Skip to main content

Advertisement

SpringerLink
Log in

Rhizobia biodiversity in Uruguay: preservation and uses

  • Review
  • Published:
Environmental Sustainability Aims and scope Submit manuscript

Abstract

This review presents a summary of the work done in Uruguay on the diversity and agricultural use of rhizobia, a group of soil bacteria able to establish symbiotic associations almost exclusively with legumes and fix atmospheric nitrogen. Uruguay has a long tradition regarding the use of microbial inoculants for agriculture. It is worth mentioning that since 1960, Uruguay has formally regulated the use of microorganisms in agriculture, being considered one of the pioneer countries where state policies on microbial inoculants have been implemented. In general, the vast majority of the work carried out in Uruguay has focused on the selection and characterization of promising bacteria to be used as biofertilizers. Therefore, the most studied symbiotic associations were those established with legumes of agricultural interest for the country, such as alfalfa, clover, lotus and soybean. The studies carried out with autochthonous alpha- and beta- rhizobia associated with diverse legume species are also considered, taking into account their ecological importance and the interest in knowing and preserving native germplasm.

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

References

  • Abraham EM, Ganopoulos I, Madesis P, Mavromatis A, Mylona P, Nianiou-Obeidat I, Parissi Z, Polidoros A, Tani E, Vlachostergios D (2019) The use of lupin as a source of protein in animal feeding: Genomic tools and breeding approaches. Int J Mol Sci 20:851

    CAS  Google Scholar 

  • Alonso Paz E (1991) El género Lupinus (LEGUMINOSAE, PAPILIONOIDEAE) en el Uruguay. Com Bot Mus Montevideo 97:1–15

    Google Scholar 

  • Altier N, Beyhaut E, Pérez C (2013) Root nodule and rhizosphere bacteria for forage legume growth promotion and disease management. In: Maheshwari D, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin, Heidelberg, pp 167–184

    Google Scholar 

  • Andrews M, Andrews ME (2017) Specificity in legume-rhizobia symbioses. Int J Mol Sci 18:705

    Google Scholar 

  • Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB, Boatwright JS, Borges LM, Brown GK, Bruneau A (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the legume phylogeny working group (LPWG). Taxon 66:44–77

    Google Scholar 

  • Bagnasco P, De la Fuente L, Gualtieri G, Noya F, Arias A (1998) Fluorescent Pseudomomas spp. as biocontrol agents against forage legume root pathogenic fungi. Soil Biol Biochem 30:1317–1322

    CAS  Google Scholar 

  • Baraibar A, Frioni L, Guedes ME, Ljunggren H (1999) Symbiotic effectiveness and ecological characterization of indigenous Rhizobium loti populations in Uruguay. Pesq Agrop Brasileira 34:1010–1017

    Google Scholar 

  • Baraibar A, Frioni L, Guedes ME, Pagliano D, Viera S, Casartelli R (1988) Relevamiento y caracterización de la población de Rhizobium loti en suelos del Uruguay. Proceedings of the XIV Reunión Latinoamericana de Rhizobiología (Ed. H Urzúa) p46–51

  • Batista L, Irisarri P, Rebuffo M, Cuitiño MJ, Sanjuán J, Monza J (2015) Nodulation competitiveness as a requisite for improved rhizobial inoculants of Trifolium pratense. Biol Fertil Soils 51:11–20

    Google Scholar 

  • Batista L, Tomasco I, Lorite MJ, Sanjuán J, Monza J (2013) Diversity and phylogeny of rhizobial strains isolated from Lotus uliginosus grown in Uruguayan soils. Appl Soil Ecol 66:19–28

    Google Scholar 

  • Berais A, Morel M, Giménez M, Monza J (2021) Cepas parásitas de alfalfa en suelos ácidos de la Cuenca lechera de Uruguay: confirmación de su presencia y competitividad frente al inoculante comercial. XXX Reunión Latinoamericana de Rizobiología V Conferencia Latinoamericana de Microorganismos Promotores del Crecimiento Vegetal – Uruguay. Available in: https://relar-pgpr.com/inicio (Accesed October 2022)

