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Variation for nodulation and plant yield of common bean genotypes and environmental effects on the genotype expression

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Abstract

Common bean symbiotic nitrogen fixation provides an ecological and economical alternative to increase bean production but it depends on soil fertility and climate conditions. The objectives of this work were to characterize common bean genotypes for their ability to establish symbiosis under controlled conditions and to study the effect of the environment on the expression of those genotypes. The experiment under controlled conditions was conducted in a greenhouse with 158 genotypes that represented the major dry bean market classes. The field experiment was carried out in six environments with 64 genotypes that were previously selected for their contrasting nodulation ability and/or root development under the controlled conditions experiment. Nodulation, plant, and grain yield data of the bean genotypes were measured in both experiments. There was a significant high variability in plant development responses among the studied genotypes associated with the rhizobial strain inoculated under controlled conditions. Two nodulation phenotypes were observed among the genotypes tested: the big-nodules phenotype (BNO) associated with almost 63% fewer nodules and 58% higher proportion of nodule biomass in the below-ground compartment than the small-nodules phenotype (SNO) with less developed aerial parts. Genotype plus genotype × environment (GGE) biplot model analysis enabled identification of the highest-yielding genotypes for the different environments. The soil chemical factors of these environments were associated with the nodule number or the biomass of the common bean genotypes. Genotypes with a BNO phenotype showed a good plant response, indicating that this phenotype may be more beneficial for plant growth and seed yield in environmental conditions that may limit nodule development. The amplitude of the genotypic variability found in this work confirms the potential for rhizobial symbiosis of adapted bean genotypes, which could constitute a preferential material for initial breeding of symbiotically active lines. The data also indicate the potential of bean breeding to identify environments containing effective strains of rhizobia essential for sustainable agriculture, improving productivity, and maintaining environmental quality.

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References

  • Abaidoo RC, Keyser HH, Singleton PW, Dashiell KE, Sanginga N (2007) Population size, distribution, and symbiotic characteristics of indigenous Bradyrhizobium spp. that nodulate TGx soybean genotypes in Africa. Appl Soil Ecol 35:57–67

    Article  Google Scholar 

  • Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. Nov. and Rhizobium giardinii sp. Nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006

    Article  PubMed  CAS  Google Scholar 

  • Andrade DS, Hungria M (2002) Maximizing the contribution of biological nitrogen fixation in tropical legume crops. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton W (eds) Nitrogen fixation, global perspectives. CABIO, London, pp 341–345

    Google Scholar 

  • Bourion V, Laguerre G, Depret G, Voisin AS, Salon C, Duc G (2007) Genetic variability in nodulation and root growth affects nitrogen fixation and accumulation in pea. Ann Bot 100:589–598

    Article  PubMed  CAS  Google Scholar 

  • Buttery BR, Park SJ, Findlay WJ (1987) Growth and yield of white bean (Phaseolus vulgaris L.) in response to nitrogen, phosphorus and potassium fertilizer and to inoculation with Rhizobium. Can J Plant Sci 67:425–432

    Article  Google Scholar 

  • Cardoso JD, Gomes DF, Goes KP, Junior FNS, Dorigo OF, Hungria M, Andrade DS (2009) Relationship between total nodulation and nodulation at the root crown of peanut, soybean and common bean plants. Soil Biol Biochem 41:1760–1763

    Article  CAS  Google Scholar 

  • DeJong TM, Brewin NJ, Phillips DS (1981) Effects of plasmid content in Rhizobium leguminosarum on pea nodule activity and plant growth. J Gen Microbiol 124:1–7

    Google Scholar 

  • Doré T (1992) Analyse, par voie d’enquête, de la variabilité des rendements et des effets précédents du pois protéagineux de printemps (Pisum sativum L.). Thèse de Doctorat, p 214

  • Drevon JJ, Hartwig UA (1997) Phosphorous deficiency increases the argon induced decline of nodule nitrogenase activity in soybean and alfalfa. Planta 201:463–469

    Article  CAS  Google Scholar 

  • Duc G, Messager A (1989) Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Sci 60:207–213

    Article  Google Scholar 

  • Ebdon JS, Gauch HG (2002) Additive Main Effect and Multiplicative Interaction analysis of national turfgrass performance trials: I. Interpretation of genotype × environment interaction. Crop Sci 42:489–496

    Article  Google Scholar 

  • Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189

    Article  Google Scholar 

  • Elbanna K, Elbadry M, Gamal-Eldin H (2009) Genotypic and phenotypic characterization of rhizobia that nodulate snap bean (Phaseolus vulgaris L.) in Egyptian soils. Syst Appl Microbiol 32:522–530

