Skip to main content
Log in

Diversity and nodulation effectiveness of rhizobia and mycorrhizal presence in climbing dry beans grown in Prespa lakes plain, Greece

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The Prespa lakes plain is an isolated area where about 1000 ha are seeded to Phaseolus vulgaris L. and Phaseolus coccineus L. Nodulation, arbuscular mycorrhizal fungal (AMF) presence and the genetic diversity of rhizobia were evaluated by 16S-ITS-23S-RFLP patterns and by sequencing. The bean rhizobial population in the region was diverse, despite its geographic isolation. No biogeographic relationships were detected, apart from a Rhizobium tropici-related strain that originated from an acidic soil. No clear pattern was detected in clustering with bean species and all isolates formed nodules with both bean species. Most strains were related to Rhizobium leguminosarum and a number of isolates were falling outside the already characterized species of genus Rhizobium. Application of heavy fertilization has resulted in high soil N and P levels, which most likely reduced nodulation and AMF spore presence. However, considerable AMF root length colonization was found in most of the fields.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbaszadeh-dahaji P, Savaghebi GhR, Asadi-rahmani H, Rejali F, Farahbakhsh M, Moteshareh-zadeh D, Omidvari M, Lindstrom K (2012) Symbiotic effectiveness and plant growth promoting traits in some Rhizobium strains isolated from Phaseolus vulgaris L. Plant Growth Regul 68:361–370

    Article  CAS  Google Scholar 

  • Adhikari D, Itoh K, Suyama L (2013) Genetic diversity of common bean (Phaseolus vulgaris L.) nodulating rhizobia in Nepal. Plant Soil 368:341–353

    Article  CAS  Google Scholar 

  • Akter Z, Pageni BB, Lupwayi NZ, Balasubramanian PM (2014) Biological nitrogen fixation and nifH gene expression in dry beans (Phaseolus vulgaris L.). Can J Plant Sci 94:203–212

    Article  CAS  Google Scholar 

  • Álvarez-Martínez ER, Valverde Á, Ramírez-Bahena MH, García-Fraile P, Tejedor C, Mateos PF, Santillana N, Zúñiga D, Peix A, Velázquez E (2009) The analysis of core and symbiotic genes of rhizobia nodulating Vicia from different continents reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarum strains together with Vicia seeds. Arch Microbiol 191:659–668

    Article  PubMed  CAS  Google Scholar 

  • Amarger N, Machere 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  CAS  PubMed  Google Scholar 

  • Andrade DS, Murphy PJ, Giller KE (2002) The diversity of Phaseolus-nodulating rhizobial populations is altered by liming of acid soils planted with Phaseolus vulgaris L. in Brazil. Appl Environ Micorbiol 68:4025–4034

    Article  CAS  Google Scholar 

  • Anguilar OM, López MV, Donato M, Morón B, Soria-Diaz ME, Mateos C, Gil-Serrano A, Sousa C, Megías M (2006) Phylogeny and nodulation signal molecule of rhizobial populations able to nodulate common beans—other than the predominant species Rhizobium etli—present in soils from the northwest of Argentina. Soil Biol Biochem 38:573–586

    Article  CAS  Google Scholar 

  • Aoki S, Kondo T, Prévost D, Nakata S, Kajita T, Ito M (2010) Genotypic and phenotypic diversity of rhizobia isolated from Lathyrus japonicus indigenous to Japan. Syst Appl Microbiol 33:383–397

    Article  CAS  PubMed  Google Scholar 

  • Aouani ME, Mhamdi R, Mars M, Elayeb M, Ghtir R (1997) Potential for inoculation of common bean by effective rhizobia in Tunisian soils. Agronomie 17:445–454

    Article  Google Scholar 

  • Aserse AA, Räsänen LA, Assefa F, Hailemariam A, Lindström K (2012) Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol 35:120–131

    Article  PubMed  Google Scholar 

  • Baginsky C, Brito B, Scherson R, Pertuzé R, Seguelm O, Cañete A, Araneda C, Johnson WE (2015) Genetic diversity of Rhizobium from nodulating beans grown in a variety of Mediterranean climate soils of Chile. Arch Microbiol 197:419–429

    Article  CAS  PubMed  Google Scholar 

  • Bernal G, Graham PH (2001) Diversity in the rhizobia associated with Phaseolus vulgaris L. in Ecuador, and comparisons with Mexican bean rhizobia. Can J Microbiol 47:526–534