  • Berriel V. (2022) Identificación de puentes verdes basados en especies de leguminosas tropicales: combinación de criterios de eficiencia de uso de agua y de fijación de N y C. PhD Thesis, 87 pp. Facultad de Ciencias. Universidad de la República Oriental del Uruguay

  • Berriel V, Monza J, Perdomo CH (2020) Cover crop selection by jointly optimizing biomass productivity, biological nitrogen fixation, and transpiration efficiency: application to two Crotalaria species. Agronomy 10(8):1116

    CAS  Google Scholar 

  • Berriel V, Morel MA, Filippi CV, Monza J (2021) Draft genome sequence of Bradyrhizobium sp strain Oc8 isolated from Crotalaria ochroleuca nodule. Curr Res Microb Sci 2:100074

    CAS  Google Scholar 

  • Bhat SV, Maughan H, Cameron AD, Yost CK (2022) Phylogenomic analysis of the genus Delftia reveals distinct major lineages with ecological specializations. Microb Genom 8:000864

    CAS  Google Scholar 

  • Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton RC, Neto NE, de Fátima LM, De Faria SM, Sprent JI, James EK (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52

    CAS  Google Scholar 

  • Bourion V, Heulin-Gotty K, Aubert V, Tisseyre P, Chabert-Martinello M, Pervent M, Delaitre C, Vile D, Siol M, Duc G, Brunel B (2018) Co-inoculation of a pea core-collection with diverse rhizobial strains shows competitiveness for nodulation and efficiency of nitrogen fixation are distinct traits in the interaction. Front Plant Sci 8:2249

    Google Scholar 

  • Braña V, Cagide C, Morel MA (2016) The sustainable use of Delftia in agriculture, bioremediation, and bioproducts synthesis. In: Castro-Sowinski S (ed) Microbial Models: from environmental to industrial sustainability. Springer Singapore, Singapore, pp 227–247

    Google Scholar 

  • Cagide C, Riviezzi B, Minteguiaga M, Morel M, Castro-Sowinski S (2018) Identification of plant compounds involved in the microbe-plant communication during the co-inoculation of soybean with Bradyrhizobium elkanii and Delftia sp. JD2. Mol Plant-Microbe Interact 31:1192–1199

    CAS  Google Scholar 

  • Castillo A, Rebuffo M, Dalla RM, Borsani O, Monza J (2012) Generation and characterization of inter-specific hybrids of Lotus uliginosus x L. corniculatus. Crop Sci 52:1572–1582

    CAS  Google Scholar 

  • Castillo A (2012) Generación de híbridos interespecíficos de L. uliginosus x L. corniculatus y evaluación de la respuesta a déficit hídrico. PhD Thesis. PEDECIBA, Universidad de la República Oriental del Uruguay

  • Castro-Sowinski S, Carrera I, Catalan AI, Coll J, Martinez-Drets GL (2002) Occurrence, diversity and effectiveness of mid-acid tolerant alfalfa nodulating rhizobia in Uruguay. Symbiosis 32:105–118

    Google Scholar 

  • Checcucci A, DiCenzo GC, Bazzicalupo M, Mengoni A (2017) Trade, diplomacy, and warfare: the quest for elite rhizobia inoculant strains. Front Microbiol 8:2207

    Google Scholar 

  • Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    CAS  Google Scholar 

  • Costa A, Panzera M, Roldán D, Viera F, Fernández S, Zabaleta M, Amarelle V, Fabiano E (2023) Diversity of Bradyrhizobium strains that nodulate Lupinus species native to Uruguay. Environ Sustain. https://doi.org/10.1007/s42398-023-00263-y

    Article  Google Scholar 

  • Dall’Agnol RF, Bournaud C, de Faria SM, Béna G, Moulin L, Hungria M (2017) Genetic diversity of symbiotic Paraburkholderia species isolated from nodules of Mimosa pudica (L.) and Phaseolus vulgaris (L.) grown in soils of the Brazilian Atlantic Forest (Mata Atlântica). FEMS Microbiol Ecol 93:027

