Skip to main content
SpringerLink
Log in

Association mapping combined with linkage analysis for aluminum tolerance among soybean cultivars released in Yellow and Changjiang River Valleys in China

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Association mapping (AM) combined with linkage mapping (LM) was executed to identify molecular markers and QTL regions associated with aluminum (Al) tolerance using relative root elongation (RRE) in hydroponics as an indicator. A set of 188 soybean cultivars released in Yellow and Changjiang River Valleys and 184 recombinant inbred lines (RIL) derived from a cross KF No. 1 (tolerant) × NN1138-2 (susceptible) was used in the study. Inheritance analysis of the RIL population suggested four major genes and polygenes controlled Al-tolerance. Further, LM indicated four additive and four epistatic QTL pairs plus a collective unmapped minor QTL were responsible for Al-tolerance and explained 29.39, 18.75 and 43.07 % of the phenotypic variation (PV), respectively. In the set of released cultivars, AM identified 11 markers significant at P < 0.03 that explained 85.2 % of PV with six of which at P < 0.01 accounted for 57.9 % of PV. Ten of these eleven AM marker-QTL were mapped within range of ~2.0 cM to ~43.0 cM outside confidence interval of respective Al-tolerance QTL in previous studies. Five markers, Satt209, Sat_364, Sat_240, Sct_190 and Satt284, were located near Al-tolerance QTL regions in this and previous LM studies. Thus, the two methods confirmed these markers as being the most likely candidate regions for Al-tolerance. Allele effects relative to the population mean for the 11 QTL were estimated, and the allele A210 of Satt209 showed greatest phenotypic effect on Al-tolerance. The two most favorable alleles from each of the 11 marker loci and their carriers were identified, and accordingly the genetic constitution of Al-tolerance for the 188 cultivars was dissected as a QTL-allele matrix. Therefore, marker-assisted pairing of crosses and marker-assisted selection of progenies can be carried out to pyramid favorable alleles of all the 11 loci. This marker-assisted breeding procedure was designated as breeding by design using a QTL-allele matrix.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Agrama HA, Yan WG (2009) Association mapping of straighthead disorder induced by arsenic in Oryza sativa. Plant Breed 128:551–558

    Article  Google Scholar 

  • Bianchi-Hall CM, Carter TE Jr, Bailey MA, Mian MAR, Rufty TW, Ashley DA, Boerma HR, Arellano C, Hussey RS, Parrott WA (2000) Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci 40:538–545

    Article  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006a) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006b) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46:1323–1330

    Article  Google Scholar 

  • Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111

    Article  PubMed  CAS  Google Scholar 

  • Campbell KAG, Carter TE Jr (1990) Aluminum tolerance in soybean: I. Genotypic correlation and repeatability of solution culture and greenhouse screening methods. Crop Sci 30:1049–1054

    Article  CAS  Google Scholar 

  • Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19. doi:10.1186/1471-2156-3-19

    Article  PubMed  Google Scholar 

  • Cui Z, Carter TE Jr, Burton JW (2000) Genetic diversity patterns in Chinese soybean cultivars based on coefficient of parentage. Crop Sci 40:1780–1793

    Article  Google Scholar 

  • Delhazie E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    Google Scholar 

  • Dong YS, Zhao L, Liu MB, Wang ZW, Jin ZQ, Sun H (2004) The genetic diversity of cultivated soybean grown in China. Theor Appl Genet 108:931–936

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JI (1990) Isolation of plant DNA from fresh tissue. Focus 12:147–151

    Google Scholar 

  • Fehr WR (1987) Principles of cultivar development, vol 1: Theory and technique. McGraw Hill Inc, New York

    Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064

    Article  PubMed  CAS  Google Scholar 

  • Foy CD, Fleming AL, Burns GR, Armiger WH (1967) Characterisation of differential aluminium tolerance among varieties of wheat and barley. Soil Sci Soc Am Proc 31:513–521

    Article  CAS  Google Scholar 

  • Foy CD, Duke JA, Devine TE (1992) Tolerance of soybean germplasm to an acid Tatum subsoil. J Plant Nutr 15:527–547

    Article  Google Scholar 

  • Gai JY (2006) Segregation analysis on genetic system of quantitative traits in plants. Front Biol China 1:85–92