    Article  CAS  PubMed  Google Scholar 

  • Bustos P, Santamaria RI, Pérez-Carrascal OM, Acosta JL, Lozano L, Juárez S, Martínez-Flores I, Martínez-Romero E, Cevallos MA, Romero D, Dávila G, Vinuesa P, Miranda F, Ormeρo E, González V (2017) Complete genome sequences of three Rhizobium gallicum symbionts associated with common bean (Phaseolus vulgaris). Genome Announc 11:e00030–17

    Article  Google Scholar 

  • Caballero-Mellado J, Martínez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26:111–121

    Google Scholar 

  • Cao Y, Wang ET, Zhao L, Chen WM, Wei GH (2014) Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem 78:128–137

    Article  CAS  Google Scholar 

  • Dall’Agnol RF, Ribeiro RA, Ormeño-Orrillo E, Rogel MA, Delamuta JRM, Andrade DS, Martínez-Romero E, Hungria M (2013) Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol 63:4167–4173

    Article  PubMed  Google Scholar 

  • Dar GH, Zargar MY, Beigh GM (1997) Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microb Ecol 34:74–80

    Article  Google Scholar 

  • Darriba D, Taboad GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Embalomatis A, Papakosta DK, Katinakis P (1994) Evaluation of Rhizobium meliloti strains isolated from indigenous populations in northern Greece. J Agron Crop Sci 172:73–80

    Article  Google Scholar 

  • García-Fraile P, Mulas-García D, Peix A, Rivas R, González- Andrés F, Velázquez E (2010) Phaseolus vulgaris is nodulated in northern Spain by Rhizobium leguminosarum strains harboring two nodC alleles present in American Rhizobium etli strains: biogeographical and evolutionary implications. Can J Microbiol 56:657–666

    Article  PubMed  CAS  Google Scholar 

  • Giller KE, Cadisch G (1995) Future benefits from biological nitrogen fixation—an ecological approach to agriculture. Plant Soil 174:255–277

    Article  CAS  Google Scholar 

  • Graham PH, Ranalli P (1997) Common bean (Phaseolus vulgaris L.). Field Crops Res 53:131–146

    Article  Google Scholar 

  • Graham PH, Rosas JC, Estevez de Jensen C, Peralta E, Tlusty B, Acosta-Gallegos J, Arraes Perreira PA (2003) Addressing edaphic constrains to bean production: the Bean/Cowpea CRSP project in perspective. Field Crops Res 82:179–192

    Article  Google Scholar 

  • Gryndler H, Leština J, Moravec V, Přikryl Z, Lipavsky J (1989) Colonization of maize roots by VAM-fungi under conditions of long-term fertilization of varying intensity. Agric Ecosyst Environ 29:183–186

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hardarson G, Bliss FA, Cigales-Rivero MR, Henson RA, Kipe-Nolt JA, Longeri L, Manrique A, Pena-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 

  • Haukka K, Lindström K, Young JPW (1996) Diversity of partial 16S rRNA sequences among and within strains of African rhizobia isolated from Acacia and Prosopis. Syst Appl Microbiol 19:352–359

    Article  Google Scholar 

  • Havlin JJ, Tisdale SL, Nelson WL, Beaton JD (2014) Chapter 4: Nitrogen. In: Havlin JJ, Tisdale SL, Nelson WL, Beaton JD (eds) Soil fertility and fertilizers, 8th edn. Pearson, Prentice Hall, Upper Saddle River, pp 117–184

    Google Scholar 

  • Hayman DS (1986) Mycorrhizae of nitrogen-fixing legumes. MIRCEN J 2:121–145

    Article  Google Scholar 

  • Hayman DS, Barea JM, Azcon R (1976) Vesicular-arbuscular mycorrhiza in southern Spain: its distribution in crops growing in soil of different fertility. Phytopathol Mediterr 15:1–6

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hou BC, Wang ET, Li Y, Jia RZ, Chen WF, Man CX, Sui XH, Chen WX (2009) Rhizobial resource associated with epidemic legumes in Tibet. Microb Ecol 57:69–81

    Article  PubMed  Google Scholar 

  • Huang YY, Cho ST, Lo WS, Wang YC, Lai EML, Kuo CH (2015) Complete genome sequence of Agrobacterium tumefaciens Ach5. Genome Announc 3:e00570–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Junier P, Alfaro M, Guevara R, Witzel KP, Carú M (2014) Genetic diversity of Rhizobium present in nodules of Phaseolus vulgaris L. cultivated in two soils of the central region in Chile. Appl Soil Ecol 80:60–66

    Article  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosmas C, Moustakas N, Tsatiris B, Danalatos N (1990) Evaluation of soil resources of the Prespa region, Greece. EEC Project B6617-25-89. Agricultural University of Athens, Athens