    Google Scholar 

  • De Meyer SM, Parker PV, Berkum R, Tian R, Seshadri TBK, Reddy V, Markowitz N, Ivanova A, Pati T, Woyke NK, Reeve W (2015) High-quality permanent draft genome sequence of the Mimosa asperata nodulating Cupriavidus sp. strain AMP6. Genom Sci 10:80. https://doi.org/10.1186/s40793-015-0074-1

    Article  CAS  Google Scholar 

  • De La Fuente L, Quagliotto L, Bajsa N, Fabiano E, Altier N, Arias A (2002) Inoculation with Pseudomonas fluorescens biocontrol strains does not affect the symbiosis between rhizobia and forage legumes. Soil Biol Biochem 34:545–548

    Google Scholar 

  • De Meyer SE, Fabiano E, Tian R et al (2015) High-quality permanent draft genome sequence of the Parapiptadenia rigida-nodulating Cupriavidus sp. strain UYPR2.512. Stand Genom Sci 10:13. https://doi.org/10.1186/1944-3277-10-13

    Article  CAS  Google Scholar 

  • Del Papa MF, Balagué LJ, Sowinski SC, Wegener C, Segundo E, Abarca FM, Toro N, Niehaus K, Pühler A, Aguilar OM, Martínez-Drets G (1999) Isolation and characterization of alfalfa-nodulating rhizobia present in acidic soils of central Argentina and Uruguay. Appli Environ Microbiol 65:1420–1427

    Google Scholar 

  • Del Papa MF, Pistorio M, Balagué LJ, Draghi WO, Wegener C, Perticari A, Niehaus K, Lagares A (2003) A microcosm study on the influence of pH and the host-plant on the soil persistence of two alfalfa-nodulating rhizobia with different saprophytic and symbiotic characteristics. Biol Fertil Soils 39:112–116

    Google Scholar 

  • Denton MD, Coventry DR, Murphy PJ, Howieson JG, Bellotti WD (2002) Competition between inoculant and naturalised Rhizobium leguminosarum bv. trifolii for nodulation of annual clovers in alkaline soils. Aust J Agric Res 53:1019–1026

    CAS  Google Scholar 

  • de Souza GK, Sampaio J, Longoni L, Ferreira S, Alvarenga S, Beneduzi A (2019) Soybean inoculants in Brazil: an overview of quality control. Brazilian J Microbiol 50:205–211

    Google Scholar 

  • DIEA (2010) Statistical Yearbook Dirección Estadísticas Agropecuarias (DIEA), Uruguay. Available in http://www.gub.uy/ministerio-ganaderia-agricultura-pesca/diea. (Accessed in October 2022)

  • DIEA (2021) Statistical Yearbook Dirección Estadísticas Agropecuarias (DIEA), Uruguay. Available in: http://www.gub.uy/ministerio-ganaderia-agricultura-pesca/diea (Accessed in October 2022)

  • Dos Reis FB Jr, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, de Fatima LM, de Queiroz LP, Scotti MR, Chen WM, Norén A, Rubio MC, de Faria SM, Bontemps C, Goi SR, Young JPW, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946

    Google Scholar 

  • Drummond CS, Eastwood RJ, Miotto ST, Hughes CE (2012) Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling. Syst Biol 61:443–460

    Google Scholar 

  • Duodu S, Carlsson G, Huss-Danell K, Svenning MM (2007) Large genotypic variation but small variation in N2 fixation among rhizobia nodulating red clover in soils of northern Scandinavia. J Appl Microbiol 102:1625–1635

    CAS  Google Scholar 

  • Frioni L, Dodera R, Malatés D, Irigoyen I (1998) An assessment of nitrogen fixation capability of leguminous trees in Uruguay. Appl Soil Ecol 7(3):271–279

    Google Scholar 

  • Frioni L, Rodrıguez A, Meerhoff M (2001) Differentiation of rhizobia isolated from native legume trees in Uruguay. Appl Soil Ecol 16:275–282

    Google Scholar 

  • Glenn AR, Dilworth MJ (1994) The life of root nodule bacteria in the acidic underground. FEMS Microbiol Lett 123:1–9