    Article  PubMed  CAS  Google Scholar 

  • FAO (1991) The soil map of the world FAO-UNESCO. Roma

  • Gabriel KR (1971) The biplot graphic display of matrices with application to principal component analysis. Biometrika 58:453–467

    Article  Google Scholar 

  • Gauch HG, Zobel RW (1996) AMMI analysis of yield trials. In: Kang MS, Gauch HG Jr (eds) Genotype-by environment interaction. CRC, Boca Raton, pp 85–122

    Chapter  Google Scholar 

  • González AM, Monteagudo AB, Casquero PA, De Ron AM, Santalla M (2006) Genetic variation and environmental effects on agronomical and commercial quality traits in the main European market classes of dry bean. Field Crops Res 95:336–347

    Article  Google Scholar 

  • Graham PH (1981) Some problems of nodulation and symbiotic nitrogen fixation in Phaseolus vulgaris L.: a review. Field Crops Res 4:93–112

    Article  Google Scholar 

  • Graham PH (2008) Ecology of the root-nodule bacteria of legumes. In: Dilworth MJ, James EK, Sprent JI, Newton WE (eds) Leguminous nitrogen-fixing symbiosis. Springer, pp 23–58

  • Hamblin A, Tennant D (1987) Root length and water uptake in cereals and grain legumes: how well are they correlated? Aust J Agric Res 38:513–527

    Article  Google Scholar 

  • Hardarson G (1993) Methods for enhancing symbiotic nitrogen fixation. Plant Soil 152:1–17

    Article  Google Scholar 

  • Hardarson G, Bliss FA, Cigales-Rivero MR, Henson RA, Kipe-Nolt JA, Longeri L, Manrique A, Peña-Cabriales JJ, Pereira PAA, Sanabria CA, Tsai SM (1993) Genotypic variation in biological nitrogen fixation by common bean. Plant Soil 152:59–70

    Article  Google Scholar 

  • Hernandez G, Drevon JJ (1991) Influence of oxygen and acetylene during in situ open-flow assays of nitrogenase activity (C2H2 reduction) in Phaseolus vulgaris root-nodules. J Plant Physiol 138:587–590

    CAS  Google Scholar 

  • Herrera-Cervera JA, Caballero-Mellado J, Laguerre G, Tichy HV, Requena N, Amarger N, Martinez-Romero E, Olivares J, Sanjuan J (1999) At least five species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 30:87–97

    Article  CAS  Google Scholar 

  • Herridge D, Rose I (2000) Breeding for enhanced nitrogen fixation in crop legumes. Field Crops Res 65:229–248

    Article  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

    Article  Google Scholar 

  • Hungria M, Vargas MAT, Araujo RS (1997) Fixaçao biologica do nitrogenio em feijoeiro. In: Vargas MAT, Hungria M (eds) Biologia dos solos dos cerrados. EMBRAPA-CPAC, Planaltina, pp 189–295

    Google Scholar 

  • Hungria M, Campo RJ, Mendes IC (2003) Benefits of inoculation of common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biol Fertil Soils 39:88–93

    Article  Google Scholar 

  • Jensen ES (1987) Seasonnal patterns of growth and nitrogen fixation in field-grown pea. Plant Soil 101:29–37

    Article  Google Scholar 

  • Kipe-Nolt JA, Vargas H, Giller KE (1993) Nitrogen fixation in breeding lines of Phaseolus vulgaris L. Plant Soil 152:103–106

    Article  Google Scholar 

  • Kovas S, Labidi N, Debez A, Abdelly C (2005) Effect of P on nodule formation and N fixation bean. Agron Sustain Dev 25:389–393

    Article  Google Scholar 

  • Laguerre G, Depret G, Bourion V, Duc G (2007) Rhizobium leguminosarum bv. viciae genotypes interact with pea plants in developmental responses of nodules, roots and shoots. New Phytol 176:680–690

    Article  PubMed  Google Scholar 

  • Latour X, Philippot L, Corberand T, Lemanceau P (1999) The establishment of an introduced community of fluorescent pseudomonas in the soil and the rhizosphere is affected by the soil type. FEMS Microbiol Ecol 30:163–170

    Article  PubMed  CAS  Google Scholar 

  • Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208

    Article  CAS  Google Scholar 

  • Martensson AM, Rydberg I (1996) Cultivar x rhizobial strain interactions in peas with respect to early symbiosis, nodule initiation and N uptake. Plant Breed 115:402–406