    Article  Google Scholar 

  • Gai JY, Chen L, Zhang YH, Zhao TJ, Xing GN, Xing H (2012) Genome-wide genetic dissection of germplasm resources, and implications for breeding by design in soybean. Breed Sci 61:495–510

    Article  PubMed  CAS  Google Scholar 

  • Habier D, Fernando RL, Deckkers JCM (2009) Genomic selection using low-density marker panels. Genetics 182:343–353

    Article  PubMed  CAS  Google Scholar 

  • Heffner EL, Sorrells ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12

    Article  CAS  Google Scholar 

  • Hill WG (2010) Understanding and using quantitative genetic variation. Philos Trans R Soc B: Bio Sci 365:73–85

    Article  Google Scholar 

  • Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108

    Article  PubMed  CAS  Google Scholar 

  • Hisano H, Shusei S, Sachiko I, Shigemi S, Tsuyuko W, Ai M, Tsunakazu F, Manabu Y, Shinobu N, Yasukazu N, Satoshi W, Kyuya H, Satoshi T (2008) Characterization of the soybean genome using EST-derived microsatellite markers. DNA Res 14:271–281

    Article  Google Scholar 

  • Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161

    Article  PubMed  CAS  Google Scholar 

  • Institute SAS (2004) SAS Institute. Inc. SAS user’s guide. SAS Institute, Inc., Cary

    Google Scholar 

  • Jena KK, Mackhill DJ (2008) Molecular markers and their use in marker-assisted selection in rice. Crop Sci 48:1266–1276

    Article  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55(1):459–493

    Article  PubMed  CAS  Google Scholar 

  • Korir PC, Zhao TJ, Gai JY (2010) A study on indicators and evaluation stages of aluminum tolerance in soybean. Front Agric China 4:280–286

    Article  Google Scholar 

  • Korir PC, Qi B, Wang Y, Zhao T, Yu D, Chen S, Gai J (2011) A study on relative importance of additive, epistasis and unmapped QTL for aluminium tolerance at seedling stage in soybean. Plant Breeding 130:551–562

    Article  CAS  Google Scholar 

  • Krill AM, Kirst M, Kochian LV, Buckler ES, Hoekenga OA (2010) Association and linkage analysis of aluminum tolerance genes in maize. PLoS ONE 5(4):e9958. doi:10.1371/journal.pone.0009958

    Article  PubMed  Google Scholar 

  • Lande R, Thompson R (1990) Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743–756

    PubMed  CAS  Google Scholar 

  • Liu Y, Gai JY (2007) Identification of tolerance to aluminum toxin and inheritance of related root traits in soybeans (Glycine max (L.) Merr.). Front Agric China 1(2):119–128

    Article  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97:46–51

    Article  PubMed  CAS  Google Scholar 

  • Maccaferri M, Sanguineti MC, Mantovani P, Demontis A, Massi A, Ammar K, Kolmer JA, Czembor JH, Ezrati S, Tuberosa R (2010) Association mapping of leaf rust response in durum wheat. Mol Breed 26:189–228

    Article  CAS  Google Scholar 

  • Malysheva-Otto LV, Ganal MW, Roder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordum vulgrae L.). BMC Genet 7:6. doi:10.1186/1471-2156-7-6

    Article  PubMed  Google Scholar 

  • Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829

    PubMed  CAS  Google Scholar 

  • Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90

    Article  PubMed  CAS  Google Scholar 

  • Peleman JD, van der Voort JR (2003) Breeding by design. Trend. Plant Sci 8:330–334

    Article  CAS  Google Scholar 

  • Piñeros MA, Magalhaes JV, Alves VM, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129:1194–1206

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181

    Article  PubMed  CAS  Google Scholar 

  • Qi B, Korir P, Zhao T, Yu D, Chen S, Gai J (2008) Mapping quantitative trait loci associated with aluminum toxin tolerance in NJRIKY recombinant inbred line population of soybean (Glycine max). J Integrat Plant Biol 50:1089–1095

    Article  CAS  Google Scholar 

  • Rosenberg NA, Burke T, Elo K, Feldman MW, Freidlin PJ, Groenen MAM, Hillel J, MäkiTanila A, Tixier-Boichard M, Vignal A, Wimmers K, Weigend S (2001) Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics 159:699–713