    CAS  Google Scholar 

  • Gonnet S, Díaz P (2000) Glutamine synthetase and glutamate synthase activities in relation to nitrogen fixation in Lotus spp. Rev Bras Fisiol Veg 2:195–202

    Google Scholar 

  • Irisarri P, Cardozo G, Tartaglia C, Reyno R, Gutiérrez P, Lattanzi FA, Rebuffo M, Monza J (2019) Selection of competitive and efficient rhizobia strains for white clover. Front Microbiol 10:768

    Google Scholar 

  • Irisarri P, Milnitsky F, Monza J, Bedmar EJ (1996) Characterization of rhizobia nodulating Lotus subbiflorus from Uruguayan soils. Plant Soil 180:39–47

    CAS  Google Scholar 

  • Izaguirre P, Beyhaut R (2003) Leguminosas en Uruguay y regiones vecinas. Parte 2: Caesalpinioideae. Parte 3: Mimosoideae. 1–302. Editorial Hemisferio Sur, ISBN 9974–645–31-X. Montevideo

  • Jorrin B, Maluk M, Atoliya N, Kumar SC, Chalasani D, Tkacz A, Singh P, Basu A, Pullabhotla SV, Kumar M, Mohanty SR (2021) Genomic diversity of pigeon pea (Cajanus cajan l Millsp) endosymbionts in India and selection of potential strains for use as agricultural inoculants. Front Plant Sci 12:1848

    Google Scholar 

  • Labandera C (2005) Actividades en fijación biológica de nitrógeno departamento de microbiología de suelos situación actual y perspectivas. Agrociencia 9:299–303

    Google Scholar 

  • Labandera C (2007) Metodologías aplicadas a la evaluación de rhizobios para inoculantes para leguminosas forrajeras en Uruguay. Trabajos Técnicos, Departamento de Microbiologia de Suelos, MGAP

    Google Scholar 

  • Labandera C (1985) Biological nitrogen fixation programme in Uruguay and activities related to BNF in Latin America and the Caribbean. In Biological nitrogen fixation in Africa: proc. of the First Conference of the African Association for Biological Nitrogen Fixation (AABNF) (Ed. H. Ssali). Nairobi Rhizobium MIRCEN, Dept. of Soil Science, University of Nairobi, Kenya

  • Labandera CA, Vincent JM (1975) Competition between an introduced strain and native Uruguayan strains of Rhizobium trifolii. Plant Soil 42:327–347

    Google Scholar 

  • Labandera C, Baraibar A, Milian A (1982) Technology of Rhizobium. Anuario-Plan-Agropecuario Trabajos Téc 3:11–15

    Google Scholar 

  • Lagurara PF (2018) Eficiencia simbiótica y capacidad competitiva de cepas de rizobios que nodulan soja en suelos con y sin historia del cultivo. MSc. Thesis. pp 127. Facultad de Agronomía, Universidad de la República. Uruguay. https://hdl.handle.net/20.500.12008/31586

  • Lindström K, Murwira M, Willems A, Altier N (2010) The biodiversity of beneficial microbe-host mutualism: the case of rhizobia. Res Microbiol 161:453–463

    Google Scholar 

  • Lorite MJ, Estrella MJ, Escaray FJ, Sannazzaro A, Videira e Castro IM, Monza J, Sanjuán J, León-Barrios, M, (2018) The Rhizobia-Lotus symbioses: deeply specific and widely diverse. Front Microbiol 9:2055

    Google Scholar 

  • LPWG (2022). Accepted Species List and Synonyms. The Legume Phylogeny Working Group. Available at: https://www.legumedata.org/taxonomy/species-list/ (Accessed October 2022)

  • Mederos M (2016) Evaluación de la eficiencia simbiótica de híbridos interespercíficos de Lotus uliginosus x Lotus corniculatus. Agronomic Engineering Thesis, Facultad de Agronomía, Universidad de la República, Uruguay

  • Milnitsky F, Frioni L, Agius F (1997) Characterization of rhizobia that nodulate native legume trees from Uruguay. Soil Biol Biochem 29:989–992

