, Volume 181, Issue 3, pp 385–404 | Cite as

New genetic sources of resistance in the genus Phaseolus to individual and combined aluminium toxicity and progressive soil drying stresses

  • Louis Butare
  • Idupulapati Rao
  • Philippe Lepoivre
  • José Polania
  • César Cajiao
  • Juan Cuasquer
  • Stephen BeebeEmail author


Bean species and genotypes show wide phenotypic variability in relation to aluminium (Al) resistance and progressive soil drying. The objective of this study was to identify and characterize sources of resistance to Al toxicity and progressive soil drying among six genotypes of common bean (Phaseolus vulgaris), four of runner bean (P. coccineus), and one of tepary bean (P. acutifolius), using hydroponic and soil cylinder screening methods. One experiment on hydroponic screening of Al resistance was carried out using a basal nutrient solution with and without 20 μM Al. Two experiments were carried out using two oxisols in 80 cm long soil cylinders with high Al (HAl) and low Al (LAl) saturation treatments. The three experiments showed an average of 36.9–53.5% inhibition of root growth with HAl compared with LAl treatments. Differences in root development and distribution were observed among genotypes and species. Two accessions of P. coccineus (G35346-2Q, G35464-5Q) and one Andean common bean genotype (ICA Quimbaya) were outstanding in root and shoot growth in the HAl treatments. P. coccineus accession (G35346-3Q) was outstanding under combined stress of Al-toxic acid soil and progressive soil drying. Accessions of P. coccineus may represent unique sources of Al resistance for the improvement of common bean through interspecific crosses.


Abiotic stress Acid soil Aluminium resistance Root growth Screening methods Water stress 



High aluminium soil saturation


Leaf area


Low aluminium soil saturation


Mean root diameter


Number of root tips


Root dry weight


Ryan–Einot–Gabriel–Welsh Multiple Test


Root to shoot


Shoot dry weight


Specific root length


Tap root length at 48 h of exposure to with and without aluminium in solution


Tap root length at 120 h of exposure to with and without aluminium in solution


Tap root elongation rate


Total root length


Visual rooting depth at 29 days


Visual rooting depth at 33 days


Water stress


Well watered



This research was supported by Bundesministerium für Wirtschaftliche Zusammenarbeit und Entwicklung (BMZ) 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”. We are very grateful to research support staff of CIAT bean program for their assistance in data collection and processing.


