Skip to main content

Advertisement

SpringerLink
Log in

Phenotypic evaluation and QTL analysis of yield and symbiotic nitrogen fixation in a common bean population grown with two levels of phosphorus supply

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Common bean is an important staple crop in Eastern Africa and Latin America. Low soil fertility is a major limitation to agronomic productivity. Symbiotic nitrogen fixation (SNF) is an important property of legumes, leading to high protein levels and high nutritional value. Nitrogen (N) metabolism and yield traits were evaluated in the common bean population DOR 364 × BAT 477 in field experiments under moderate and low phosphorus (P) soil conditions resembling environments found on farmers’ fields. Low P availability in soil severely limits seed yield, and trait correlations with yield reveal that high biomass as well as early maturity and efficient seed filling are important for good performance in low P stress, resembling drought resistance. Investigation of SNF and soil N uptake under low P stress showed reduced seed nitrogen levels and major variation in soil-derived N. In low P conditions, no significant reduction of %N derived from the atmosphere (%Ndfa) was observed; however, %Ndfa was correlated with yield, indicating that under stress SNF becomes an important asset. Significant genetic variation was observed for yield, yield components, and SNF ability suggesting that traits can be improved by breeding. Quantitative trait loci (QTLs) for %Ndfa and seed N concentration were discovered on chromosomes Pv07 and Pv02; independent yield QTLs were identified on the same chromosomes. Two QTL hotspots that affect several traits including yield components were found on Pv02 and Pv06; the latter represents a constitutive QTL hotspot independent from the environment. QTLs may be used for marker design and molecular breeding.

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

100SdW:

100 seed weight

SdCN:

Carbon to nitrogen ratio in seed

DF:

Days to flowering

DPM:

Days to physiological maturity

TNdfs:

Nitrogen derived from soil per hectare

TNdfa:

Nitrogen derived from the atmosphere per hectare

%Ndfa:

Percentage of nitrogen derived from the atmosphere

FVFM:

Photosynthetic efficiency on younger fully expanded leaf

LP:

Low phosphorus

MP:

Moderate phosphorus

PBH:

Pod Biomass at harvest

PHI:

Pod harvest index

PNA:

Pod number per area

QTL:

Quantitative trait locus

RIL:

Recombinant inbred line

SdC:

Seed carbon content in per cent

SdN:

Seed nitrogen content in per cent

SdN_ha:

Seed nitrogen per hectare

SdNA:

Seed number per area

ShBH:

Shoot biomass at harvest

SCMR:

SPAD chlorophyll meter reading in younger fully expanded leaf

SBH:

Stem biomass at harvest

SCOND:

Stomatal conductance on younger fully expanded leaf

Yd:

Yield per hectare

References

  • Andrews M, Lea PJ (2013) Our nitrogen “footprint”: the need for increased crop nitrogen use efficiency. Ann Appl Biol 163:165–169. doi:10.1111/aab.12052

    Article  CAS  Google Scholar 

  • Araújo SS, Beebe S, Crespi M et al (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280. doi:10.1080/07352689.2014.898450

    Article  Google Scholar 

  • Asfaw A, Blair MW (2012) Quantitative trait loci for rooting pattern traits of common beans grown under drought stress versus non-stress conditions. Mol Breed 30:681–695. doi:10.1007/s11032-011-9654-y

    Article  Google Scholar 

  • Asfaw A, Blair MW, Struik PC (2012) Multienvironment quantitative trait loci analysis for photosynthate acquisition, accumulation, and remobilization traits in common bean under drought stress. G3 (Bethesda) 2:579–595. doi:10.1534/g3.112.002303

    Article  CAS  Google Scholar 

  • Assefa T, Beebe SE, Rao IM et al (2013) Pod harvest index as a selection criterion to improve drought resistance in white pea bean. Field Crop Res 148:24–33. doi:10.1016/j.fcr.2013.04.008

