nature 562(7728):519–525. https://doi.org/10.1038/s41586-018-0594-0
Staswick PE, Hermodson MA, Nielsen NC (1981) Identification of the acidic and basic subunit complexes of glycinin. J Biol Chem 256(16):8752–8755
Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci U S A 98(20):11806–11811. https://doi.org/10.1073/pnas.201413498
Tsao HE, Lui SN, Lo AH, Chen S, Wong HY, Wong CK, Jiang L, Wong KB (2022) Structural insights into how vacuolar sorting receptors recognize the sorting determinants of seed storage proteins. Proc Natl Acad Sci U S A 119(1). https://doi.org/10.1073/pnas.2111281119
Tajuddin T, Watanabe S, Yamanaka N, Harada K (2003) Analysis of quantitative trait loci for protein and lipid contents in soybean seeds using recombinant inbred lines. Breed Sci 53:133–140
Tan-Wilson AL, Wilson KA (2012) Mobilization of seed protein reserves. Physiol Plant 145(1):140–153. https://doi.org/10.1111/j.1399-3054.2011.01535.x
Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217(1):35–53. https://doi.org/10.1111/nph.14876
To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18(7):1642–1651. https://doi.org/10.1105/tpc.105.039925
Tripathi N, Khare D (2016) Molecular approaches for genetic improvement of seed quality and characterization of genetic diversity in soybean: a critical review. Biotechnol Lett 38(10):1645–1654. https://doi.org/10.1007/s10529-016-2154-8
Tsuda M, Kaga A, Anai T, Shimizu T, Sayama T, Takagi K, Machita K, Watanabe S, Nishimura M, Yamada N, Mori S, Sasaki H, Kanamori H, Katayose Y, Ishimoto M (2015) Construction of a high-density mutant library in soybean and development of a mutant retrieval method using amplicon sequencing. BMC Genomics 16:1014. https://doi.org/10.1186/s12864-015-2079-y
Tumer NE, Thanh VH, Nielsen NC (1981) Purification and characterization of mRNA from soybean seeds. Identification of glycinin and beta-conglycinin precursors. J Biol Chem 256(16):8756–8760
Vaughn JN, Nelson RL, Song Q, Cregan PB, Li Z (2014) The genetic architecture of seed composition in soybean is refined by genome-wide association scans across multiple populations. G3 4(11):2283–2294. https://doi.org/10.1534/g3.114.013433
Verdier J, Thompson RD (2008) Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol 49(9):1263–1271. https://doi.org/10.1093/pcp/pcn116
Vitale A, Raikhel NV (1999) What do proteins need to reach different vacuoles? Trends Plant Sci 4(4):149–155. https://doi.org/10.1016/s1360-1385(99)01389-8
Wakasa Y, Takaiwa F (2013) Seed storage proteins. In: Brenner’s encyclopedia of genetics. Elsevier Science, pp 346–348. https://doi.org/10.1016/b978-0-12-374984-0.01378-4
Wang X, Jiang G-L, Green M, Scott RA, Hyten DL, Cregan PB (2012) Quantitative trait locus analysis of saturated fatty acids in a population of recombinant inbred lines of soybean. Mol Breed 30(2):1163–1179. https://doi.org/10.1007/s11032-012-9704-0
Wang X, Jiang G-L, Song Q, Cregan PB, Scott RA, Zhang J, Yen Y, Brown M (2014a) Quantitative trait locus analysis of seed sulfur-containing amino acids in two recombinant inbred line populations of soybean. Euphytica 201(2):293–305. https://doi.org/10.1007/s10681-014-1223-0
Wang X, Jiang GL, Green M, Scott RA, Song Q, Hyten DL, Cregan PB (2014b) Identification and validation of quantitative trait loci for seed yield, oil and protein contents in two recombinant inbred line populations of soybean. Mol Genet Genomics 289(5):935–949. https://doi.org/10.1007/s00438-014-0865-x
Wang S, Yokosho K, Guo R, Whelan J, Ruan YL, Ma JF, Shou H (2019) The soybean sugar transporter GmSWEET15 mediates sucrose export from endosperm to early embryo. Plant Physiol 180(4):2133–2141. https://doi.org/10.1104/pp.19.00641
Wang S, Liu S, Wang J, Yokosho K, Zhou B, Yu Y-C, Liu Z, Frommer WB, Ma JF, Chen L-Q, Guan Y, Shou H, Tian Z (2020) Simultaneous changes in seed size, oil content and protein content driven by selection of SWEET homologues during soybean domestication. Natl Sci Rev 7(11):1776–1786. https://doi.org/10.1093/nsr/nwaa110
Wang J, Mao L, Zeng Z, Yu X, Lian J, Feng J, Yang W, An J, Wu H, Zhang M, Liu L (2021) Genetic mapping high protein content QTL from soybean ‘Nanxiadou 25’ and candidate gene analysis. BMC Plant Biol 21(1):388. https://doi.org/10.1186/s12870-021-03176-2
