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The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population

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Abstract

Aluminum (Al) toxicity to plant roots is a major problem of acidic soils. The main chemical reaction involved is Al hydrolysis. Application of lime or nitrate fertilizers to raise soil pH reduces Al toxicity but not as economically as a plant genotypes with natural tolerance against this stress. Ammonium fertilization of crops and assimilation of ammonium (even that derived from dinitrogen) are particularly acidifying of the root zone. The aims of the present study were to find genotypes of soybean tolerant to aluminum stress and identify QTL underlying that trait. Used were recombinant inbred lines (RILs) derived from the cross of ‘Essex’ by ‘Forrest’. RILs were grown in a greenhouse for 3 weeks and then transferred to hydroponics in a growth chamber. Root lengths (RL) were measured before and 72 h after Al treatment. RL before and after Al treatment were measured and used to calculate root tolerance index (RTI) and relative mean growth (RMG). RILs 1, 85, 40 and 83 had significant (P < 0.005) tolerance to Al stress judged by RL after Al, RTI and RMG. Eleven minor but significant marker–trait associations (P < 0.05) were detected using one-way ANOVA but only two major loci were significant in composite interval maps (LOD >3.0). The QTL on linkage group F (chromosome 13) was in the interval Satt160–Satt252 with a peak at 24 cM (peak LOD was 3.3). The QTL underlay 31% of trait variation and the Essex allele provided an additional 1.61 cm of root growth over 72 h in the presence of Al. The QTL on linkage group C2 (probably chromosome 4) was in the interval from Satt202 to Satt371 with a peak at 3.2 cM (peak LOD was 14.7). The QTL underlay 34% of trait variation or 1.81 cm of growth over 72 h in the presence of Al. Both loci encompassed genes implicated in citrate metabolism, a method of aluminum detoxification known to vary among soybean cultivars. Two major loci and at least nine minor loci were inferred to underlie tolerance to Al. RILs and markers may be used to select alleles that increase tolerance to soybean against Al stress.

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References

  • 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 

  • Chang SJC, Doubler TW, Kilo V, Suttner RJ, Klein JH III, Schmidt ME, Gibson PT, Lightfoot DA (1997) Association of field resistance to soybean sudden death syndrome (SDS) and cyst nematode (SCN). Crop Sci 37:965–971

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Foy CD (1974) Effect of aluminum on plant growth. In: Carson EW (ed) The plant root and its environment. University Press of Virginia, Charlottesville, pp 601–642

    Google Scholar 

  • Hnetkovsky N, Chang SJC, Doubler TW, Gibson PT, Lightfoot DA (1996) Genetic mapping of loci underlying field resistance to soybean sudden death syndrome (SDS). Crop Sci 36:393–400

    Article  CAS  Google Scholar 

  • Huang JW, Shaff JE, Grunes DL, Kochian LV (1992) Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum sensitive wheat cultivars. Plant Physiol 98:230–237

    Article  CAS  PubMed  Google Scholar 

  • Kassem MA, Kang CH, Njiti V, Iqbal MJ, Wood AJ, Lightfoot DA (2004) Loci underlying resistance to manganese toxicity mapped in a soybean recombinant inbred line population. Plant Soil 260:183–196

    Article  Google Scholar 

  • Kassem MA, Shultz JL, Maksem K, Cho Y, Wood AJ, Iqbal MJ, Lightfoot DA (2006) An updated ‘Essex’ by ‘Forrest’ linkage map and first composite interval map of QTL underlying six soybean traits. Theor Appl Genet 113:1015–1026

    Article  CAS  PubMed  Google Scholar 

  • Kinraide TB (1991) Identity of the rhizotoxic aluminum species. Plant Soil 134:167–178

    CAS  Google Scholar 

  • Kochian LV (2004) How do crop plants tolerate acidic soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Lander E, Green P, Abrahamson J, Barlow A, Daley M, Lincoln S, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lightfoot DA, Njiti VN, Gibson PT, Kassem MA, Iqbal JM, Meksem K (2005) Registration of the ‘Essex’ by ‘Forrest’ recombinant inbred line mapping population. Crop Sci 45:1678–1681

    Article  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46

    Article  CAS  PubMed  Google Scholar 

  • Meksem K, Pantazopoulos P, Njiti VN, Hyten LD, Arelli PR, Lightfoot DA (2001) ‘Forrest’ resistance to soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. Theor Appl Genet 103:710–717

    Article  CAS  Google Scholar 

  • Moore R, Evans ML, Fondreu WM (1990) Inducing gravitropic curvature of primary roots of Zea mays cv Agrotropic. Plant Physiol 92:310–315