    Article  Google Scholar 

  • Martínez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11–23

    Article  Google Scholar 

  • Martínez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426

    Article  PubMed  Google Scholar 

  • Martínez-Romero E, Hernández-Lucas I, Peña-Cabriales JJ, Castellanos JZ (1998) Symbiotic performance of some modified Rhizobium etli strains in assays with Phaseolus vulgaris beans that have a high capacity to fix N2. Plant Soil 204:89–94

    Article  Google Scholar 

  • Miranda BD, Bliss FA (1991) Selection for increased seed nitrogen accumulation in common bean: implications for improving dinitrogen fixation and seed yield. Plant Breed 106:301–311

    Article  CAS  Google Scholar 

  • Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R (2007) Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol 187:79–85

    Article  PubMed  CAS  Google Scholar 

  • Mostasso FL, Dias BG, Vargas MAT, Hungria M (2002) Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res 73:121–132

    Article  Google Scholar 

  • Nleya T, Walley F, Vanderbeng A (2002) Nodulation, seed yield and dinitrogen fixation in determinate and indeterminate common bean cultivars. Ann Rep Bean Improv Coop 45:54–55

    Google Scholar 

  • Oka-Kira E, Kawaguchi M (2006) Long-distance signalling to control root nodule number. Curr Opin Plant Biol 9:496–502

    Article  PubMed  CAS  Google Scholar 

  • Pate JS (1985) Physiology of pea—a comparison with other legumes in terms of economy of carbon and nitrogen in whole-plant and organ functioning. In: Hebblethwaite PD, Heath MC, Dawkins TCK (eds) The pea crop. Butterworths, London, pp 279–296

    Google Scholar 

  • Pereira PAA, Araujo RS, Rocha REM, Steinmetz S (1984) Capacidade dos genotipos de feijoeiro de fixar N2 atmosferico. Pesqui Agropecu Bras 19:811–815

    Google Scholar 

  • Provorov NA, Tikhonovich IA (2003) Genetic resources for improving nitrogen fixation in legume-rhizobia symbiosis. Genet Resour Crop Evol 50:89–99

    Article  CAS  Google Scholar 

  • Qiao YF, Tang C, Han XZ, Miao SJ (2007) Phosphorus deficiency delays the onset of nodule function in soybean (Glycine max Murr.). J Plant Nutr 30:1341–1353

    Article  CAS  Google Scholar 

  • Ramos MLG, Boddey RM (1987) Yield and nodulation of Phaseolus vulgaris and the competitivity of an introduced Rhizobium strain: effects of lime, mulch and repeated cropping. Soil Biol Biochem 19:171–177

    Article  Google Scholar 

  • Rengel Z (2002) Breeding for better symbiosis. Plant Soil 245:147–162

    Article  CAS  Google Scholar 

  • Ribet J, Drevon JJ (1995) Increase in permeability to oxygen and in oxygen uptake of soybean nodules under limiting phosphorus nutrition. Physiol Plant 94:298–304

    Article  CAS  Google Scholar 

  • Ribet J, Drevon JJ (1996) The phosphorous requirement of N2-fixing and urea-fed Acacia mangium. New Phytol 132:383–390

    Article  CAS  Google Scholar 

  • Rodríguez-Navarro DN, Buendia AM, Camacho M, Lukas MM, Santamatria C (2000) Characterization of Rhizobium spp. Bean isolates from South West Spain. Soil Biol Biochem 32:1601–1613

    Article  Google Scholar 

  • Sagan M, Duc G (1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20:229–245

    Google Scholar 

  • Salon C, Munier-Jolain NG, Duc G, Voisin AS, Grandgirard D, Larmure A, Emery RJN, Ney B (2001) Grain legume seed filling in relation to nitrogen acquisition: a review and prospects with particular reference to pea. Agronomie 21:539–552

    Article  Google Scholar 

  • Santalla M, Amurrio JM, De Ron AM (2001) Symbiotic interactions between Rhizobium leguminosarum strains and elite cultivars of Pisum sativum L. J Agron Crop Sci 187:59–68

    Article  Google Scholar 

  • Schulze J, Adgo E, Merbach W (1999) Carbon costs associated with N2 fixation in Vicia faba L. and Pisum sativum L. over a 14-day period. Plant Biol 1:625–631

    Article  Google Scholar 

  • Skøt L (1983) Cultivar and Rhizobium strain effects on the symbiotic performance of pea (Pisum sativum). Physiol Plant 59:585–589