    CAS  Google Scholar 

  • Monza J, Fabiano E, Arias A (1992) Characterization of an indigenous population of rhizobia nodulating Lotus corniculatus. Soil Biol Biochem 24:241–247

    CAS  Google Scholar 

  • Morel M, Tartaglia C, Delpino J, Sanjuán J, Monza J (2021) Relaciones evolutivas entre rizobios eficientes y parásitos de trébol blanco: sumando evidencias de transferencia lateral de genes simbióticos. XXX Reunión Latinoamericana de Rizobiología V Conferencia Latinoamericana de Microorganismos Promotores del Crecimiento Vegetal – Uruguay. Available in: https://relar-pgpr.com/inicio (Accesed October 2022)

  • Morel MA (2010) Mecanismos implicados en la tolerancia a cromo en bacterias: potenciales aplicaciones biotecnológicas. MSc Thesis. pp 152. Facultad de Ciencias, Universidad de la República. Uruguay

  • Morel MA, Cagide C, Castro-Sowinski S (2016a) The contribution of secondary metabolites in the success of bioformulations. In: Arora N, Mehnaz S, Balestrini R (eds) Bioformulations: for sustainable agriculture. Springer, New Delhi, pp 235–250

    Google Scholar 

  • Morel MA, Cagide C, Minteguiaga MA, Dardanelli MS, Castro-Sowinski S (2014) The pattern of secreted molecules during the co-inoculation of alfalfa plants with Sinorhizobium meliloti and Delftia sp. strain JD2: An interaction that improves plant yield. Mol Plant-Microbe Interact 28:134–142

    Google Scholar 

  • Morel MA, Iriarte A, Jara E, Musto H, Castro-Sowinski S (2016b) Revealing the biotechnological potential of Delftia sp. JD2 by a genomic approach. AIMS Bioeng 3:156–175

    CAS  Google Scholar 

  • Morel MA, Ubalde MC, Brana V, Castro-Sowinski S (2011) Delftia sp. JD2: a potential Cr (VI)-reducing agent with plant growth promoting activity. Arch Microbiol 193:63–68

    CAS  Google Scholar 

  • Morón A, Baethgen W (1996) Relevamiento de la fertilidad de los suelos bajo producción lechera. INIA Serie Técnica 73. Montevideo, Uruguay. p16

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411:948–950

    CAS  Google Scholar 

  • Nangul A, Moot DJ, Brown D, Ridgway HJ (2013) Nodule occupancy by Rhizobium leguminosarum strain WSM1325 following inoculation of four annual Trifolium species in Canterbury, New Zealand. J Agricul Res 56:215–223

    Google Scholar 

  • Oliveira F, Guerra J, Ribeiro R, Almeida D, Silva E, Urquiaga S, Espindola J (2007) The use of sunn hemp as green manure intercropped with taro. Hortic Bras 25:562–566

    Google Scholar 

  • Pereira N, Soares I, Miranda F (2016) Decomposition and nutrient release of leguminous green manure species in the Jaguaribe-Apodi region, Ceará. Brazil Cienc Rural 46:970–975

    CAS  Google Scholar 

  • Pereira-Gómez M, Ríos C, Zabaleta M, Lagurara P, Galvalisi U, Iccardi P, Azziz G, Battistoni F, Platero R, Fabiano E (2020) Native legumes of the Farrapos protected area in Uruguay establish selective associations with rhizobia in their natural habitat. Soil Biol Biochem 148:107854

    Google Scholar 

  • Pérez E, Labandera C (1998) Especificidad simbiótica dentro del género Lotus. Actas de la XIX Reunión Latinoamericana de Rhizobiología

  • Platero R, James EK, Rios C, Iriarte A, Sandes L, Zabaleta M, Battistoni F, Fabiano E (2016) Novel Cupriavidus strains isolated from root nodules of native Uruguayan Mimosa species. Appl Environ Microbiol 82:3150–3164

