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Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery

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Abstract

Aluminum (Al) toxicity is an important abiotic stress that affects soybean production in acidic soils throughout the world. Development of Al-tolerant cultivars is an efficient and environmentally friendly solution to the problem. A previous report identified quantitative trait loci (QTL) for Al tolerance inherited from PI 416937, using restriction fragment length polymorphism markers, in a population of Young × PI 416937. The population was genotyped with 162 simple sequence repeats to enhance the power of QTL detection and enable the selection of candidate genes for functional marker development. Two QTL that explained 54 % of the phenotypic variation in root extension under Al stress conditions (HIAL) were refined on chromosomes (chr) Gm08 and Gm16. Three QTL located on chr Gm08, Gm16 and Gm19 explained 59 % of the phenotypic variation in root extension as a percent of control (PC). Two major QTL, designated qAL_HIAL_08 and qAL_PC_08, controlling HIAL and PC, respectively, were mapped to the same genomic region on chr Gm08 and inherited their favorable allele from PI 416937. These QTL explained 45 and 41 % of phenotypic variation in HIAL and PC, respectively. Six homologues for citrate synthase (CS) genes were found in the soybean genome sequence at chr Gm02, Gm08, Gm14, Gm15, and Gm18. Sixteen single nucleotide polymorphisms (SNPs) were identified in the CS homologue on chr Gm08. A SimpleProbe assay of Glyma08g42400-SNP was developed for the major QTL on chr Gm08. The SNPs identified from this region could be used for marker-assisted selection of Al tolerance.

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References

  • Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 121(3):472–480

    Article  CAS  Google Scholar 

  • Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132(4):2205–2217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barone P, Rosellini D, LaFayette P, Bouton J, Veronesi F, Parrott W (2008) Bacterial citrate synthase expression and soil aluminum tolerance in transgenic alfalfa. Plant Cell Rep 27(5):893–901

    Article  CAS  PubMed  Google Scholar 

  • Bianchi-Hall CM, Carter TEJ, Rufty TW, Arellano C, Boerma HR, Ashley DA, Burton JW (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci 38(2):513–522

    Article  CAS  Google Scholar 

  • Bianchi-Hall CM, Carter TEJ, 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(2):538–545

    Article  CAS  Google Scholar 

  • Burton J, Brim C (1987) Registration of ‘Young’soybean. Crop Sci 27:1093

    Google Scholar 

  • Caires EF, Garbuio FJ, Churka S, Barth G, Correa JCL (2008) Effects of soil acidity amelioration by surface liming on no-till corn, soybean, and wheat root growth and yield. Eur J Agron 28(1):57–64. doi:10.1016/j.eja.2007.05.002

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12(2):133–139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genet Genomics 277(5):589–600

    Article  CAS  PubMed  Google Scholar 

  • Diwan N, Cregan P (1997) Automated sizing of fluorescent-labeled simple sequence repeat (SSR) markers to assay genetic variation in soybean. Theor Appl Genetics 95(5):723–733

    Article  CAS  Google Scholar 

  • Dong D, Peng X, Yan X (2004) Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiol Plant 122(2):190–199

    Article  CAS  Google Scholar 

  • Fontecha G, Silva-Navas J, Benito C, Mestres M, Espino F, Hernandez-Riquer M, Gallego F (2007) Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theor Appl Genetics 114(2):249–260

    Article  CAS  Google Scholar 

  • Gai J, Liu Y, Lv H, Xing H, Zhao T, Yu D, Chen S (2007) Identification, inheritance and QTL mapping of root traits related to tolerance to rhizo-spheric stresses in soybean (G. max (L.) Merr.). Frontiers Agric China 1(2):119–128

    Article  Google Scholar 

  • Gonzalez R, Ricardi M, Iusem N (2011) Atypical epigenetic mark in an atypical location: cytosine methylation at asymmetric (CNN) sites within the body of a non-repetitive tomato gene. BMC Plant Biol 11(1):94

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Han Y, Zhang W, Zhang B, Zhang S, Wang W, Ming F (2009) One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Mol Biotechnol 42(3):299–305

    Article  CAS  PubMed  Google Scholar 

  • Hiradate S, Ma JF, Matsumoto H (2007) Strategies of plants to adapt to mineral stresses in problem soils. In: Advances in agronomy, vol 96. Advances in agronomy. Elsevier Academic Press Inc, San Diego, pp 65–132. doi:10.1016/s0065-2113(07)96004-6

  • Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103(25):9738–9743. doi:10.1073/pnas.0602868103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hudak C, Patterson R (1995) Vegetative growth analysis of a drought-resistant soybean plant introduction. Crop Sci 35(2):464–471

    Article  Google Scholar 

  • Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152(3):1203

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keim P, Shoemaker RC, Palmer RG (1989) Restriction fragment length polymorphism diversity in soybean. Theor Appl Genetics 77:786–792

    Article  CAS  Google Scholar 

  • King CA, Purcell LC, Brye KR (2009) Differential wilting among soybean genotypes in response to water deficit. Crop Sci 49(1):290–298

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274(1–2):175–195. doi:10.1007/s11104-004-1158-7

    Article  CAS  Google Scholar 

  • Lee SH, Bailey MA, Mian MAR, Carter TE, 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 Genetics 93(5–6):649–657

    Article  CAS  Google Scholar 

  • Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the Intact root system. Plant Physiol 141(2):674–684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • López-Marín H, Rao I, Blair M (2009) Quantitative trait loci for root morphology traits under aluminum stress in common bean (Phaseolus vulgaris L.). Theor Appl Genetics 119(3):449–458. doi:10.1007/s00122-009-1051-0

    Article  Google Scholar 

  • Ma JF (2007) Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol 264:225–252

    Article  CAS  PubMed  Google Scholar 

  • Meer J, Manly K, Cudmore Jr R (2002) User manual for map manager QTX. Roswell Park Cancer Institute Buffalo, 1–182

  • Meyer JDF, Silva DCG, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA, Graham MA (2009) Identification and analyses of candidate genes for Rpp4-mediated resistance to Asian soybean rust in soybean. Plant Physiol 150(1):295–307. doi:10.1104/pp.108.134551

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mian MAR, Bailey MA, Ashley DA, Wells R, Carter TE, Parrott WA, Boerma HR (1996) Molecular markers associated with water use efficiency and leaf ash in soybean. Crop Sci 36(5):1252–1257

    Article  CAS  Google Scholar 

  • Narasimhamoorthy B, Bouton J, Olsen K, Sledge M (2007) Quantitative trait loci and candidate gene mapping of aluminum tolerance in diploid alfalfa. Theor Appl Genetics 114(5):901–913

    Article  CAS  Google Scholar 

  • Narvel JM, Carter TE Jr, Jakkula LR, Alvernaz J, Bailey MA, Mian MAR, Lee SH, Lee GJ, Boerma HR (2004) Registration of NC113 soybean mapping population. Crop Sci 44(2):704–706

    Google Scholar 

  • Pantalone VR, Rebetzke GJ, Burton JW, Carter TE (1996) Phenotypic evaluation of root traits in soybean and applicability to plant breeding. Crop Sci 36(2):456–459

    Article  Google Scholar 

  • Peiffer GA, King K, Severin A, May GD, Cianzio SR, Lin S-f, Lauter NC, Shoemaker R (2012) Identification of candidate genes underlying an iron efficiency QTL in soybean. Plant Physiol 158(4):1745–1754. doi:10.1104/pp.111.189860

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum-resistance mechanisms in wheat (roles of root apical phosphate and malate exudation). Plant Physiol 112(2):591

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pham A-T, McNally K, Abdel-Haleem H, Roger Boerma H, Li Z (2013) Fine mapping and identification of candidate genes controlling the resistance to southern root-knot nematode in PI 96354. Theor Appl Genetics 126(7):1825–1838. doi:10.1007/s00122-013-2095-8

    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(9):1089–1095. doi:10.1111/j.1744-7909.2008.00682.x

    Article  CAS  PubMed  Google Scholar 

  • Sadok W, Sinclair TR (2009) Genetic variability of transpiration response to vapor pressure deficit among soybean (Glycine max [L.] Merr.) genotypes selected from a recombinant inbred line population. Field Crops Res 113(2):156–160

    Article  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-C, 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 

  • Shen R, Iwashita T, Ma JF (2004) Form of Al changes with Al concentration in leaves of buckwheat. J Exp Bot 55(394):131

    Article  CAS  PubMed  Google Scholar 

  • Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123(2):543–552. doi:10.1104/pp.123.2.543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Silva IR, Smyth TJ, Israel DW, Raper CD, Rufty TW (2001a) Magnesium ameliorates aluminum rhizotoxicity in soybean by increasing citric acid production and exudation by roots. Plant Cell Physiol 42(5):546–554. doi:10.1093/pcp/pce067