    Google Scholar 

  • Kwon SW, Park JY, Kim JS, Kang JW, Cho YH, Lim CK, Parker MA, Lee GB (2005) Phylogenetic analysis of the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium on the basis of 16S rRNA gene and internally transcribed spacer region sequences. Int J Syst Evol Microbiol 55:263–270

    Article  CAS  PubMed  Google Scholar 

  • Laguerre G, Mavingui P, Allard MR, Charnay MP, Louvrier P, Mazurier SI, Rigottier-Gois L, Amarger N (1996) Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-López A, Rogel-Hernández MA, Barois I, Ceballos AIO, Martínez J, Ormeño-Orrillo E, Martínez-Romero E (2012) Rhizobium grahamii sp. nov., from nodules of Dalea leporina, Leucaena leucocephala and Clitoria ternatea, and Rhizobium mesoamericanum sp. nov., from nodules of Phaseolus vulgaris, siratro, cowpea and Mimosa pudica. Int J Syst Evol Microbiol 62:2264–2271

    Article  PubMed  CAS  Google Scholar 

  • Mavromatis AG, Arvanitoyannis S, Korkovelos AE, Giakountis A, Chatzitheodorou VA, Goulas CK (2010) Genetic diversity among common bean (Phaseolus vulgaris L.) Greek landraces and commercial cultivars: nutritional components, RAPD and morphological markers. Span J Agric Res 8:986–994

    Article  Google Scholar 

  • Mhamdi R, Jebara M, Aouani ME, Ghrir R, Mars M (1999) Genotypic diversity and symbiotic effectiveness of rhizobia isolated from roots nodules of Phaseolus vulgaris L., grown in Tunisian soils. Biol Fertil Soil 28:313–320

    Article  Google Scholar 

  • Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Mnasri B, Saïdi S, Chihaou SA, Mhamdi R (2012) Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a northern Tunisian field. Syst Appl Microbiol 35:263–269

    Article  CAS  PubMed  Google Scholar 

  • Mnasri B, Liu TY, Saidi S, Chen WF, Chen WX, Zhang XX, Mhamdi R (2014) Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 64:1501–1506

    Article  CAS  PubMed  Google Scholar 

  • Nelson M, Guhlin J, Epstein B, Tiffin P, Sadowsky MJ (2018) The complete replicons of 16 Ensifer meliloti strains offer insights into intra-and inter-replicon gene transfer, transposon-associated loci, and repeat elements. Microb Genom 4:e000174

    PubMed Central  Google Scholar 

  • Oliveira JP, Galli-Terasawa LV, Enke CG, Cordeiro VK, Armstrong LCT, Hungria M (2011) Genetic diversity of rhizobia in a Brazilian oxisol nodulating Mesoamerican and Andean genotypes of common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 27:643–650

    Article  Google Scholar 

  • Pavel BA, Vasile CI (2012) PyElph—a software tool for gel images analysis and phylogenetices. BMC Bioinform 13:9

    Article  Google Scholar 

  • Pérez-Ramírez NO, Rogel MA, Wang E, Castellanos JZ, Martínez-Romero E (1998) Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol Ecol 26:289–296

    Article  Google Scholar 

  • Prévost D, Antoun H (2007) Root nodule bacteria and symbiotic nitrogen fixation, Chapter 31. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis. CRC Press, Boca Raton, pp 379–397

    Google Scholar 

  • Rahmani ΗΑ, Räsänen LA, Afshari M, Lindström K (2011) Genetic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in soils of Iran. Appl Soil Ecol 48:287–293

    Article  Google Scholar 

  • Redecker D, von Berswordt-Wallrabe P, Beck DP, Werner D (1997) Influence of inoculation with arbuscular mycorrhizal fungi on stable isotopes of nitrogen in Phaseolus vulgaris. Biol Fert Soils 24:344–346

    Article  CAS  Google Scholar 

  • Rodriguez-Navarro DN, Buendia AM, Camacho M, Lucas MM, Santamaria C (2000) Characterization of Rhizobium spp. bean isolates from south west Spain. Soil Biol Biochem 32:1601–1613

    Article  CAS  Google Scholar 

  • Santamaría RI, Bustos P, Pérez-Carrascal OM, Miranda-Sánchez F, Vinuesa P, Martínez-Flores I, Juárez S, Lozano L, Martínez-Romero E, Cevallos MA, Romero D, Dávila G, Ormeño-Orrillo E, González V (2017) Complete genome sequences of eight Rhizobium symbionts associated with common bean (Phaseolus vulgaris). Genome Announc 5:e00645–17

    Article  PubMed  PubMed Central  Google Scholar 

  • Sessitch A, Ramirez-Saad H, Hardarson G, Akkermans ADL, DeVos WM (1997) Classification of Austrian rhizobia and the Mexican isolate FL27 obtained from Phaseolus vulgaris L. as Rhizobium gallicum. Int J Syst Bacteriol 47:1097–1101