  1. Armiger WH, Foy CD, Fleming AL, Caldwell BE (1968) Differential tolerance of soybean varieties to an acid soil high in exchangeable aluminum. Agron J 60:67–70CrossRefGoogle Scholar
  2. Bianchi-Hall CM, Carter TE Jr, Rufty TW, Arellano C, Boerma HR, Ahley DA, Burton JW (1998) Heritability and resource allocation of aluminum tolerance derived from soybean PI 416937. Crop Sci 38:513–522CrossRefGoogle Scholar
  3. 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 PI416937 in hydroponics. Crop Sci 40:538–545CrossRefGoogle Scholar
  4. Blair MW, López-Marín HD, Rao IM (2009) Identification of aluminum resistant Andean genotypes of common bean (Phaseolus vulgaris L.). Braz J Plant Physiol 21(4):291–300CrossRefGoogle Scholar
  5. Campbell KAG, Carter TE Jr (1990) Aluminum tolerance in soybean. I. Genotypic correlation and repeatability of solution culture and greenhouse screening methods. Crop Sci 30:1049–1054CrossRefGoogle Scholar
  6. Carter TE Jr, Rufty TW (1993) Soybean plant introductions exhibiting drought and aluminum tolerance. In: Kuo CG (ed) Adaptation of food crops to temperature and water stress: proceedings of an international symposium, Taiwan, 13–18 Aug 1992. Publi. no. 93-410. Asian Vegetable Research and Development Center, Shanhua, pp 335–346Google Scholar
  7. Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260CrossRefGoogle Scholar
  8. Choi HK, Mun JH, Jin Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB et al (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294PubMedCrossRefGoogle Scholar
  9. CIAT (2005) Bean improvement for the tropics. Project IP-1, annual report 2005. CaliGoogle Scholar
  10. CIAT (2008) Improved beans for the developing world. Outcome line SBA-1. Annual report 2008. CaliGoogle Scholar
  11. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321PubMedGoogle Scholar
  12. Devine TE, Foy CD, Mason DL, Fleming AL (1979) Aluminum tolerance in soybean germplasm. Soybean Genet Newsl (Ames) 6:763–782Google Scholar
  13. Eisenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  14. Eticha D, Zahn M, Bremer M, Yang Z, Rangel AF, Rao IM, Horst WJ (2010) Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Ann Bot 105:1119–1128PubMedCrossRefGoogle Scholar
  15. Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plant Anal 19:959–987CrossRefGoogle Scholar
  16. Foy CD, Fleming AL, Armiger WJ (1969) Aluminum tolerance of soybean varieties in relation to calcium nutrition. Agron J 61:505–511CrossRefGoogle Scholar
  17. Foy CD, Duke JA, Devine TE (1992) Tolerance of soybean germplasm to an acid tatum subsoil. J Plant Nutr 15:527–547CrossRefGoogle Scholar
  18. Gale MR, Grigal DF (1987) Vertical root distribution of northern tree species in relation to successional status. Can J For Res 17:829–834CrossRefGoogle Scholar
  19. Girdthai T, Joglory S, Kesmala T, Vorasoot N, Akkasaeng C, Wongkaew S, Holbrook CC, Patanothai A (2010) Relationship between root characteristics of peanut in hydroponics and pot studies. Crop Sci 50:159–167CrossRefGoogle Scholar
  20. Horst WJ, Klotz F (1990) Screening soybean for aluminum tolerance and adaptation to acid soils. In: El Bassam N et al (eds) Genetic aspects of plant mineral nutrition. Kluwer Academic Publishers, Dordrecht, pp 355–360Google Scholar
  21. Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197PubMedCrossRefGoogle Scholar
  22. Johansen C, Baldev B, Brouwer JB, Erskine W, Jermyn WA, Lang LJ, Malik BA, Miah AA, Silim SN (1994) Biotic and abiotic stresses constraining productivity of cool season food legumes in Asia, Africa and Oceania. In: Muehlbauer FJ, Kaiser WJ (eds) Expanding the production and use of cool season food legumes. Kluwer Academic Publishers, Dordrecht, pp 175–194Google Scholar
  23. 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
  24. Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological causes and ecological consequences. Adv Ecol Res 23:87–261Google Scholar
  25. Lambers H, Nagel OW, van Arendonk JJCM (1995) The control of biomass partitioning in plants from “favourable” and “stressful” environments: a role for gibberellins and cytokinins. Bulg J Plant Physiol 21(2–3):24–32Google Scholar
  26. Little R (1988) Plant soil interaction at low pH: problem solving genetic approach. Commun Soil Sci Plant Anal 19:1239–1257CrossRefGoogle Scholar
  27. López-Marín HD, Rao IM, Blair MW (2009) Quantitative trait loci for aluminum toxicity resistance in common bean (Phaseolus vulgaris L.). Theor Appl Genet 119:449–458PubMedCrossRefGoogle Scholar
  28. Lynch J (1995) Update on root biology: root architecture and plant productivity. Plant Physiol 109:7–13PubMedGoogle Scholar
  29. Manrique G, Rao IM, Beebe S (2006) Identification of aluminum resistant common bean genotypes using a hydroponic screening method. Paper presented at the 18th world congress of soil science, Philadelphia, USA, 9–15 Jul 2006Google Scholar
  30. Marschner H (1991) Mechanisms of adaptation of plants to acid soils. Plant Soil 134:1–20Google Scholar
  31. Massot N, Llugany M, Poschenrieder Ch, Barcelo J (1999) Callose production production as indicator of aluminum toxicity in bean cultivars. J Plant Nutr 22:1–10CrossRefGoogle Scholar
  32. Mossor-Pietraszewska T (2001) Effect of aluminum on plant growth and metabolism. Acta Biolochim Pol 48(3):673–686Google Scholar
  33. Muñoz-Perea CG, Terán H, Allen RG, Wright JL, Westermann DT, Singh SP (2006) Selection for drought resistance in dry bean landraces and cultivars. Crop Sci 46:2111–2120CrossRefGoogle Scholar
