Skip to main content

Advertisement

SpringerLink
Log in

Identification of new QTLs for seed mineral, cysteine, and methionine concentrations in soybean [Glycine max (L.) Merr.]

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Increased concentrations of important nutrients in edible parts of plants could result in biofortified foods. Soybean [Glycine max (L.) Merr.] is a major legume crop and an important source of certain nutrients, including protein and minerals, in human and animal diets. Understanding the underlying genetic basis of seed composition is crucial to improving seed nutrient composition. In this study we used three soybean recombinant inbred line mapping populations derived from the crosses Williams 82 × DSR-173, Williams 82 × NKS19-90 and Williams 82 × Vinton 81, and constructed a joint linkage map from these populations. Forty quantitative trait loci (QTLs) were detected for 18 traits: seed weight, seed magnesium, sulfur, calcium, manganese, potassium, iron, cobalt, nickel, copper, zinc, selenium, molybdenum, cadmium and arsenic concentrations, total nitrogen:total sulfur (N:S) ratio, cysteine and methionine concentrations. Using the joint linkage map, we detected nine QTLs that were not identified in the individual populations. We identified several candidate genes that might contribute to these traits, including transporters and genes involved in nitrogen and amino acid metabolism. Some strong QTLs had no obvious candidate genes, offering the possibility that subsequent confirmation of these QTLs may result in identification of new genes affecting seed nutrients in soybean. Seed weight and seed mineral concentrations were not highly correlated, suggesting the possibility of improving seed mineral concentrations without significant changes in seed weight. An inverse relationship between N:S ratio and most other minerals suggests the possibility of using N:S ratio as an indirect measure of seed mineral concentration in soybean breeding programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

References

  • Aastveit AH, Aastveit K (1993) Effects of genotype-environment interactions on genetic correlations. Theor Appl Genet 86:1007–1013

    Article  CAS  PubMed  Google Scholar 

  • Anderson J (1993) Selenium interactions in sulfur metabolism. In: De Kok IS et al (ed) Sulfur nutrition and assimilation in higher plants: regulatory agricultural and environmental aspects. SPB Academic, pp 49–60

  • Arahana VS, Graef GL, Specht JE, Steadman JR, Eskridge KM (2001) Identification of QTLs for resistance to Sclerotinia sclerotiorum in soybean. Crop Sci 41:180–188

    Article  CAS  Google Scholar 

  • Beebe S, Gonzalez AV, Rengifo J (2000) Research on trace minerals in the common bean. Food Nutr Bull 21:387–391

    Google Scholar 

  • Bernard RL, Cremeens CR (1988) Registration of “Williams 82” Soybean. Crop Sci 28:1027

    Google Scholar 

  • Bordat A, Savois V, Nicolas M, Salse J, Chauveau A, Bourgeois M, Potier J, Houtin H, Rond C, Murat F, Marget P, Aubert G, Burstin J (2011) Translational genomics in legumes allowed placing in silico 5460 unigenes on the pea functional map and identified candidate genes in Pisum sativum L. Genes Genomes Genetics 1:93–103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Cakmak I, Ozkan H, Braun HJ, Welch RM, Romheld V (2000) Zinc and iron concentrations in seeds of wild, primitive and modern wheats. Food Nutr Bull 21:401–403

    Google Scholar 

  • Chatzav M, Peleg Z, Ozturk L, Yazici A, Fahima T, Cakmak I, Saranga Y (2010) Genetic diversity for grain nutrients in wild emmer wheat: potential for wheat improvement. Ann Bot 105:1211–1220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Coles ND, McMullen MD, Balint-Kurti PJ, Pratt RC, Holland JB (2010) Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis. Genetics 184:799–812

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Csanádi G, Vollmann J, Stift G, Lelley T (2001) Seed quality QTLs identified in a molecular map of early maturing soybean. Theor Appl Genet 103:912–919

    Article  Google Scholar 

  • Curie C, Cassin G, Couch D, Divol F, Higuchi K, Marie Le Jean, Misson J, Schikora A, Czernic P, Mari S (2009) Metal movement within the plant: contribution of nicotianamine and yellow stripe 1-like transporters. Ann Bot 103:1–11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414