    Article  CAS  PubMed  Google Scholar 

  • Silva IR, Smyth TJ, Israel DW, Raper CD, Rufty TW (2001b) Magnesium is more efficient than calcium in alleviating aluminum rhizotoxicity in soybean and its ameliorative effect is not explained by the Gouy-Chapman-Stern model. Plant Cell Physiol 42(5):538–545. doi:10.1093/pcp/pce066

    Article  CAS  PubMed  Google Scholar 

  • Silva IR, Smyth TJ, Israel DW, Rufty TW (2001c) Altered aluminum inhibition of soybean root elongation in the presence of magnesium. Plant Soil 230(2):223–230. doi:10.1023/a:1010384516517

    Article  CAS  Google Scholar 

  • Silva IR, Smyth TJ, Raper CD, Carter TE, Rufty TW (2001d) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiol Plant 112(2):200–210. doi:10.1034/j.1399-3054.2001.1120208.x

    Article  CAS  PubMed  Google Scholar 

  • Sloane R, Patterson R, Carter T Jr (1990) Field drought tolerance of a soybean plant introduction. Crop Sci 30(1):118–123

    Article  Google Scholar 

  • Song Q, Marek L, Shoemaker R, Lark K, Concibido V, Delannay X, Specht J, Cregan P (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genetics 109(1):122–128. doi:10.1007/s00122-004-1602-3

    Article  CAS  Google Scholar 

  • Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J Biol Chem 277(40):37741–37746. doi:10.1074/jbc.M204050200

    Article  CAS  PubMed  Google Scholar 

  • Tan M (2010) Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiol Biochem 48(1):21–26

    Article  CAS  PubMed  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(5):1499–1507

    Article  Google Scholar 

  • Wang S, Basten C, Zeng Z (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC

  • Wang D, Ma Y, Yang Y, Liu N, Li C, Song Y, Zhi H (2011a) Fine mapping and analyses of R SC8 resistance candidate genes to soybean mosaic virus in soybean. Theor Appl Genetics 122(3):555–565. doi:10.1007/s00122-010-1469-4

    Article  Google Scholar 

  • Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J, Fu BY, Li ZK (2011b) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62(6):1951

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe T, Osaki M, Yoshihara T, Tadano T (1998) Distribution and chemical speciation of aluminum in the Al accumulator plant. Melastoma malabathricum L. Plant Soil 201(2):165–173

    Article  CAS  Google Scholar 

  • Watanabe T, Jansen S, Osaki M (2005) The beneficial effect of aluminium and the role of citrate in Al accumulation in Melastoma malabathricum. New Phytol 165(3):773–780

    Article  CAS  PubMed  Google Scholar 

  • Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265(1):17–29. doi:10.1007/s11104-005-0693-1

    Article  CAS  Google Scholar 

  • Zeng ZB, Kao CH, Basten CJ (1999) Estimating the genetic architecture of quantitative traits. Genet Res 74(03):279–289

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126(6):1189–1201

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Cheng H, Geng L, Kan G, Cui S, Meng Q, Gai J, Yu D (2009) Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica 167(3):313–322

    Article  CAS  Google Scholar 

  • Zhong L, Xu Y, Wang J (2009) DNA-methylation changes induced by salt stress in wheat Triticum aestivum. Afr J Biotechnol 8(22):6201–6207

    CAS  Google Scholar 

  • Zhou LL, Bai GH, Ma HX, Carver BF (2007) Quantitative trait loci for aluminum resistance in wheat. Mol Breeding 19(2):153–161

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by funds allocated to the Georgia Agricultural Experiment Stations and grants from the United Soybean Board.

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Authors and Affiliations

  1. Institute of Plant Breeding, Genetics and Genomics, Center for Applied Genetic Technologies, University of Georgia, 111 Riverbend Rd., Athens, GA, 30602, USA

    Hussein Abdel-Haleem, H. Roger Boerma & Zenglu Li

  2. USDA-ARS, Raleigh, NC, 27695, USA

    Thomas E. Carter Jr.

  3. Department of Crop Science, North Carolina State University, Raleigh, NC, 27695, USA

    Thomas E. Carter Jr. & Thomas W. Rufty

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  1. Hussein Abdel-Haleem
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  2. Thomas E. Carter Jr.
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  3. Thomas W. Rufty
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Correspondence to Hussein Abdel-Haleem.

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Abdel-Haleem, H., Carter, T.E., Rufty, T.W. et al. Quantitative trait loci controlling aluminum tolerance in soybean: candidate gene and single nucleotide polymorphism marker discovery. Mol Breeding 33, 851–862 (2014). https://doi.org/10.1007/s11032-013-9999-5

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