    Article  Google Scholar 

  • Tamimi SM, Timko MP (2003) Effects of ehtylene and inhibitors of ethylene synthesis and action on nodulation in common bean (Phaseolus vulgaris L.). Plant Soil 257:125–131

    Article  CAS  Google Scholar 

  • Thies JE, Singleton PW, Bohlool BB (1991) Influence of the size of indigenous rhizobial population on establishment and symbiotic performance of introduced rhizobia on field-grown legumes. Appl Environ Microbiol 57:19–28

    PubMed  CAS  Google Scholar 

  • Thies JE, Woomer PL, Singleton PW (1995) Enrichment of Bradyrhizobium spp populations in soil due to cropping of the homologous host plant. Soil Biol Biochem 27:633–636

    Article  CAS  Google Scholar 

  • Vadez V, Rodier F, Payre H, Drevon JJ (1996) Nodule permeability to O2 and nitrogenase linked respiration in bean genotypes varying in the tolerance of N2 fixation to P deficiency. Plant Physiol Biochem 34:871–878

    CAS  Google Scholar 

  • Vessey JK (1992) Cultivar differences in assimilate partitioning and capacity to maintain N2 fixation rate in pea during pod-filling. Plant Soil 139:185–194

    Article  CAS  Google Scholar 

  • Vincent JM (1970) Manual for the practical study of root nodule bacteria. Backwell Scientific Publications, Oxford

    Google Scholar 

  • Voisin AS, Salon C, Jeudy C, Warembourg FR (2003) Seasonal patterns of 13C partitioning between shoots and nodulated roots of N2- or nitrate-fed Pisum sativum L. Ann Bot 91:539–546

    Article  PubMed  CAS  Google Scholar 

  • Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural. Soil Biol Biochem 40:803–813

    Article  CAS  Google Scholar 

  • Waluyo SH, Lie TA, Mannetje L (2004) Effect of phosphate on nodule primordia of soybean (Glycine max) in acid soils in rhizotron experiments. Indonesian J Agric Sci 5:27–44

    Google Scholar 

  • Yan W, Hunt LA (2001) Interpretation of genotype by environment interaction for winter wheat yield in Ontario. Crop Sci 41:19–25

    Article  Google Scholar 

  • Yan W, Kang S (2003) GGE biplot analysis: a graphical tool for breeders, geneticist and agronomist. CRC Press, Boca Raton

    Google Scholar 

  • Yan W, Rajcan I (2002) Biplot evaluation of test sites and trait relations of soybean in Ontario. Crop Sci 42:11–20

    Article  PubMed  Google Scholar 

  • Yan W, Hunt LA, Sheng Q, Szlavnics Z (2000) Cultivar evaluation and mega-environment investigation based on GGE biplot. Crop Sci 40:596–605

    Article  Google Scholar 

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Acknowledgements

This research was supported by the projects FAIR-510564, and PGIDIT09MDS026403PR and INCITE07PXI403088ES from the European Union (Programme Marie Curie Reintegration Grant) and Galician Government, respectively. M. De La Fuente and A. P. Rodiño acknowledge fellowships from the Xunta de Galicia that allowed her to carry out this study. Special thanks to E. Martinez (UNAM-Mexico) and C. Revellin (INRA-France) for supplying the rhizobia strain. The authors are grateful to the Diputación Provincial de Pontevedra for farm facilities and A. Castro, E. Pérez and A. López for technical assistance.

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  1. Plant Genetic Resources Department, Misión Biológica de Galicia, CSIC, P.O. Box 28, 36080, Pontevedra, Spain

    Ana Paula Rodiño, Maria De La Fuente, Antonio M. De Ron & Marta Santalla

  2. Soil Science Department, Phytopatological Station Do Areeiro, Subida a la Robleda s/n, 36153, Pontevedra, Spain

    Maria J. Lema

  3. INRA- SupAgro Montpellier- UMR1222, 2, Place Viala, 34060, Montpellier, France

    Jean Jacques Drevon

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  1. Ana Paula Rodiño
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  2. Maria De La Fuente
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  3. Antonio M. De Ron
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  4. Maria J. Lema
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  5. Jean Jacques Drevon
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Correspondence to Ana Paula Rodiño.

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Rodiño, A.P., De La Fuente, M., De Ron, A.M. et al. Variation for nodulation and plant yield of common bean genotypes and environmental effects on the genotype expression. Plant Soil 346, 349–361 (2011). https://doi.org/10.1007/s11104-011-0823-x

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