    Article  CAS  PubMed  Google Scholar 

  • Ding G, Yang M, Hu Y, Liao Y, Shi L, Xu F, Meng J (2010) Quantitative trait loci affecting seed mineral concentrations in Brassica napus grown with contrasting phosphorus supplies. Ann Bot 105:1221–1234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fehr W, Bahrenfus J, Walker A (1984) Registration of ‘Vinton 81’ soybean. Crop Sci 24:384

    Article  Google Scholar 

  • Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17:282–286

    Article  CAS  PubMed  Google Scholar 

  • Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843–D846

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gregorio GB, Senadhira D, Htut H, Graham RD (2000) Breeding for trace mineral density in rice. Food Nutr Bull 21:382–386

    Google Scholar 

  • Grusak MA, DellaPenna D (1999) Improving the nutrient composition of plants to enhance human nutrition and health. Annu Rev Plant Physiol Plant Mol Biol 50:133–161

    Article  CAS  PubMed  Google Scholar 

  • 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 109:552–561

    Article  CAS  PubMed  Google Scholar 

  • Hyten DL, Choi I, Song Q, Specht JE, Carter TE, Shoemaker RC, Hwang E, Matukumalli LK, Cregan PB (2010) A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 50:960. doi:10.2135/cropsci2009.06.0360

    Article  CAS  Google Scholar 

  • Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J Exp Bot 58:2909–2915

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390

    Article  CAS  PubMed  Google Scholar 

  • Jegadeesan S, Yu K, Poysa V, Gawalko E, Morrison MJ, Shi C, Cober E (2010) Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [Glycine max (L.) Merr]. Theor Appl Genet 121:283–294

    Article  CAS  PubMed  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204. doi:10.1104/pp.104.045625

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim W, Chronis D, Juergens M, Schroeder AC, Hyun SW, Jez JM, Krishnan HB (2012) Transgenic soybean plants overexpressing O-acetylserine sulfhydrylase accumulate enhanced levels of cysteine and Bowman-Birk protease inhibitor in seeds. Planta 235:13–23

    Article  CAS  PubMed  Google Scholar 

  • King KE, Ga Peiffer, Reddy M, Lauter N, Lin SF, Cianzio S, Shoemaker RC (2013) Mapping of iron and zinc quantitative trait loci in soybean for association to iron deficiency chlorosis resistance. J Plant Nutr 36:2132–2153. doi:10.1080/01904167.2013.766804

    Article  CAS  Google Scholar 

  • Kitamura K (1995) Genetic improvement of nutritional and food processing quality in soybean. Jpn Agric Res Q 29:1–8

    Google Scholar 

  • Kleese RA, Rasmusson DC, Smith LH (1968) Genetic and environmental variation in mineral element accumulation in barley, wheat, and soybeans. Crop Sci 8:591

    Article  Google Scholar 

  • Krishnan HB, Jang S, Kim W, Kerley MS, Oliver MJ, Trick HN (2011) Biofortification of soybean meal: immunological properties of the 27 kDa γ-zein. J Agric Food Chem 59:1223–1228

    Article  CAS  PubMed  Google Scholar 

  • Lucas MR, Diop NN, Wanamaker S, Ehlers JD, Roberts PA, Close TJ (2011) Cowpea-soybean synteny clarified through an improved genetic map. Plant Genome 4:218–225

    Article  CAS  Google Scholar 

  • Maughan PJ, Maroof MAS, Buss GR (1996) Molecular-marker analysis of seed-weight: genomic locations, gene action, and evidence for orthologous evolution among three legume species. Theor Appl Genet 93:574–579

    Article  CAS  PubMed  Google Scholar 

  • McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genom 11:184

    Article  Google Scholar 

  • Imtiaz M, Alloway BJ, Shah KH, Siddiqui SH, Memon MY Aslam M, P K (2003) Zinc nutrition of wheat: I: growth and zinc uptake. Asian J Plant Sci 2:152–155

  • Mian MAR, Bailey MA, Tamulonis JP, Shipe ER, Carter TE, Parrott WA, Ashley DA, Hussey RS, Boerma HR (1996) Molecular markers associated with seed weight in two soybean populations. Theor Appl Genet 93:1011–1016