Warrington CV, Abdel-Haleem H, Hyten DL, Cregan PB, Orf JH, Killam AS, Bajjalieh N, Li Z, Boerma HR (2015) QTL for seed protein and amino acids in the Benning x Danbaekkong soybean population. Theor Appl Genet 128(5):839–850. https://doi.org/10.1007/s00122-015-2474-4
Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Ann Rev Plant Biol 56:253–279. https://doi.org/10.1146/annurev.arplant.56.032604.144201
Kambhampati S, Aznar-Moreno JA, Hostetler C, Caso T, Bailey SR, Hubbard AH, Durrett TP, Allen DK (2019) On the inverse correlation of protein and oil: examining the effects of altered central carbon metabolism on seed composition using soybean fast neutron mutants. Metabolites 10(1). https://doi.org/10.3390/metabo10010018
Wei Z, Pan T, Zhao Y, Su B, Ren Y, Qiu L (2020) The small GTPase Rab5a and its guanine nucleotide exchange factors are involved in post-Golgi trafficking of storage proteins in developing soybean cotyledon. J Exp Bot 71(3):808–822. https://doi.org/10.1093/jxb/erz454
Weiss MG, Weber CR, Williams LF, Probst AH (1952) Correlation of agronomic characters and temperature with seed compositional characters in soybeans, as influenced by variety and time of planting. Agron J 44(6):289–297. https://doi.org/10.2134/agronj1952.00021962004400060002x
Whiting RM, Torabi S, Lukens L, Eskandari M (2020) Genomic regions associated with important seed quality traits in food-grade soybeans. BMC Plant Biol 20(1):485. https://doi.org/10.1186/s12870-020-02681-0
Wilcox JR (2001) Sixty years of improvement in publicly developed elite soybean lines. Crop Sci 41(6):1711–1716. https://doi.org/10.2135/cropsci2001.1711
Wilcox JR, Shibles RM (2001) Interrelationships among seed quality attributes in soybean. Crop Sci 41(1):11–14. https://doi.org/10.2135/cropsci2001.41111x
Wolf RB, Cavins JF, Kleiman R, Black LT (1982) Effect of temperature on soybean seed constituents: oil, protein, moisture, fatty acids, amino acids and sugars. J Am Oil Chem Soc 59(5):230–232. https://doi.org/10.1007/BF02582182
Xie M, Chung CY, Li MW, Wong FL, Wang X, Liu A, Wang Z, Leung AK, Wong TH, Tong SW, Xiao Z, Fan K, Ng MS, Qi X, Yang L, Deng T, He L, Chen L, Fu A et al (2019) A reference-grade wild soybean genome. Nat Commun 10(1):1216. https://doi.org/10.1038/s41467-019-09142-9
Yu H, Lin T, Meng X, Du H, Zhang J, Liu G, Chen M, Jing Y, Kou L, Li X, Gao Q, Liang Y, Liu X, Fan Z, Liang Y, Cheng Z, Chen M, Tian Z, Wang Y et al (2021) A route to de novo domestication of wild allotetraploid rice. Cell. https://doi.org/10.1016/j.cell.2021.01.013
Xu H, Zhang L, Zhang K, Ran Y (2020) Progresses, challenges, and prospects of genome editing in soybean (Glycine max). Front Plant Sci 11:571138. https://doi.org/10.3389/fpls.2020.571138
Yang H, Wang W, He Q, Xiang S, Tian D, Zhao T, Gai J (2019) Identifying a wild allele conferring small seed size, high protein content and low oil content using chromosome segment substitution lines in soybean. Theor Appl Genet 132(10):2793–2807. https://doi.org/10.1007/s00122-019-03388-z
Yang Y, La TC, Gillman JD, Lyu Z, Joshi T, Usovsky M, Song Q, Scaboo A (2022) Linkage analysis and residual heterozygotes derived near isogenic lines reveals a novel protein quantitative trait loci from a Glycine soja accession. Front Plant Sci 13:938100. https://doi.org/10.3389/fpls.2022.938100
Funding
This work was funded by the National Natural Science Foundation of China (31871643, 32230078, 31801390). This work was also supported by “Strategic Priority Research Program” of the Chinese Academy of Sciences (XDA24010105), Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design (2022B1212010013-3), and Hainan Yazhou Bay Seed Laboratory of China (B21HJ0110).
Author information
Authors and Affiliations
Contributions
SL drafted the manuscript. ZL, XH, and XL conceived the article and revised the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Soybean Functional Genomics.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, S., Liu, Z., Hou, X. et al. Genetic mapping and functional genomics of soybean seed protein. Mol Breeding 43, 29 (2023). https://doi.org/10.1007/s11032-023-01373-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-023-01373-5