Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean

Hong Liao A B , Xiaolong Yan B , Gerardo Rubio A C , Steve E. Beebe D , Matthew W. Blair D and Jonathan P. Lynch A E

A Department of Horticulture, The Pennsylvania State University, University Park, PA 16 802, USA.

B Laboratory of Plant Nutritional Genetics and Root Biology Center, South China Agricultural University, Guangzhou 510 642, China.

C Faculty of Agronomy, University of Buenos Aires, 1417 Buenos Aires, Argentina.

D International Centre for Tropical Agriculture (CIAT), AA 6713, Cali, Colombia.

E Corresponding author; email:

Functional Plant Biology 31(10) 959-970
Submitted: 19 December 2004  Accepted: 18 August 2004   Published: 14 October 2004


Root gravitropism determines the relative distribution of plant roots in different soil layers, and therefore, may influence the acquisition of shallow soil resources such as phosphorus (P). Growth pouch and field studies were conducted to evaluate root gravitropism of common bean (Phaseolus vulgaris L.) in response to P deficiency and to detect quantitative trait loci (QTL) associated with this trait. A deep-rooted genotype, DOR364, was crossed with a shallow-rooted genotype, G19833, to obtain 86 F5.7 recombinant inbred lines (RILs). Root gravitropic traits were measured as basal root growth angle (BRGA), shallow basal root length (SBRL, basal root length in the top 0–3 cm of soil) and relative shallow basal root length (RSBRL, percentage of basal root length in the top 0–3 cm of soil relative to total basal root length). Large genetic variability for these traits was found in the parents and RILs, with BRGA ranging from –18.73 to 56.69º and SBRL ranging from 0.42 to 2.63 m per plant. The parents and six RILs with contrasting root gravitropism were further evaluated in the field, where root shallowness was significantly correlated with plant growth and P uptake. QTL were detected by single point analysis (SPA), interval mapping (IM) and composite interval mapping (CIM) techniques with a genetic map for the DOR364 × G19833 population consisting of 236 molecular markers. The IM / CIM QTL were detected among the 11 linkage groups of common bean, with 16 QTL controlling the above root traits and six QTL controlling P acquisition efficiency (PAE) in the field study. At least three of the root trait QTL were associated with QTL for PAE, suggesting that root gravitropic traits are associated with PAE and that QTL for these traits can be used to facilitate selection and breeding for higher P efficiency in common bean and other crops.

Keywords: basal root growth angle, common bean, phosphorus acquisition efficiency, root gravitropism.


Basten CJ Weir BS Zeng ZB 1999 ‘QTL Cartographer Version 1.13.’ Department of Statistics, North Carolina State University Raleigh, NC

Beebe S Pedraza F Rojas M Gutierrez J Tohme J 1998 A genetic map of common bean combining RFLP, RAPD, SCAR and AFLP markers. Annual Report of the Bean Improvement Cooperative 41 95 96

Beebe S Lynch JP Galwey N Tohme J Ochoa I 1997 A geographical approach to identify phosphorus-efficient genotypes among landraces and wild ancestors of common bean. Euphytica 95 325 336

Berta G Trotta A Fusconi A Hooker JE Munro M Atkinson D Giovannetti M Morini S Fortuna P Tisserant B 1995 Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiology 15 281 293

Blair MW Pedraza F Buendia HF Gaitán-Solís E Beebe SE Gepts P Tohme J 2003 Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theoretical and Applied Genetics 107 1362 1374

Blum A Johnson JW 1992 Transfer of water from roots into dry soil and the effect on wheat water relations and growth. Plant and Soil 145 141 149

Bonser AM Lynch JP Snapp S 1996 Effect of phosphorus deficiency on growth angle of basal roots of Phaseolus vulgaris L. New Phytologist 132 281 288

Borch K Bouma T Lynch JP Brown KM 1999 Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant, Cell and Environment 22 425 431

Bray JM Kurtz LT 1945 Determination of total organic and available forms of P in soils. Soil Science 59 39 45

Champoux MC Wang G Sarkarung S Mackill DJ O’Toole JC Huang N McCouch SR 1995 Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theoretical and Applied Genetics 90 969 981