    Article  CAS  PubMed  Google Scholar 

  • Moraghan JT, Helms TC (2005) Seed iron in diverse soybean genotypes. J Plant Nutr 28:1453–1463

    Article  CAS  Google Scholar 

  • Negeri AT, Coles ND, Holland JB, Balint-Kurti PJ (2011) Mapping QTL controlling southern leaf blight resistance by joint analysis of three related recombinant inbred line populations. Crop Sci 51:1571

    Article  Google Scholar 

  • Orf JH, Chase K, Jarvik T, Mansur LM, Cregan PB, Adler FR, Lark KG (1999) Genetics of soybean agronomic traits: comparison of three related recombinant inbred populations. Crop Sci 39:1642–1651

    Article  Google Scholar 

  • Ozkan H, Brandolini A, Torun A, Altintas S, Eker S, Kilian B, Braun HJ, Salamini F, Cakmak I (2007) Natural variation and identification of microelements content in seeds of einkorn wheat (Triticum monococcum). In: Buck HT, Nisi JE, Salom N (eds) Wheat production in stressed environments: proceedings of the 7th international wheat conference. Mar del Plata, Argentina, pp 455–462

    Chapter  Google Scholar 

  • Panthee DR, Pantalone VR, Sams CE, Saxton AM, West DR, Rayford WE (2004a) Genomic regions governing soybean seed. J Am Oil Chem Soc 81:99–103

    Google Scholar 

  • Panthee DR, Kwanyuen P, Sams CE, West DR, Saxton AM, Pantalone VR (2004b) Quantitative trait loci β-conglycinin (7S) and glycinin (11S) fractions of soybean storage protein. J Am Oil Chem Soc 81:1005–1012

    Article  CAS  Google Scholar 

  • 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 45:2015

    Article  CAS  Google Scholar 

  • Panthee DR, Pantalone VR, Sams CE, Saxton AM, West DR, Orf JH, Killam AS (2006a) Quantitative trait loci controlling sulfur containing amino acids, methionine and cysteine, in soybean seeds. Theor Appl Genet 112:546–553

    Article  CAS  PubMed  Google Scholar 

  • Panthee DR, Pantalone VR, Saxton AM, West DR, Sams CE (2006b) Genomic regions associated with amino acid composition in soybean. Mol Breed 17:79–89

    Article  CAS  Google Scholar 

  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD (1988) Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature 335:721–726

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Cakmak I, Ozturk L, Yazici A, Jun Y, Budak H, Korol AB, Fahima T, Saranga Y (2009) Quantitative trait loci conferring grain mineral nutrient concentrations in durum wheat × wild emmer wheat RIL population. Theor Appl Genet 119:353–369

    Article  CAS  PubMed  Google Scholar 

  • Qu LQ, Yoshihara T, Ooyama A, Goto F, Takaiwa F (2005) Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds. Planta 222:225–233

    Article  CAS  Google Scholar 

  • Raboy V, Dickenson DB, Below F (1984) Variation in seed total phosphorus, phytic acid, zinc, calcium, magnesium, and protein among lines of Glycine max and G. soja. Crop Sci 24:431–434

    Article  CAS  Google Scholar 

  • Ramesh SA, Choimes S, Schachtman DP (2004) Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Mol Biol 54:373–385

    Article  CAS  PubMed  Google Scholar 

  • Ranocha P, McNeil SD, Ziemak MJ, Li C, Tarczynski MC, Hanson AD (2001) The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity. Plant J 25:575–584

    Article  CAS  PubMed  Google Scholar 

  • Sankaran RP, Huguet T, Grusak MA (2009) Identification of QTL affecting seed mineral concentrations and content in the model legume Medicago truncatula. Theor Appl Genet 119:241–253

    Article  CAS  PubMed  Google Scholar 

  • 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, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Severin AJ, Cannon SB, Graham MM, Grant D, Shoemaker RC (2011) Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. Plant Cell 23:3129–3136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sexton PJ, Naeve SL, Paek NC, Shibles R (1998) Sulfur availability, cotyledon nitrogen:sulfur ratio, and relative abundance of seed storage proteins of soybean. Crop Sci 38:983–986

