Theoretical and Applied Genetics

, Volume 119, Issue 3, pp 449–458 | Cite as

Quantitative trait loci for root morphology traits under aluminum stress in common bean (Phaseolus vulgaris L.)

  • Hernán D. López-Marín
  • Idupulapati M. Rao
  • Matthew W. Blair
Original Paper


Aluminum (Al) toxicity is a major limiting factor of crop production in acid soils, which are found mostly in developing countries of the tropics and sub-tropics. Common bean (Phaseolus vulgaris L.) is particularly sensitive to Al toxicity; and development of genotypes with better root growth in Al-toxic soils is a priority. The objectives of the present study were to physiologically assess root architectural traits in a recombinant inbred line (RIL) population of common bean that contrasts for Al resistance (DOR364 × G19833) and to identify quantitative trait loci (QTL) controlling root growth under two nutrient solutions, one with 20 μM Al concentration and the other without Al, both at pH 4.5. A total of 24 QTL were found through composite interval mapping analysis, 9 for traits under Al treatment, 8 for traits under control treatment, and 7 for relative traits. Root characteristics expressed under Al treatment were found to be under polygenic control, and some QTL were identified at the same location as QTL for tolerance to low phosphorous stress, thus, suggesting cross-links in genetic control of adaptation of common bean to different abiotic stresses.


Quantitative Trait Locus Common Bean Total Root Length Transgressive Segregation Specific Root Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Average root diameter


Distal part of the transition zone


Elongation zone


Linkage group


Average number of root tips


Root dry weight


Recombinant inbred line


Specific root length


Tap root elongation rate


Total root length



The authors duly acknowledge the partial financial support to CIAT from BMZ/GTZ, Germany through a restricted core project (No. 05.7860.9-001.00) entitled “Fighting drought and aluminum toxicity: Integrating functional genomics, phenotypic screening and participatory evaluation with women and small-scale farmers to develop stress-resistant common bean and Brachiaria for the tropics”. Our thanks also go to S. Beebe, W. Horst, A. F. Rangel, G. Manrique, G. Machado and M. C. Duque for their advice on germplasm, phenotypic screening and statistical analysis.