    PubMed  CAS  Google Scholar 

  • Ryan PR, Ditomaso JM, Kochian LV (1993) Aluminum toxicity in root —an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446

    Article  CAS  Google Scholar 

  • Semon M, Nielsen R, Jones MP, McCouch SR (2005) The population structure of African cultivated rice Oryza glaberrima (Steud.): evidence for elevated levels of linkage disequilibrium caused by admixture with O. sativa and ecological adaptation. Genetics 169:1639–1647

    Article  PubMed  CAS  Google Scholar 

  • Sharma AD, Sharma H, Lightfoot DA (2011) The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population. Theor Appl Genet 122:687–694

    Article  PubMed  CAS  Google Scholar 

  • Song QJ, Marek LF, Shoemaker RC, Lark KG, Concibido VC, Delannay X, Specht JE, Cregan PB (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128

    Article  PubMed  CAS  Google Scholar 

  • Spehar CR (1995) Diallel analysis for mineral element absorption in tropical adapted soybeans [Glycine max (L.)] Merrill. Theor Appl Genet 90:707–711

    Article  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genome-wide studies. Proc Nat Acad Sci USA 100:9440–9445

    Article  PubMed  CAS  Google Scholar 

  • Van-Ooijen JW, Voorrips RE (2002) JOINMAP 3.0, Software for the Calculation of Genetic Linkage Maps. Plant Research International: Wageningen

  • Vargas-Duque J, Pandey S, Granados G, Ceballos H, Knapp E (1994) Inheritance of tolerance to soil acidity in tropical maize. Crop Sci 34:50–54

    Article  Google Scholar 

  • Villagarcia MR, Carter TE, Rufty TW, Niewoehner AS, Jennette MW, Arrellano C (2001) Genotypic rankings for aluminum tolerance of soybean roots grown in hydroponics and sand culture. Crop Sci 41:1499–1507

    Article  Google Scholar 

  • von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Wang YF (2009) Genomic characterization of simple sequence repeats and establishment, integration and application of high density genetic linkage map in soybean. Ph. D. Dissertation. Nanjing Agricultural University, Nanjing, China, pp 60–75

  • Wang S, Basten CJ, Zeng ZB (2005) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

  • Wang J, McClean PE, Lee R, Goos RJ, Helms T (2008) Association mapping of iron deficiency chlorosis loci in soybean (Glycine max L. Merr.) advanced breeding lines. Theor Appl Genet 116:777–787

    Article  PubMed  CAS  Google Scholar 

  • Wilkening S, Chen B, Hemminki K, Forst A (2006) STR markers for kinship analysis. Hum Biol 78:1–8

    Article  PubMed  Google Scholar 

  • Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artificial selection on the maize genome. Science 308:1310–1314

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Zhu J, Williams W (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536

    Article  PubMed  CAS  Google Scholar 

  • Zhang WK, Wang YJ, Luo GZ, Zhang JS, He CY, Wu XL, Gai JY, Chen SY (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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The National Key Basic Research Program (2009CB1184, 2010CB1259, 2011CB1093), the National Hightech R & D Program (2011AA10A105, 2012AA101106), the Natural Science Foundation of China (31071442) and the MOE 111 Project (B08025) supported this work.

Author information

Authors and Affiliations

  1. Soybean Research Institute, Nanjing Agricultural University, Nanjing, 210095, China

    Paul C. Korir, Jun Zhang, Kejing Wu, Tuanjie Zhao & Junyi Gai

  2. National Center for Soybean Improvement, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Tuanjie Zhao & Junyi Gai

  3. Key Laboratory of Biology and Genetic Improvement of Soybean, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Tuanjie Zhao & Junyi Gai

  4. National Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Tuanjie Zhao & Junyi Gai

Authors
  1. Paul C. Korir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kejing Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tuanjie Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junyi Gai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junyi Gai.

Additional information

Communicated by H. T. Nguyen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Korir, P.C., Zhang, J., Wu, K. et al. Association mapping combined with linkage analysis for aluminum tolerance among soybean cultivars released in Yellow and Changjiang River Valleys in China. Theor Appl Genet 126, 1659–1675 (2013). https://doi.org/10.1007/s00122-013-2082-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2082-0

Keywords

Search

Navigation