    CAS  Google Scholar 

  • Quagliotto L, Azziz G, Bajsa N, Vaz P, Pérez C, Ducamp F, Cadenazzi M, Altier N, Arias A (2009) Three native Pseudomonas fluorescens strains tested under growth chamber and field conditions as biocontrol agents against damping-off in alfalfa. Biol Control 51:42–50

    Google Scholar 

  • Ramsay JP, Ronson CW (2015) Genetic regulation of symbiosis island transfer in Mesorhizobium loti. Biol Nitrogen Fixat 3:217–224

    Google Scholar 

  • Real D, Labandera CA, Howieson JG (2005) Performance of temperate and subtropical forage legumes when over-seeding native pastures in the basaltic region of Uruguay. Aust J Exp Agric 45:279–287

    Google Scholar 

  • Riviezzi B, Cagide C, Pereira A, Herrmann C, Lombide R, Lage M, Sicardi I, Lage P, Castro-Sowinski S, Morel MA (2020) Improved nodulation and seed yield of soybean (Glycine max) with a new isoflavone-based inoculant of Bradyrhizobium elkanii. Rhizosphere 15:100219

    Google Scholar 

  • Riviezzi B, García-Laviña CX, Morel MA, Castro-Sowinski S (2021a) Facing the communication between soybean plants and microorganisms (Bradyrhizobium and Delftia) by quantitative shotgun proteomics. Symbiosis 83:293–304

    CAS  Google Scholar 

  • Riviezzi B, Campmajó G, Cagide C, Carrera E, Saurina J, Castro-Sowinski S, Olivaro C, Nuñez O, Morel M (2021b) Comparative metabolite analysis of Delftia-Bradyrhizobium co-inoculated soybean plants using UHPLC-HRMS-based metabolomic profiling. Symbiosis 85:325–341

    CAS  Google Scholar 

  • Rodríguez Blanco A, Csukasi F, Abreu C, Sicardi M (2008) Characterization of rhizobia from Sesbania species native to seasonally wetland areas in Uruguay. Biol Fertil Soils 44:925–932

    Google Scholar 

  • Rodríguez Blanco A, Sicardi M, Frioni L (2010) Competition for nodule occupancy between introduced and native strains of Rhizobium leguminosarum biovar trifolii. Biol Fert Soils 46:419–425

    Google Scholar 

  • Rodriguez Rodriguez NE, Beyhaut E, Sicardi M, Rodríguez-Blanco A (2023) Bioprospection of naturalized soybean-nodulating Bradyrhizobium strains in Uruguayan soils: a genetic and symbiotic approach. Environ Sustain. 5:1–1

    Google Scholar 

  • Segundo E, Martinez-Abarca F, Dillewijn PV, Fernández-López M, Lagares A, Martinez-Drets G, Niehaus K, Pühler A, Toro N (1999) Characterisation of symbiotically efficient alfalfa-nodulating rhizobia isolated from acid soils of Argentina and Uruguay. FEMS Microbiol Ecol 28:169–176

    CAS  Google Scholar 

  • Sotelo M, Irisarri P, Lorite MJ, Casaretto E, Rebuffo M, Sanjuán J, Monza J (2011) Diversity of rhizobia nodulating Lotus corniculatus grown in northern and southern regions of Uruguay. Appl Soil Ecol 49:197–207

    Google Scholar 

  • Tabáres-da Rosa S, Signorelli S, Del Papa MF, Sabatini O, Reyno R, Lattanzi F, Rebuffo M, Sanjuán J, Monza Galetti J (2019) Rhizobia inoculants for alfalfa in acid soils: A proposal for Uruguay. Agrociencia 23:1–13

    Google Scholar 

  • Tartaglia C, Azziz G, Lorite MJ, Sanjuán J, Monza J (2019) Phylogenetic relationships among introduced and autochthonous rhizobia nodulating Trifolium spp. in Uruguayan soils. Appl Soil Ecol 139:40–46

    Google Scholar 

  • Taulé C, Zabaleta M, Mareque C, Platero R, Sanjurjo L, Sicardi M, Frioni L, Battistoni F, Fabiano E (2012) New beta-proteobacterial rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol 78(6):1692–700

