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Genetic architecture of biofortification traits in soybean (Glycine max L. Merr.) revealed through association analysis and linkage mapping

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Abstract

Seed mineral elements are essential not only for seed germination and seedling morphological formation but also for human health. The genetic dissection of seed mineral accumulation is important for mineral biofortification in soybean. However, the molecular mechanisms controlling mineral element accumulation are genetically complex because a number of genetic loci are involved in the metabolic pathways of mineral accumulation in seeds. The objective of this study was to detect the genetic loci for mineral concentrations in soybean seeds, including calcium (Ca), magnesium (Mg), iron (Fe), zinc (Zn) and phosphorus (P). Quantitative trait loci (QTL) mapping for the corresponding traits was performed in 184 recombinant inbred lines (RILs) and 219 cultivated soybean accessions. The data for each year and the average across 2 years were used for identification and mapping of QTL controlling seed mineral concentrations. Linkage mapping in the RILs identified totally 35 significant QTL for the five seed mineral concentrations in three cases, some of which were co-localized. Association mapping in the 219 accessions detected 28 single-nucleotide polymorphisms associated with the seed mineral concentrations. Among these, BARC-018099-02516, which was associated with seed Zn concentration, was located close to qZn-11-2. There were 20 putative mineral-related genes in interesting regions of mineral QTL. Three QTL for seed weight were mapped in the RILs, two QTL for seed weight were co-localized with seed Ca, Zn and P concentration QTL which anchored to the same region on chromosome 11. These results will provide a profound understanding of the genetic basis for seed mineral accumulation in soybean seeds and the foundation for mineral biofortification through marker-assisted selection breeding.

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Abbreviations

ANOVA:

Analysis of variance

CHr.:

Chromosome

GLM:

General linear model

MAS:

Marker-assisted selection

PVE:

Proportion of phenotypic variance explained

QTL:

Quantitative trait locus

References

  • Blair MW, Astudillo C, Grusak M, Graham R, Beebe S (2009a) Inheritance of seed iron and zinc concentrations in common bean (Phaseolus vulgaris L.). Mol Breed 23:197–207

    Article  CAS  Google Scholar 

  • Blair MW, Sandoval TA, Caldas GV, Beebe SE, Páez MI (2009b) Quantitative trait locus analysis of seed phosphorus and seed phytate content in a recombinant inbred line population of common bean. Crop Sci 49:237–246

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cichy KA, Caldas GV, Snapp SS, Blair MW (2009) QTL analysis of seed iron, zinc, and phosphorus levels in an Andean bean population. Crop Sci 49:1742–1750

    Article  CAS  Google Scholar 

  • Cockram J, White J, Zuluaga DL et al (2010) Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci 107:21611–21616

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coelho CMM, Santos JCP, Tsai SM, Vitorello VA (2002) Seed phytate content and phosphorus uptake and distribution in dry bean genotypes. Braz J Plant Physiol 14:51–58

    Article  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330

    Article  CAS  PubMed  Google Scholar 

  • Darvasi A, Weinreb A, Minke V, Weller JI, Soller M (1993) Detecting marker-QTL linkage and estimating QTL gene effect and map location using a saturated genetic map. Genetics 134:943–951

    CAS  PubMed Central  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 

  • Divecha N, Irvine RF (1995) Phospholipid signaling review. Cell 80:269–278

    Article  CAS  PubMed  Google Scholar 

  • Frossard E, Bucher M, Mächler F, Mozafar A, Hurrell R (2000) Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J Sci Food Agric 80:861–879

    Article  CAS  Google Scholar 

  • Fu S, Zhan Y, Zhi H, Gai J, Yu D (2006) Mapping of SMV resistance gene Rsc-7 by SSR markers in soybean. Genetica 128:63–69

    Article  CAS  PubMed  Google Scholar 

  • Gelin JR, Forster S, Grafton KF, McClean PE, Rojas-Cifuentes GA (2007) Analysis of seed zinc and other minerals in a recombinant inbred population of navy bean (Phaseolus vulgaris L.). Crop Sci 47:1361–1366

    Article  CAS  Google Scholar 

  • Ghandilyan A, Vreugdenhil D, Aarts MG (2006) Progress in the genetic understanding of plant iron and zinc nutrition. Physiol Plant 126:407–417