    Article  Google Scholar 

  • Batjes N (1997) A world data set of derived properties by FAO-UNESCO soil unit for global modelling

  • Batjes NH (2011) Global distribution of soil phosphorus retention potential. Wageningen, Plant Research International (PRI), Wageningen UR and ISRIC Worl Soil Information. Report 6, 42

  • Beebe S (2012) Common bean breeding in the tropics. In: Janick J (ed) Plant breeding reviews. pp 357–427

  • Beebe SE, Rojas-Pierce M, Yan X et al (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423. doi:10.2135/cropsci2005.0226

    Article  CAS  Google Scholar 

  • Beebe SE, Rao IM, Cajiao C, Grajales M (2008) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci 48:582–592. doi:10.2135/cropsci2007.07.0404

    Article  Google Scholar 

  • Beebe SE, Rao IM, Blair MW, Acosta-Gallegos JA (2013) Phenotyping common beans for adaptation to drought. Front Physiol 4:1–20. doi:10.3389/fphys.2013.00035

    Article  Google Scholar 

  • Blair MW, Galeano CH, Tovar E et al (2012) Development of a Mesoamerican intra-genepool genetic map for quantitative trait loci detection in a drought tolerant × susceptible common bean (Phaseolus vulgaris L.) cross. Mol Breed 29:71–88. doi:10.1007/s11032-010-9527-9

    Article  PubMed  Google Scholar 

  • Bliss FA (1993) Breeding common bean for improved biological nitrogen fixation. Plant Soil 152:71–79

    Article  Google Scholar 

  • Bourion V, Laguerre G, Depret G et al (2007) Genetic variability in nodulation and root growth affects nitrogen fixation and accumulation in pea. Ann Bot 100:589–598. doi:10.1093/aob/mcm147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broughton WJ, Hern G, Blair M et al (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 55:55–128

    Article  Google Scholar 

  • Chavarro MC, Blair MW (2010) QTL analysis and effect of the fin locus on tropical adaptation in an inter-gene pool common bean population. Trop Plant Biol 3:204–218. doi:10.1007/s12042-010-9058-x

    Article  Google Scholar 

  • CIAT (1988) Simbiosis Leguminosa-Rizobio; manual de métodos de evaluacón, selección y manejo agronómico. Seccion Microbiologia de suelos, programa de pastos tropicales y programa de fríjol. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia

  • Cichy KA, Blair MW, Galeano CH et al (2009a) QTL analysis of root architecture traits and low phosphorus tolerance in an Andean bean population. Crop Sci 49:59–68

    Article  CAS  Google Scholar 

  • Cichy KA, Snapp SS, Blair MW (2009b) Plant growth habit, root architecture traits and tolerance to low soil phosphorus in an Andean bean population. Euphytica 165:257–268. doi:10.1007/s10681-008-9778-2

    Article  CAS  Google Scholar 

  • Ferguson B, Lin M-H, Gresshoff PM (2013) Regulation of legume nodulation by acidic growth conditions. Plant Signal Behav 8:e23426. doi:10.4161/psb.23426

    Article  PubMed  PubMed Central  Google Scholar 

  • Galeano CH, Fernandez AC, Franco-Herrera N et al (2011) Saturation of an intra-gene pool linkage map: towards a unified consensus linkage map for fine mapping and synteny analysis in common bean. PLoS One 6:e28135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall AE, Richard A, Condon AG et al (1994) Carbon isotopo discriminations and plant breeding. In: Plant breeding reviews. Ju. Wiley, Janick, pp 81–113

    Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crop Res 65:151–164. doi:10.1016/S0378-4290(99)00084-2

    Article  Google Scholar 

  • Jiang C, Gao X, Liao L et al (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470. doi:10.1104/pp.107.103788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamfwa K, Cichy KA, Kelly JD (2015) Genome-wide association analysis of symbiotic nitrogen fixation in common bean. Theor Appl Genet. doi:10.1007/s00122-015-2562-5