    Article  CAS  Google Scholar 

  • Sharma S, Kaur M, Goyal R, Gill BS (2011) Physical characteristics and nutritional composition of some new soybean (Glycine max (L.) Merrill) genotypes. J Food Sci. doi:10.1007/s13197-011-0517-7

    Google Scholar 

  • 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. Cell Biol Mol Genet 41:493–509

    CAS  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182

    Article  CAS  PubMed  Google Scholar 

  • Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci USA 104:18807–18812

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta SK (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164:371–378

    Article  CAS  Google Scholar 

  • Vasconcelos MW, Musetti V, Chee-Ming L, Datta SK, Grusak MA (2004) Functional analysis of transgenic rice (Oryza sativa L.) transformed with an Arabidopsis thaliana ferric reductase (AtFRO2). Soil Sci Plant Nutr 50:1151–1157

    Article  CAS  Google Scholar 

  • Vasconcelos M, Eckert H, Arahana V, Graef G, Grusak MA, Clemente T (2006) Molecular and phenotypic characterization of transgenic soybean expressing the Arabidopsis ferric chelate reductase gene, FRO2. Planta 224:1116–1128

    Article  CAS  PubMed  Google Scholar 

  • Vreugdenhil D, Aarts MGM, Koornneef M, Nelissen H, Ernst WHO (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant, Cell Environ 27:828–839

    Article  CAS  Google Scholar 

  • Wang J, Li Y, Zhang Y, Chai T (2013) Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep 32:651–662

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Grusak MA (2008) Quantitative trait locus mapping for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. New Phytol 179:1033–1047

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Sankaran RP (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci 180:562–574

    Article  CAS  PubMed  Google Scholar 

  • Waters BM, Chu H, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waters BM, Uauy C, Dubcovsky J, Grusak MA (2009) Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain. J Exp Bot 60:4263–4274

    Article  CAS  PubMed  Google Scholar 

  • Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364

    Article  CAS  PubMed  Google Scholar 

  • Werner AK, Sparkes IA, Romeis T, Witte C (2008) Identification, biochemical characterization, and subcellular localization of allantoate amidohydrolases from Arabidopsis and soybean. Plant Physiol 146:418–430

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets–iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Close TJ, Lonardi S (2011) Accurate construction of consensus genetic maps via integer linear programming. IEEE/ACM Trans Comp BiolBioinform 8:381–394

    Article  Google Scholar 

  • Zhang B, Chen P, Shi A, Hou A, Ishibashi T, Wang D (2009) Putative quantitative trait loci associated with calcium content in soybean seed. J Hered 100:263–269

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Chen P, Florez-Palacios SL, Shi A, Hou A, Ishibashi T (2010) Seed quality attributes of food-grade soybeans from the U.S. and Asia. Euphytica 173:387–396

    Article  Google Scholar 

  • Zuber H, Davidian J, Aubert G et al (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol 154:913–926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported in part by grants from the Nebraska Soybean Board to B.M.W. and G.G. The authors thank Anthony Delaney, Alec Hogan and Grace Troupe for technical assistance, and Drs. Aaron Lorenz and Jim Specht for assistance with linkage mapping software.

Author information

Authors and Affiliations

  1. Department of Agronomy and Horticulture, University of Nebraska–Lincoln, 377 K PLSH, Lincoln, NE, 68583-0915, USA

    Raghuprakash Kastoori Ramamurthy, Joseph Jedlicka, George L. Graef & Brian M. Waters

Authors
  1. Raghuprakash Kastoori Ramamurthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph Jedlicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. George L. Graef
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brian M. Waters
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian M. Waters.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 647 kb)

Supplementary material 2 (XLSX 489 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kastoori Ramamurthy, R., Jedlicka, J., Graef, G.L. et al. Identification of new QTLs for seed mineral, cysteine, and methionine concentrations in soybean [Glycine max (L.) Merr.]. Mol Breeding 34, 431–445 (2014). https://doi.org/10.1007/s11032-014-0045-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-014-0045-z

Keywords

Search

Navigation