    Article  CAS  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 

  • Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol 177:889–898

    Article  CAS  PubMed  Google Scholar 

  • Guzmán-Maldonado SH, Martínez O, Acosta-Gallegos JA, Guevara-Lara F, Paredes-López O (2003) Putative quantitative trait loci for physical and chemical components of common bean. Crop Sci 43:1029–1035

    Article  Google Scholar 

  • Hao D, Cheng H, Yin Z, Cui S, Zhang D, Wang H, Yu D (2012) Identification of single nucleotide polymorphisms and haplotypes associated with yield and yield components in soybean (Glycine max) landraces across multiple environments. Theor Appl Genet 124:447–458

    Article  CAS  PubMed  Google Scholar 

  • Hu Z, Zhang H, Kan G, Ma D, Zhang D, Shi G, Hong D, Zhang G, Yu D (2013) Determination of the genetic architecture of seed size and shape via linkage and association analysis in soybean (Glycine max L. Merr.). Genetica 141:247–254

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Zhao Y, Wei X et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39

    Article  Google Scholar 

  • Jin T, Zhou J, Chen J, Zhu L, Zhao Y, Huang Y (2013) The genetic architecture of zinc and iron content in maize grains as revealed by QTL mapping and meta-analysis. Breed Sci 63:317–324

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • King KE, Lauter N, Lin SF, Scott MP, Shoemaker RC (2013a) Evaluation and QTL mapping of phosphorus concentration in soybean seed. Euphytica 189:261–269

    Article  CAS  Google Scholar 

  • King KE, Peiffer GA, Lauter N, Reddy M, Lin SF, Cianzio S, Shoemaker RC (2013b) Mapping of iron and zinc quantitative trait loci in soybean (Glycine max L. Merr.) for association to iron deficiency chlorosis resistance. J Plant Nutr 36:2132–2153

    Article  CAS  Google Scholar 

  • Knappe S, Flügge UI, Fischer K (2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol 131:1178–1190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee S, Jeong HJ, Kim SA, Lee J, Guerinot ML, An G (2010) OsZIP5 is a plasma membrane zinc transporter in rice. Plant Mol Biol 73:507–517

    Article  CAS  PubMed  Google Scholar 

  • Li L, Tutone AF, Drummond RSM, Gardner RC, Luan S (2001) A novel family of magnesium transport genes in Arabidopsis. Plant Cell 13:2761–2775

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Huang Y, Bergelsona J, Nordborg M, Borevitza JO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci 49:21199–21204

    Article  Google Scholar 

  • Liang Q, Cheng X, Mei M, Yan X, Liao H (2010) QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann Bot 106:223–234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin S, Grant D, Cianzio S, Shoemaker R (2000) A molecular characterization of iron deficiency chlorosis in soybean. J Plant Nutr 23:1929–1939

    Article  CAS  Google Scholar 

  • Lopez-Millan AF, Ellis DR, Grusak MA (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol Biol 54:583–596

    Article  CAS  PubMed  Google Scholar 

  • Lott JNA, Ockenden I, Raboy V, Batten GD (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci Res 10:11–33

    CAS  Google Scholar 

  • Mamidi S, Chikara S, Goos RJ, Hyten DL, Annam D, Moghaddam SM, Lee RK, Cregan PB, McClean PE (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164

    Article  CAS  Google Scholar 

  • McCouch SR, Chen X, Panaud O, Temnykh S, Xu Y, Cho YG, Huang N, Ishii T, Blair M (1997) Microsatellite marker development, mapping and application in rice genetics and breeding. Plant Mol Biol 35:89–99

    Article  CAS  PubMed  Google Scholar 

  • Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277:4738–4746

    Article  CAS  PubMed  Google Scholar 

  • Nestel P, Bouis HE, Meenakshi JV, Pfeiffer W (2006) Biofortification of staple food crops. J Nutr 136:1064–1067

    CAS  PubMed  Google Scholar 

  • Neumann K, Kobiljski B, Denčić S, Varshney RK, Börner A (2011) Genome-wide association mapping: a case study in bread wheat (Triticumaestivum L.). Mol Breed 27:37–58

    Article  Google Scholar 

  • Niu Y, Xu Y, Liu X, Yang S, Wei S, Xie F, Zhang Y (2013) Association mapping for seed size and shape traits in soybean cultivars. Mol Breed 31:785–794