  1. Alonso-Blanco C, Koornneef M (2000) Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci 5:22–29PubMedCrossRefGoogle Scholar
  2. Arruda P, Jorge R (1997) Aluminum induced organic acid exudation by roots of an aluminum-tolerant tropical maize. Phytochemistry 45:675–681CrossRefGoogle Scholar
  3. Beebe SE, Rojas-Pierce M, Yan XL, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423CrossRefGoogle Scholar
  4. Blair MW, Pedraza F, Buendía HF, Gaitán-Solís E, Beebe SE, Gepts P, Thome J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374PubMedCrossRefGoogle Scholar
  5. Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Venderleyden J (2003) Bean (Phaseolus spp)—model food legumes. Plant Soil 252:55–128CrossRefGoogle Scholar
  6. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedGoogle Scholar
  7. Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.): II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702PubMedGoogle Scholar
  8. Foy CD (1984) Physiological effects of hydrogen, aluminium and manganese toxicities in acid soils. In: Adams F (ed) Soil acidity, liming. American Society of Agronomy, Wisconsin, pp 57–97Google Scholar
  9. Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, Howell SH, Kochian LV (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132:936–948PubMedCrossRefGoogle Scholar
  10. Horst WJ, Schmohl N, Baluška F, Sivaguru M (1999) Does aluminium affect root growth of maize through interaction with the cell wall–plasma membrane-cytoskeleton continuum? Plant Soil 215:163–174CrossRefGoogle Scholar
  11. Ishikawa S, Wagatsuma T, Sasaki R, Ofei-Manu P (2000) Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species. Soil Sci Plant Nutr 46:751–758Google Scholar
  12. Kerven GL, Edwards DG, Asher CJ, Hallman PS, Kobot S (1989) Aluminium determination in soil solution. II. Short-term colorimetric procedure for the measurement of inorganic monomeric aluminium in the presence of organic acid ligands. Aust J Soil Res 27:91–102CrossRefGoogle Scholar
  13. Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352PubMedCrossRefGoogle Scholar
  14. Kobayashi Y, Koyama H (2002) QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol 43:1526–1533PubMedCrossRefGoogle Scholar
  15. Kobayashi Y, Furuta Y, Ohno T, Hara T, Koyama H (2005) Quantitative trait loci controlling aluminium tolerance in two accessions of Arabidopsis thaliana (Landsberg erecta and Cape Verde Islands). Plant Cell Environ 28:1516–1524CrossRefGoogle Scholar
  16. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46:237–260CrossRefGoogle Scholar
  17. 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 55:459–493PubMedCrossRefGoogle Scholar
  18. Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956PubMedCrossRefGoogle Scholar
  19. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum resistant cultivar. Plant Physiol 126:397–410PubMedCrossRefGoogle Scholar
  20. Lee EH, Foy CD (1986) Aluminum tolerance of two snapbean cultivars related to organic acid content evaluated by high-performance liquid chromatography. J Plant Nutr 9:1481–1498CrossRefGoogle Scholar
  21. Liao H, Yan X, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31:953–970Google Scholar
  22. 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 141:674–684PubMedCrossRefGoogle Scholar
  23. Llugany M, Poschenrieder C, Barceló J (1995) Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiol Plant 93:265–271CrossRefGoogle Scholar
  24. Ma Z, Miyasaka S (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865PubMedCrossRefGoogle Scholar
  25. Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997) Detoxifying aluminum with buckwheat. Nature 390:569–570CrossRefGoogle Scholar
  26. Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefGoogle Scholar
  27. Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y (2002) Responce of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol 43:652–659PubMedCrossRefGoogle Scholar
  28. Magalhaes JV, Garvin DF, Wang Y, Sorrels M, Klein P, Shaffert R, Li L, Kochian LV (2004) Comparative mapping of major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167:1905–1914PubMedCrossRefGoogle Scholar
  29. Magalhaes JV, Liu JP, Guimarães CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Piñeros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genetics 39:1156–1161CrossRefGoogle Scholar
  30. Miyasaka S, Bute J, Howell R, Foy C (1991) Mechanisms of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol 96:737–746PubMedCrossRefGoogle Scholar
  31. Nguyen VT, Burrow MD, Nguyen HT, Le BT, Le TD, Paterson AH (2001) Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theor Appl Genet 102:1002–1010CrossRefGoogle Scholar
  32. Nguyen VT, Nguyen BD, Sarkarung S, Martinez C, Paterson AH, Nguyen HT (2002) Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Gen Genomics 267:772–780CrossRefGoogle Scholar
  33. Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source. Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593PubMedGoogle Scholar
  34. Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum tolerance mechanism in maize (Zea mays L.). Planta 196:788–795CrossRefGoogle Scholar
  35. Piñeros MA, Magalhaes JV, Alves MCV, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiol 129:1194–1206PubMedCrossRefGoogle Scholar
  36. Rangel AF, Mobin M, Rao IM, Horst WJ (2005) Proton toxicity interferes with the screening of common bean (Phaseolus vulgaris L.) genotypes for aluminium resistance in nutrient solution. J Plant Nutr Soil Sci 168:607–616CrossRefGoogle Scholar
  37. Rangel AF, Rao IM, Horst WJ (2007) Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. J Exp Bot 58:3895–3904PubMedCrossRefGoogle Scholar
  38. Rao IM (2002) Role of physiology in improving crop adaptation to abiotic stresses in the tropics: The case of common bean and tropical forages. In: Pessarakli M (ed) Handbook of plant, crop physiology. Marcel Dekker Inc., New York, pp 583–613Google Scholar
  39. Rao IM, Zeigler RS, Vera R, Sarkarung S (1993) Selection and breeding for acid-soil tolerance in crops: upland rice and tropical forages as case studies. BioScience 43:454–465CrossRefGoogle Scholar
  40. Rincón M, Gonzales R (1992) Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol 99:1021–1028PubMedCrossRefGoogle Scholar
  41. 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 44:437–446CrossRefGoogle Scholar
  42. Samac DA, Tesfaye M (2003) Plant improvement for tolerance to aluminum in acid soils—a review. Plant Cell Tissue Organ Cult 75:189–207CrossRefGoogle Scholar
  43. SAS Institute (1999) SAS/STAT User’s guide version 8. Cary, North Carolina, pp 3884Google Scholar
  44. Shen H, Yan X, Cai K, Matsumoto H (2004) Differential Al resistance and citrate secretion in the tap and basal roots of common bean seedlings. Physiol Plant 121:595–603CrossRefGoogle Scholar
  45. Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116:155–163CrossRefGoogle Scholar
  46. Sivaguru M, Baluška F, Volkmann D, Felle HH, Horst WJ (1999) Impacts of aluminum on the cytoskeleton of maize root apex. Short-term effect on the distal part of the transition zone. Plant Physiol 119:1073–1082PubMedCrossRefGoogle Scholar
  47. Thung M, Rao IM (1999) Integrated management of abiotic stresses. In: Singh SP (ed) Common bean improvement in the twenty-first century. Kluwer, DordrechtGoogle Scholar
  48. Tice KR, Parker DR, DeMason DA (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiol 100:309–318PubMedCrossRefGoogle Scholar
  49. von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15CrossRefGoogle Scholar
  50. Wang S, Basten CJ, Zeng ZB (2006) Windows QTL cartographer v2.5. Statistical genetics. North Carolina State University, Raleigh Google Scholar
  51. Wu P, Liao CY, Hu B, Yi KK, Ni JJ, He C (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genetics 100:1295–1303CrossRefGoogle Scholar
  52. Xue Y, Wan JM, Jiang L, Liu LL, Su N, Zhai HQ, Ma JF (2006) QTL analysis of aluminum resistance in rice (Oryza sativa L.). Plant Soil 287:375–383CrossRefGoogle Scholar
  53. Yan XL, 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 265:17–29CrossRefGoogle Scholar
  54. Zheng SJ, Yang JL (2005) Target sites of aluminum phytotoxicity. Biol Plant 49:321–331CrossRefGoogle Scholar
  55. Zheng SJ, Ma JF, Matsumoto H (1998a) Continuous secretion of organic acids is related to aluminum resistance during relatively long-term exposure to aluminum stress. Physiol Plant 103:209–214CrossRefGoogle Scholar
  56. Zheng SJ, Ma JF, Matsumoto H (1998b) High aluminum resistance in buckwheat: I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol 117:745–751CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Hernán D. López-Marín
    • 1
  • Idupulapati M. Rao
    • 1
  • Matthew W. Blair
    • 1
    • 2
  1. 1.CIAT, International Center for Tropical AgricultureMiamiUSA
  2. 2.CaliColombia

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