Chu WK Chang SC 1966 Surface activity of inorganic soil phosphorus. Soil Science 101 459 464

CIAT 1991 ‘Centro Internacional de Agricultura Tropical Annual Report, 1990.’ (CIAT: Cali, Colombia)

Dellaporta SL Wood J Hicks JB 1983 A plant DNA minipreparation: version II. Plant Molecular Biology 1 19 21

Espeleta JF Eissenstat DM 1998 Responses of citrus fine roots to localized soil drying: a comparison of seedlings with adult fruiting trees. Tree Physiology 18 113 119

Fan M Zhu J Richards C Brown KM Lynch JP 2003 Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology 30 493 506

FAO Food and Agriculture Organization 1991 ‘Production yearbook 1990. Vol. 44.’ Food and Agriculture Organization Rome

Freyre R Skroch PW Geffroy V Adam-Blondon AF Shirmohamadali A Johnson WC Llaca V Nodari RO Pereira PA Tsai SM 1998 Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theoretical and Applied Genetics 97 847 856

Ge Z Rubio G Lynch J 2000 The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218 159 171 DOI

Gerloff GC Gabelman WH 1983 Genetic basis of inorganic plant nutrition. ‘Encyclopedia of plant P hysiology. Vol. 15 B’. Lauchli A Bieleski RL 453 476 Springer-Verlag New York

Gu WK Weeden NF Yu J Wallace DH 1995 Large scale, cost-effective screening of PCR products in marker-assisted selection applications. Theoretical and Applied Genetics 91 465 470

Hu B Wu P Liao CY Zhang WP Ni JJ 2001 QTLs and epistasis underlying activity of acid phosphatase under phosphorus sufficient and deficient conditions in rice (Oryza sativa L.). Plant and Soil 230 99 105

Ho MD McCannon BC Lynch JP 2004 Optimization modeling of plant root architecture for water and phosphorus acquisition. Journal of Theoretical Biology 226 331 340 DOI

Huang B 1999 Water relations and root activities of Buchloe dactyloides and Zoysia japonica in response to localized soil drying. Plant and Soil 208 179 186 DOI

Jones N Ougham H Thomas H 1997 Markers and mapping: we are all geneticists now. New Phytologist 137 165 177 DOI

Kirk GJD van Du L 1997 Changes in rice root architecture, porosity, and oxygen and proton release under phosphorus deficiency. New Phytologist 135 191 200

Lander ES Green P Abrahamson J Barlow A Daly MJ Lincoln SE Newburg L 1987 Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1 174 181

Liao H Rubio G Yan X Cao A Brown KM Lynch JP 2001 Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil 232 69 79

Lynch JP 1998 a The role of nutrient-efficient crops in modern agriculture. Journal of Crop Production 1 241 264

Lynch JP 1998 b Root architecture and phosphorus acquisition efficiency in common bean. ‘Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes’. Lynch JP Deikman J 81 91 American Society of Plant Physiologists Rockville

Lynch JP Beebe SE 1995 Adaptation of beans (Phaseolus vulgaris L.) to low phosphorus availability. HortScience 30 1165 1171

Lynch JP Brown KM 2001 Topsoil foraging — an architectural adaptation to low phosphorus availability. Plant and Soil 237 225 237

Lynch JP Ho M 2004 Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil, In press.

Lynch JP van Beem J 1993 Growth and architecture of seedling roots of common bean genotypes. Crop Science 33 1253 1257

Miller CR Ochoa I Nielsen KL Beck D Lynch JP 2003 Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Functional Plant Biology 30 973 985

Murphy J Riley J 1962 A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27 31 36 DOI

Ni JJ Wu P Senadira D Huang N 1998 Mapping QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theoretical and Applied Genetics 97 1361 1369 DOI

Pothuluri JV Kissel DE Whitney DA Thien SJ 1986 Phosphorus uptake from soil layers having different soil test phosphorus levels. Agronomy Journal 78 991 994

Price AH Tomos AD 1997 Genetic dissection of root growth in rice (Oryza sativa L.) II: mapping quantitative trait loci using molecular markers. Theoretical and Applied Genetics 95 143 152