    Article  CAS  Google Scholar 

  • Norton GJ, Deacon CM, Xiong LZ, Huang SY, Meharg AA, Price AH (2010) Genetic mapping of the rice ionome in leaves and grain: identification of QTL for 17 elements including arsenic, cadmium, iron and selenium. Plant Soil 329:139–153

    Article  CAS  Google Scholar 

  • Ragland M, Briat JF, Gagnon J, Laulhere JP, Massenet O, Theil EC (1990) Evidence for conservation of ferritin sequences among plants and animals and for a transit peptide in soybean. J Biol Chem 265:18339–18344

    CAS  PubMed  Google Scholar 

  • Ramamurthy RK, Jedlicka J, Graef GL, Waters BM (2014) Identification of new QTL for seed mineral, cysteine, and methionine concentrations in soybean [Glycine max (L.) Merr.]. Mol Breed 34:431–445

    Article  Google Scholar 

  • Rude RK, Gruber HE (2004) Magnesium deficiency and osteoporosis: animal and human observations. J Nutr Biochem 15:710–716

    Article  CAS  PubMed  Google Scholar 

  • Sankaran R, Huguet T, Grusak M (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 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Schulera M, Rellán-Álvarezb R, Fink-Straubec C, Abadíab J, Bauera P (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24:2380–2400

    Article  Google Scholar 

  • Schwertmann U (1991) Solubility and dissolution of iron oxides. Plant Soil 130:1–25

    Article  CAS  Google Scholar 

  • Shi R, Li H, Tong Y, Jing R, Zhang F, Zou C (2008) Identification of quantitative trait locus of zinc and phosphorus density in wheat (Triticumaestivum L.) grain. Plant Soil 306:95–104

    Article  CAS  Google Scholar 

  • Song H, Yin Z, Chao M, Ning L, Zhang D, Yu D (2014) Functional properties and expression quantitative trait loci for phosphate transporter GmPT1 in soybean. Plant Cell Environ 37:462–472

    Article  CAS  PubMed  Google Scholar 

  • Stangoulis JC, Huynh BL, Welch RM, Choi EY, Graham RD (2007) Quantitative trait loci for phytate in rice grain and their relationship with grain micronutrient content. Euphytica 154:289–294

    Article  Google Scholar 

  • Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Over expression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Bastern J, Zeng Z (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC, USA

  • 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 

  • Zhang W, Wang Y, Luo G, Zhang J, He C, Wu X, Gai J, Chen S (2004) QTL mapping of ten agronomic traits on the soybean (Glycine max L. Merr.) genetic map and their association with EST markers. Theor Appl Genet 108:1131–1139

    Article  CAS  PubMed  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 D, Song H, Cheng H, Hao D, Wang H, Kan G, Jin H, Yu D (2014a) The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 10(1):e1004061

  • Zhang H, Hao D, Sitoe HM, Yin Z, Hu Z, Zhang G, Yu D (2014b) Genetic dissection of the relationship between plant architecture and yield component traits in soybean (Glycine max L. Merr.) by association analysis. Plant Breeding (Under review)

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Acknowledgments

We are grateful to Dr. Juan Liu from the Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, for her advice regarding the manuscript. This work was supported in part by the National Natural Science Foundation of China (no. 31171573 and no. 31370034) and the Jiangsu Provincial Support Program (no. BE2012328).

Conflict of interest

The authors have declared that no competing interests exist.

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetics and Germplasm Enhancement, National Center for Soybean Improvement, Nanjing Agricultural University, Nanjing, 210095, China

    Lihua Ning, Pingdong Sun, Qing Wang, Deyuan Ma, Zhenbin Hu, Guozheng Zhang, Hao Cheng & Deyue Yu

  2. Department of Agronomy, Henan Agricultural University, Zhengzhou, China

    Dan Zhang

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  1. Lihua Ning
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  2. Pingdong Sun
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  3. Qing Wang
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  4. Deyuan Ma
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  5. Zhenbin Hu
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  6. Dan Zhang
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  7. Guozheng Zhang
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  8. Hao Cheng
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  9. Deyue Yu
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Correspondence to Deyue Yu.

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Ning, L., Sun, P., Wang, Q. et al. Genetic architecture of biofortification traits in soybean (Glycine max L. Merr.) revealed through association analysis and linkage mapping. Euphytica 204, 353–369 (2015). https://doi.org/10.1007/s10681-014-1340-9

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  • DOI: https://doi.org/10.1007/s10681-014-1340-9

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