    Article  CAS  PubMed  Google Scholar 

  • Njiti VN, Doubler TW, Suttner RJ, Gray LE, Gibson PT, Lightfoot DA (1998) Resistance to soybean sudden death syndrome and root colonization by Fusarium solani f. sp. glycines in near-isogeneic lines. Crop Sci 38:472–477

    Article  Google Scholar 

  • Njiti VN, Meksem K, Iqbal MJ, Johnson JE, Kassem MA, Zobrist KF, Kilo VY, Lightfoot DA (2002) Common loci underlie resistance to soybean sudden death syndrome in ‘Forrest’, ‘Pyramid’, ‘Essex’ and ‘Douglas’. Theor Appl Genet 104:294–300

    Article  CAS  PubMed  Google Scholar 

  • Parker DR, Bertsch PM (1992) Formation of the “Al13” tridecameric polycation under diverse synthesis conditions. Environ Sci Technol 26:914–921

    Article  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 Integr Plant Biol 50:1089–1095

    Article  CAS  PubMed  Google Scholar 

  • Rengel Z, Robinson DL (1989) Aluminum effects on growth and macronutrient uptake by annual ryegrass. Agron J 81:208–215

    Article  CAS  Google Scholar 

  • Ruben E, Aziz J, Afzal J, Njiti VN, Triwitayakorn K, Iqbal MJ, Yaegashi S, Arelli PR, Town CD, Ishihara H, Meksem K, Lightfoot DA (2006) Genomic analysis of the ‘Peking’ rhg1 locus: candidate genes that underlie soybean resistance to the cyst nematode. Mol Genet Genomics 276:320–330

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sanchez PA, Salinas JG (1981) Low input technology for managing Oxisols and Ultisols in tropical America. Adv Agron 34:279–406

    Article  CAS  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Hideo S, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress: up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  CAS  PubMed  Google Scholar 

  • Triwitayakorn K, Njiti VN, Iqbal MJ, Yaegashi S, Town CD, Lightfoot DA (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome/Génome 48:125–138

    Article  CAS  Google Scholar 

  • Villagarcia MR, Carter TE Jr, 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 

  • Wang S, Basten CJ, Zeng Z-B (2005) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, USA. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. Accessed 14 Apr 2010

  • Yuan J, Njiti VN, Meksem K, Iqbal MJ, Triwitayakorn K, Kassem MA, Davis GT, Schmidt ME, Lightfoot DA (2002) Quantitative trait loci in two soybean recombinant inbred line populations segregating for yield and disease resistance. Crop Sci 42:271–277

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded over the past 11 years in part by grants from the NSF 9872635, ISA 95-122-04; 98-122-02 and 02-127-03 and USB 2228-6228. The integrated genetic and physical map was based upon work supported by the National Science Foundation under Grant No. 9872635. Any opinions, findings, and conclusions or recommendations expressed in this material were those of the author(s) and do not necessarily reflect the views of the National Science Foundation or United States Department of Agriculture. The support of SIUC, College of Agriculture and Office of the Vice Chancellor for Research to DAL was appreciated. The authors thank James H. Klein III, Drs. P. Gibson, O. Myers Jr. and M. Schmidt for assistance with germplasm development and maintenance from 1991 to 2000. We thank the “Soybean Genome Project”, at “DoE Joint Genome Institute” for release of the WGS reads, scaffolds and genome sequence.

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Author notes

  1. Aman D. Sharma

    Present address: Department of Soil Science, University of Florida, Gainesville, FL, USA

  2. Hemlata Sharma

    Present address: Department of Plant Breeding and Genetics, Rajasthan College of Agriculture, Udaipur, India

Authors and Affiliations

  1. Plant Biotechnology and Genomics Core-Facility, Department of Plant, Soil, and Agricultural Systems, Southern Illinois University, Carbondale, IL, 62901, USA

    Aman D. Sharma, Hemlata Sharma & David A. Lightfoot

  2. Center for Excellence, The Illinois Soybean Center, Southern Illinois University, Carbondale, IL, 62901, USA

    David A. Lightfoot

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  1. Aman D. Sharma
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  2. Hemlata Sharma
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  3. David A. Lightfoot
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Correspondence to David A. Lightfoot.

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Communicated by M. Bohn.

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Sharma, A.D., Sharma, H. & Lightfoot, D.A. The genetic control of tolerance to aluminum toxicity in the ‘Essex’ by ‘Forrest’ recombinant inbred line population. Theor Appl Genet 122, 687–694 (2011). https://doi.org/10.1007/s00122-010-1478-3

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  • DOI: https://doi.org/10.1007/s00122-010-1478-3

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