    PubMed  Google Scholar 

  • Leidi EO, Rodriguez-Navarro DN (2000) Nitrogen and phosphorus availability limit N fixation in bean. New Phytol 147:337–346

    Article  CAS  Google Scholar 

  • Li B, Li Y, Wu H et al (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N 2 fixation. PNAS 113:6496–6501. doi:10.1073/pnas.1523580113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP, Beebe SE (1995) Adaptations of beans (Phaseolus vulgaris L.) to low-phosphorus availability. Hortscience 30:1165–1171

    CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd Ed. Academic Press Inc., London, UK

  • Miguel MA, Widrig A, Vieira RF et al (2013) Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris). Ann Bot 112:973–982. doi:10.1093/aob/mct164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miklas PN, Porch TG (2010) Guidelines for common bean QTL nomenclature. Annu Rep Bean Improv Coop 53:202–204

    Google Scholar 

  • Mourice SK, Tryphone GM (2012) Evaluation of common bean (Phaseolus vulgaris L.) genotypes for adaptation to low phosphorus. International Scholarly Research Network Agronomy ID309614:1–9. doi: 10.5402/2012/309614

  • Olivera M, Tejera N, Iribarne C (2004) Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris): effect of phosphorus. Physiol Plant 121:498–505. doi:10.1111/j.1399-3054.2004.00355.x

    Article  CAS  Google Scholar 

  • Polanía J, Rao M, Beebe S, Garcia R (2009) Root development and distribution under drought stress in common bean (Phaseolus vulgaris L.) in a soil tube system. Agronomia Colombiana 27:25–32

    Google Scholar 

  • Polania J, Poschenrieder C, Beebe S, Rao IM (2016a) Effective use of water and increased dry matter partitioned to grain contribute to yield of common bean improved for drought resistance. Front Plant Sci. doi:10.3389/fmicb.2015.00927

    PubMed  PubMed Central  Google Scholar 

  • Polania J, Poschenrieder C, Beebe S, Rao IM (2016b) Estimation of phenotypic variability in symbiotic nitrogen fixation ability of common bean under drought stress using 15N natural abundance in grain. Eur J Agron 79:66–73. doi:10.1016/j.eja.2016.05.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramaekers L, Remans R, Rao IM et al (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176

    Article  Google Scholar 

  • Ramaekers L, Galeano CH, Garzón N et al (2013) Identifying quantitative trait loci for symbiotic nitrogen fixation capacity and related traits in common bean. Mol Breed 31:163–180. doi:10.1007/s11032-012-9780-1

    Article  CAS  Google Scholar 

  • Ramírez M, Flores-Pacheco G, Reyes JL et al (2013) Two common bean genotypes with contrasting response to phosphorus deficiency show variations in the microRNA 399-mediated PvPHO2 regulation within the PvPHR1 signaling pathway. Int J Mol Sci 14:8328–8344. doi:10.3390/ijms14048328

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao IM (2014) Advances in improving adaptation of common bean and Brachiaria forage grasses to abiotic stresses in the tropics. In: Pessarakl M (ed) Handbook of plant and crop physiology, Third Edit. CRC Press, Taylor and Francis Group, Boca Raton, FL., pp 847–889

  • Rao IM, Miles JW, Beebe SE, Horst WJ (2016) Root adaptations to soils with low fertility and aluminium toxicity. Ann Bot. doi:10.1093/aob/mcw073

    PubMed  PubMed Central  Google Scholar 

  • Remans R, Beebe S, Blair M et al (2007) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.) Plant Soil 302:149–161

    Article  Google Scholar 

  • Rotaru V, Sinclair TR (2009) Interactive influence of phosphorus and iron on nitrogen fixation by soybean. Environ Exp Bot 66:94–99