  34. Narasimhamoorthy B, Blancaflor EB, Bouton JH, Payton ME, Sledge MK (2007) A comparison of hydroponics, soil, and root staining methods for evaluation of aluminum tolerance in Medicago truncatula (Barrel medic) germplasm. Crop Sci 47:321–328CrossRefGoogle Scholar
  35. Pandey S, Ceballos H, Mgnavaca R, Bahia Filho AFC, Duque-Vargas J, Vinasco LE (1994) Genetics of tolerance to soil acidity in tropical maize. Crop Sci 34:1511–1514CrossRefGoogle Scholar
  36. Polanía J, Rao IM, Beebe S, García R (2009) Desarrollo y distribución de raices bajo estrés por sequía en frijol común (Phaseolus vulgaris L.) en un sistema de tubos con suelo. Agron Colomb 27:25–32Google Scholar
  37. Rangel AF, Mobin M, Rao IM, Horst WJ (2005) Proton toxicity interferes with the screening of common bean (Phaseolus vulgaris L.) genotypes for aluminum resistance in nutrient solution. J Plant Nutr Soil Sci 168:607–616CrossRefGoogle Scholar
  38. Rangel AF, Rao IM, Horst WJ (2007) Spatial aluminum sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminum resistance. J Exp Bot 58:3896–3904CrossRefGoogle Scholar
  39. Rangel AF, Rao IM, Horst WJ (2009) Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris L.) genotypes in relation to Al toxicity. Physiol Plant 135:162–173PubMedCrossRefGoogle Scholar
  40. Rangel AF, Rao IM, Braum HP, Horst WJ (2010) Aluminum resistance in common bean (Phaseolus vulgaris L.) involves induction and maintenance of citrate exudation from root apices. Physiol Plant 138:176–190PubMedCrossRefGoogle Scholar
  41. Rao IM (2001) 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 and crop physiology. Marcel Dekker, Inc., New York, pp 583–613Google Scholar
  42. Rao IM, Beebe S, Ricaurte J, Teran H, Singh S (2004) Common bean (Phaseolus vulgaris L.) genotypes tolerant to aluminum-toxic soils in the tropics. In: Matsumoto H, Nanzyo M, Inubushi K, Yamamoto Y, Koyama H, Saigusa M, Osaki M, Sakurai K (eds) Proceedings of the 6th international symposium on plant–soil interactions at low pH. Japanese Society of Soil Science and Plant Nutrition (JSSSPN), pp 272–273Google Scholar
  43. Rao IM, Beebe S, Ricaurte J, Cajiao C, Polania J, Garcia R (2007) Phenotypic evaluation of drought resistance in advanced lines of common bean (Phaseolus vulgaris L.). Paper presented at ASA-CSSA-SSSA international annual meeting, New Orleans, LA, USA, 4–8 Nov 2007Google Scholar
  44. Ryan PR, DiTomaso JM, Kochian LV (1993) Aluminum toxicity in roots: an investigation of spatial sensitivity and the role of the cap. J Exp Bot 44:437–446CrossRefGoogle Scholar
  45. Ryser P, Lambers H (1995) Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant Soil 170:251–265CrossRefGoogle Scholar
  46. Sapra VT, Mebrahtu T, Mugwira LM (1982) Soybean germplasm and cultivar aluminum tolerance in nutrient solution and Bladen clay loam soil. Agron J 74:687–690CrossRefGoogle Scholar
  47. Silva IR, Smyth TJ, Israel DW, Rufty TW (2001) Altered aluminum inhibition of soybean root elongation in the presence of magnesium. Plant Soil 230:223–230CrossRefGoogle Scholar
  48. Singh SP, White JW (1988) Breeding common beans for adaptation to drought conditions. In: White JW, Hoogenboom F, Ibarra F, Singh SP (eds) Research on drought tolerance in common bean. Working Document No. 41, Bean Program. CIAT, Cali, pp 261–285Google Scholar
  49. Spehar CR (1994) Aluminum tolerance of soya bean genotypes in short term experiments. Euphytica 76:73–80CrossRefGoogle Scholar
  50. Sponchiado BN, White JW, Castillo JA, Jones PG (1989) Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Exp Agric 25:249–257CrossRefGoogle Scholar
  51. Subbarao GV, Johansen C, Slinkard AE, Nageswara Rao RC, Saxena NP, Chauhan YS (1995) Strategies for improving drought tolerance in grain legumes. Crit Rev Plant Sci 14:469–523Google Scholar
  52. Thung M, Rao IM (1999) Integrated management of abiotic stresses. In: Singh SP (ed) Common bean improvement in the twenty-first century. Kluwer Academic Publishers, Dordrecht, pp 331–370Google Scholar
  53. Urrea-Gómez R, Ceballos H, Pandey S, Bahía Filho AFC, León LA (1996) A greenhouse screening technique for acid soil tolerance in maize. Agron J 88:806–812CrossRefGoogle Scholar
  54. Villagarcia MR, Carter TE Jr, Rufty TW, Niewoehner AS, Jennette MW, Arrellano C (2001) Genotypic ranking for aluminum tolerance of soybean roots grown in hydroponics and sand culture. Crop Sci 41:1499–1507CrossRefGoogle Scholar
  55. White JW, Castillo JA (1988) Studies at CIAT on mechanisms of drought tolerance in common bean. In: White JW, Hoogenboom G, Ibarra F, Singh SP (eds) Research on drought tolerance in common bean. Centro Internacional de Agricultura Tropical, Cali, pp 146–151Google Scholar
  56. Wortmann CS, Kirkby RA, Eledu CA, Allan DJ (1998) Atlas of common bean (Phaseolus vulgaris L.) production in Africa. CIAT publication no. 297. CIAT, CaliGoogle Scholar
  57. Yang Z, Eticha D, Rao IM, Horst WJ (2010) Alteration of cell-wall porosity is involved in osmotic stress-induced enhancement of aluminum resistance in common bean (Phaseolus vulgaris L.). J Exp Bot 61:3245–3258PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Louis Butare
    • 1
    • 2
    • 3
  • Idupulapati Rao
    • 1
  • Philippe Lepoivre
    • 2
  • José Polania
    • 1
  • César Cajiao
    • 1
  • Juan Cuasquer
    • 1
  • Stephen Beebe
    • 1
    Email author
  1. 1.Centro Internacional de Agricultura Tropical (CIAT)CaliColombia
  2. 2.Université de Liège (ULg), Gembloux Agro-Bio Tech, Unité de PhytopathologieGemblouxBelgium
  3. 3.Institut des Sciences Agronomiques du Rwanda (ISAR)KigaliRwanda

Personalised recommendations