    Google Scholar 

  • Torres-Tejerizo G, Del Papa MF, Draghi W, Lozano M, Giusti MA, Martini C, Salas ME, Salto I, Wibberg D, Szczepanowski R (2011) First genomic analysis of the broad-host-range Rhizobium sp. LPU83 strain, a member of the low-genetic diversity Oregon-like Rhizobium sp. group. J Biotechnol 155:3–10

    CAS  Google Scholar 

  • Torres-Tejerizo G, Rogel MA, Ormeño-Orrillo E, Althabegoiti MJ, Nilsson JF, Niehaus K, Schlüter A, Pühler A, Del Papa MF, Lagares A, Martínez-Romero E (2016) Rhizobium favelukesii sp. nov., isolated from the root nodules of alfalfa (Medicago sativa L). Int Jf Syst Evol Microbiol 66:4451–4457

    Google Scholar 

  • Ubalde MC, Braña V, Sueiro F, Morel MA, Martínez-Rosales C, Marquez C, Castro-Sowinski S (2012) The versatility of Delftia sp. isolates as tools for bioremediation and biofertilization technologies. Curr Microbiol 64:597–603

    CAS  Google Scholar 

  • Yanes ML (2014) Caracterización de una cepa de Pseudomonas fluorescens promotora del crecimiento vegetal. PhD Thesis. PEDECIBA, Facultad de Ciencias, Universidad de la República

  • Yates RJ, Howieson JG, Real D, Reeve WG, Vivas-Marfisi A, O’Hara GW (2005) Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii. Aust J Exp Agric 45:189–198

    Google Scholar 

  • Zabaleta M, Platero R, Taulé C, Mareque C, Battistoni F, Fabiano E (2015) Mejora del crecimiento de la leguminosa arbórea Parapiptadenia rigida (Benth.) Brenan en condiciones de cultivo a campo mediante el uso de bacterias del grupo de los Rizobios. In: V Congreso Latinoamericano de Agroecología-SOCLA La Plata, Argentina. Available in: http://sedici.unlp.edu.ar/handle/10915/52687 (Accessed in October 2022)

Download references

Acknowledgements

The authors express their gratituded to Programa de desarrollo de Ciencias Básicas (PEDECIBA) and Sistema Nacional de Investigadores (SNI).

Author information

Authors and Affiliations

  1. Laboratorio Microbiología Molecular, Departamento BIOGEM, Instituto de Investigaciones Biológicas Clemente Estable (IIBCE), Av. Italia 3318, 11600, Montevideo, Uruguay

    Elena Fabiano & Raúl Platero

  2. Laboratorio de Microbiología, Facultad de Agronomía, Universidad de la República, Av. Garzón 780, 11300, Montevideo, Uruguay

    Pilar Irisarri & Gastón Azziz

  3. Laboratorio de Microbiología de Suelos, Facultad de Ciencias, Universidad de la República, Igua 4225, 11400, Montevideo, Uruguay

    María Morel

  4. Laboratorio de Bioquímica, Facultad de Agronomía, Universidad de la República, Av. Garzón 780, 11300, Montevideo, Uruguay

    Jorge Monza

Authors
  1. Elena Fabiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raúl Platero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pilar Irisarri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gastón Azziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jorge Monza
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors participated in the writing of the manuscript in general. In particular, EF, RP and GA wrote the section dealing with nodulating rhizobia Mimosoidea clade, while MM, PI and JM wrote the section dealing with nodulating rhizobia Papilionoideas subfamily. All authors read and reviewed the final version, and approved the submission of the manuscript.

Corresponding author

Correspondence to Jorge Monza.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author declares that there is no conflict of interest. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported.

Research involving human participants and/or animals

This research has not involved Human Participants and/or Animals. The submitted work is original and was not submitted been published elsewhere in any form or language.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fabiano, E., Platero, R., Irisarri, P. et al. Rhizobia biodiversity in Uruguay: preservation and uses. Environmental Sustainability 6, 109–119 (2023). https://doi.org/10.1007/s42398-023-00278-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42398-023-00278-5

Keywords

Search

Navigation