    Article  CAS  Google Scholar 

  • SAS-Institute (2011) SAS Institute Inc. 2011. SAS® 9.3 System Options: Reference, Second Edition

  • Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756. doi:10.1071/PP9860699c

    CAS  Google Scholar 

  • Silva DA, Fátima Esteves AJ, Messias U et al (2014) Efficiency in the use of phosphorus by common bean genotypes. Sci Agric 71:232–239

    Article  Google Scholar 

  • Singh A (2015) Nitrogen and phosphorus resorption efficiency in some leguminous and non-leguminous tropical tree species planted on coal mine spoil in a tropical dry environment. Ambit J Educ Res Rev 1:1–7

    CAS  Google Scholar 

  • 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 25:249–257

    Article  Google Scholar 

  • Tsvetkova GE, Georgiev GI (2007) Changes in phosphate fractions extracted from different organs of phosphorus starved nitrogen fixing pea plants. J Plant Nutr 30:2129–2140. doi:10.1080/01904160701700616

    Article  CAS  Google Scholar 

  • Unkovich MJ, Pate JS, Sanford P, Armstrong EL (1994) Potential precision of the delta-N-15 natural-abundance method in-field estimates of nitrogen-fixation by crop and pasture legumes in south-west Australia. Aust J Agric Res 45:119–132

    Article  Google Scholar 

  • Vadez V, Lasso JH, Beck DP, Drevon JJ (1999) Variability of N2-fixation in common bean (Phaseolus vulgaris L .) under P deficiency is related to P use efficiency N2-fixation tolerance to P deficiency. Euphytica 199079:231–242. doi:10.1016/j.jplph.2012.03.013

    Article  Google Scholar 

  • Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng Z-B (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC.( http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)

Download references

Acknowledgments

This project was supported by the CGIAR Research Program on Grain Legumes. We would like to thank all donors who supported this work through their contributions to the CGIAR Fund. We acknowledge the contributions made by E. Tovar, G. Borrero, and M. Rivera and the Bean Breeding team of the Bean Program of the International Center for Tropical Agriculture (CIAT). We also thank M. Otero and J. Molina for technical assistance.

Author information

Authors and Affiliations

  1. Bean Program, International Center for Tropical Agriculture (CIAT), A. A 6713, Cali, Colombia

    Lucy M. Diaz, Jaumer Ricaurte, Cesar Cajiao, Idupulapati Rao, Steve Beebe & Bodo Raatz

  2. Corporación Colombiana de Investigación Agropecuaria (Corpoica), Km 14 vía Mosquera, Bogotá, Colombia

    Carlos H. Galeano

Authors
  1. Lucy M. Diaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaumer Ricaurte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cesar Cajiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carlos H. Galeano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Idupulapati Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steve Beebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bodo Raatz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Diaz LM: Writing of the manuscript, analysis of genetic data, and statistical analysis of phenotypic data

Ricaurte J: Field evaluation and statistical analysis of phenotypic data

Cajiao C: Trial design and field evaluation

Galeano C: Idea conception and preliminary analysis of linkage and QTL

Rao I: leadership of physiological evaluations, discussion, and improvements of the manuscript

Beebe S: Idea conception, leadership of field trial activities, discussion, and improvements of the manuscript

Raatz B: leadership of genetic analysis and writing of the manuscript

Corresponding author

Correspondence to Bodo Raatz.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Key Message

Low phosphorus stress in Phaseolus vulgaris reduces yield and seed nitrogen, but has no strong effect on percentage of nitrogen derived from the atmosphere. QTLs were identified for SNF and yield components.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Diaz, L.M., Ricaurte, J., Cajiao, C. et al. Phenotypic evaluation and QTL analysis of yield and symbiotic nitrogen fixation in a common bean population grown with two levels of phosphorus supply. Mol Breeding 37, 76 (2017). https://doi.org/10.1007/s11032-017-0673-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-017-0673-1

Keywords

Search

Navigation