Skip to main content

Advertisement

SpringerLink
Log in

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

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

Abstract

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.

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
Fig. 2

Similar content being viewed by others

Abbreviations

ARD:

Average root diameter

DTZ:

Distal part of the transition zone

EZ:

Elongation zone

LG:

Linkage group

NRT:

Average number of root tips

RDW:

Root dry weight

RIL:

Recombinant inbred line

SRL:

Specific root length

TRE:

Tap root elongation rate

TRL:

Total root length

References

  • Alonso-Blanco C, Koornneef M (2000) Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci 5:22–29

    Article  PubMed  CAS  Google Scholar 

  • Arruda P, Jorge R (1997) Aluminum induced organic acid exudation by roots of an aluminum-tolerant tropical maize. Phytochemistry 45:675–681

    Article  Google Scholar 

  • 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 46:413–423

    Article  CAS  Google Scholar 

  • 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 107:1362–1374

    Article  PubMed  CAS  Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Venderleyden J (2003) Bean (Phaseolus spp)—model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • 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 103:695–702

    PubMed  CAS  Google Scholar 

  • 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 57–97

    Google Scholar 

  • 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 132:936–948

    Article  PubMed  CAS  Google Scholar 

  • 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 215:163–174

    Article  CAS  Google Scholar 

  • 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 46:751–758

    CAS  Google Scholar 

  • 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 27:91–102

    Article  CAS  Google Scholar 

  • 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 52:1339–1352

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Koyama H (2002) QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol 43:1526–1533

    Article  PubMed  CAS  Google Scholar 

  • 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 28:1516–1524

    Article  CAS  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 55:459–493

    Article  PubMed  CAS  Google Scholar 

  • 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 122:945–956

    Article  PubMed  CAS  Google Scholar 

  • 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 126:397–410

    Article  PubMed  CAS  Google Scholar 

  • 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 9:1481–1498

    Article  CAS  Google Scholar 

  • 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 31:953–970

    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 141:674–684

    Article  PubMed  CAS  Google Scholar 

  • 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 93:265–271

    Article  CAS  Google Scholar 

  • Ma Z, Miyasaka S (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865

    Article  PubMed  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997) Detoxifying aluminum with buckwheat. Nature 390:569–570

    Article  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  PubMed  CAS  Google Scholar 

  • 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 43:652–659

    Article  PubMed  CAS  Google Scholar 

  • 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 167:1905–1914

    Article  PubMed  CAS  Google Scholar 

  • 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 39:1156–1161

    Article  CAS  Google Scholar 

  • Miyasaka S, Bute J, Howell R, Foy C (1991) Mechanisms of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol 96:737–746

    Article  PubMed  CAS  Google Scholar 

  • 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 102:1002–1010

    Article  CAS  Google Scholar 

  • 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 267:772–780

    Article  CAS  Google Scholar 

  • 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 106:583–593

    PubMed  CAS  Google Scholar 

  • Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum tolerance mechanism in maize (Zea mays L.). Planta 196:788–795

    Article  CAS  Google Scholar 

  • 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 129:1194–1206

    Article  PubMed  CAS  Google Scholar 

  • 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 168:607–616

    Article  CAS  Google Scholar 

  • 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 58:3895–3904

    Article  PubMed  CAS  Google Scholar 

  • 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 583–613

    Google Scholar 

  • 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 43:454–465

    Article  Google Scholar 

  • Rincón M, Gonzales R (1992) Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol 99:1021–1028

    Article  PubMed  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 

  • Samac DA, Tesfaye M (2003) Plant improvement for tolerance to aluminum in acid soils—a review. Plant Cell Tissue Organ Cult 75:189–207

    Article  CAS  Google Scholar 

  • SAS Institute (1999) SAS/STAT User’s guide version 8. Cary, North Carolina, pp 3884

  • 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 121:595–603

    Article  CAS  Google Scholar 

  • Sivaguru M, Horst WJ (1998) The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol 116:155–163

    Article  CAS  Google Scholar 

  • 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 119:1073–1082

    Article  PubMed  CAS  Google Scholar 

  • Thung M, Rao IM (1999) Integrated management of abiotic stresses. In: Singh SP (ed) Common bean improvement in the twenty-first century. Kluwer, Dordrecht

    Google Scholar 

  • Tice KR, Parker DR, DeMason DA (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiol 100:309–318

    Article  PubMed  CAS  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 S, Basten CJ, Zeng ZB (2006) Windows QTL cartographer v2.5. Statistical genetics. North Carolina State University, Raleigh 

    Google Scholar 

  • 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 100:1295–1303

    Article  CAS  Google Scholar 

  • 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 287:375–383

    Article  CAS  Google Scholar 

  • 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 265:17–29

    Article  CAS  Google Scholar 

  • Zheng SJ, Yang JL (2005) Target sites of aluminum phytotoxicity. Biol Plant 49:321–331

    Article  CAS  Google Scholar 

  • 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 103:209–214

    Article  CAS  Google Scholar 

  • 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 117:745–751

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. CIAT, International Center for Tropical Agriculture, 1380 N.W. 78th Ave, Miami, FL, 33126, USA

    Hernán D. López-Marín, Idupulapati M. Rao & Matthew W. Blair

  2. A. A. 6713, Cali, Colombia

    Matthew W. Blair

Authors
  1. Hernán D. López-Marín
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Idupulapati M. Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew W. Blair
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew W. Blair.

Additional information

Communicated by F. Muehlbauer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1051-0

Keywords

Search

Navigation