Price AH Tomos AD Virk DS 1997 Genetic dissection of root growth in rice (Oryza sativa L.) I: a hydrophonic screen. Theoretical and Applied Genetics 95 132 142 DOI

Rubio G Walk T Ge Z Yan X Liao H Lynch JP 2001 Root gravitropism and below ground competition among neighboring plants: a modeling approach. Annals of Botany 88 929 940 DOI

Rubio G Liao H Yan X Lynch JP 2003 Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Science 43 598 607

Schuurman JJ Goedewaagen MAJ 1971 ‘Methods for the examination of root systems and roots: methods in use at the Institute for Soil Fertility for eco-morphological root investigations.’ Centre for Agricultural Publishing and Documentation Wageningen

Singh SP Urrea CA Gutierrez JA Garcia J 1989 Selection for yield at two fertilizer levels in small seeded common bean. Canadian Journal of Plant Science 69 1011 1017

Singh SP Gepts P Debouck DG 1991 Races of common bean (Phaseolus vulgaris, Fabaceae). Economic Botany 45 379 396

Stam P 1998 Crop physiology, QTL analysis and plant breeding. ‘Inherent variation in plant growth: physiological mechanisms and ecological consequences’. Lambers H 429 440 Backhuys Publishers Leiden

Thung M 1990 Phosphorus: a limiting nutrient in bean (Phaseolus vulgaris L.) production in Latin America and field screening for efficiency and response. ‘Genetic aspects of plant mineral nutrition’. El Bassam N 501 521 Kluwer Academic Publishers The Netherlands

Trotta A Carminati C Schellenbaum L Scannerini S Fusconi A Berta G 1991 Correlation between root morphogenesis, VA mycorrhizal infection and phosphorus nutrition. Developments in Agricultural and Managed-forest Ecology 24 333 339

Vallejos EC Sakiyama NS Chase CD 1992 A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 82 353 357

Vance CP Uhde-Stone C Allen DL 2003 Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157 423 447

Wilkinson L Hill M Vang E 1992 ‘SYSTAT Statistics.’ SYSTAT Inc. Evanston, PA

Wissuwa M Ae N 2001 Genotypic differences in the presence of hairs on roots and gynophores of peanuts (Arachis hypogaea L.) and their significance for phosphorus uptake. Journal of Experimental Botany 52 1703 1710

Wissuwa M Wegner J Ae N Yano M 2002 Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theoretical and Applied Genetics 105 890 897 DOI

Wortmann CS Kirkby RA Eledu CA Allen DJ 1998 ‘Atlas of common bean (Phaseolus vulgaris L.) production in Africa.’ CIAT Cali, Colombia

Wraith JM Baker JM 1991 High resolution measurement of root water uptake using automated time-domain reflectometry. Soil Science Society of America Journal 55 928 932

Yan X Lynch JP Beebe SE 1995 a Genetic variation for phosphorus efficiency of common bean in contrasting soil types: I. vegetative response. Crop Science 35 1086 1093

Yan X Lynch JP Beebe SE 1995 b Genetic variation for phosphorus efficiency of common bean in contrasting soil types: II. yield response. Crop Science 35 1094 1099

Yang M Yan X 1998 Preliminary studies on morphological and physiological mechanisms of Stylosanthes guianensis for P efficiency on an acid soil. Acta Agrestia Sinica 6 212 220

Yang M Yan X 1999 Genotypic variation of Stylosanthes guianensis in P efficiency on an acid soil of red earth region. Acta Agrestia Sinica 7 113 120

Zhang WP Wu P Hu B Liao CY 2001 QTLs and epistasis for seminal root length under a different water supply in rice (Oryza sativa L.). Theoretical and Applied Genetics 103 118 123

Zhang YJ 2002 Ethylene and phosphorus responses in plants. PhD thesis. The Pennsylvania State University PA

Zobel RW 1996 Genetic control of root systems. ‘Plant roots: the hidden half’. Waisel Y Eshel A Kafkafi U 21 30 Marcel Dekker Inc New York

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