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego

    Google Scholar 

  • Somasegaran P, Hoben HJ (1985) Methods in legume-rhizobium technology. University of Hawaii NifTAL Project and MIRCEN

  • Sylvia DM (1994) Vesicular-arbuscular mycorrhizal (VAM) fungi. In: Weaver RW, Angle JS, Bottomley PJ, Bezdicek D, Smith S, Tabatabai A, Wollum AG (eds) Methods of soil analysis, Part 2. Microbiological and biochemical properties, vol 5. Soil Science Society of America, Madison, pp 351–378

    Google Scholar 

  • Tamimi SM (2002) Genetic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of common bean (Phaseolus vulgaris L.) grown in the soils of the Jordan valley. Appl Soil Ecol 19:183–190

    Article  Google Scholar 

  • Tertivanidis K, Koutita O, Papadopoulos II, Tokatlidis IS, Tamoutsidis EG, Pappa-Michailidou V, Koutsika-Sotiriou M (2008) Genetic diversity in bean populations based on random amplified polymorphic DNA markers. Biotechnology 7:1–9

    Article  CAS  Google Scholar 

  • Thies JE, Bohlool BB, Singleton PW (1992) Environmental effects on competition for nodule occupancy between introduced and indigenous rhizobia and among introduced strains. Can J Microbiol 38:493–500

    Article  Google Scholar 

  • Valverde A, Ingua JM, Peix A, Cervantes E, Velásquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol 56:2631–2637

    Article  CAS  PubMed  Google Scholar 

  • Van Cauwenberghe J, Verstraete B, Lemaire B, Lievens B, Michiels J, Honnay O (2014) Population structure of root nodulating Rhizobium leguminosarum in Vicia cracca populations at local to regional geographic scales. Syst Appl Microbiol 37:613–621

    Article  PubMed  Google Scholar 

  • Wang L, Cao Y, Wang ET, Qiao YJ, Jiao S, Liu ZS, Zhao L, Wei GH (2016) Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi province. Syst Appl Microbiol 39:211–219

    Article  PubMed  Google Scholar 

  • Wei GH, Zhang ZX, Chen C, Chen WM, Ju WT (2008) Phenotypic and genetic diversity of rhizobia isolated from nodules of the legume genera Astragalus, Lespedeza and Hedysarum in northwestern China. Microbiol Res 163:651–662

    Article  CAS  PubMed  Google Scholar 

  • Yan H, Ji ZJ, Jiao YS, Wang ET, Chen WF, Guo BL, Chen WX (2016) Genetic diversity and distribution of rhizobia associated with the medicinal legumes Astragalus spp. and Hedysarum polybotrys in agricultural soils. Syst Appl Microbiol 39:141–149

    Article  PubMed  Google Scholar 

  • Zurdo-Piñeiro JL, García-Fraile P, Rivas R, Peix A, León-Barrios M, Willems A, Mateos PF, Martínez-Molina E, Velázquez E, van Berkum P (2009) Rhizobia from Lanzarote, the Canary Islands, that nodulate Phaseolus vulgaris have characteristics in common with Sinorhizobium meliloti isolates from mainland Spain. Appl Environ Microbiol 75:2354–2359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Research Committee of Aristotle University of Thessaloniki (Grant number 89313). The authors would also like to thank Kyriaki Kosmanidou and the “Pelecanos” cooperative for their assistance in field sampling.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ioannis Ipsilantis.

Additional information

Communicated by Yusuf Akhter.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

S 1

. Agarose gel of the PCR products where multiple or single band may be observed before (left) and after HaeII digestion (right). Highlighted are the bands that were successfully sequenced. M: 100 base DNA ladder marker, 1: PYL2, 2: ORM3, 3: ORM1, 4: PYL6, 5: PYL7, 6: SLL3, 7: SLL7, 8: PYL6, 9: KAR6, 10: ORM4, 11: SLL8, 12: PYL5, 13: ERG2, 14: LAI3 (DOCX 142 kb)

S 2

. Agarose gel of the PCR products where multiple or single band may be observed before (up) and after HaeII digestion (down). Highlighted are the bands that were successfully sequenced. M: 100 base DNA ladder marker, 1: ORM2, 2: PYL3, 3: KAR1, 4: KAR7, 5: KAR9, 6: SLL1, 7: PYL2, 8: MIK3, 9: KAR2, 10: KAR8, 11: SLL6, 12: SLA2, 13: LAI2, 14: PYL4, 16: SLL12, 17: SLA5, 18: OPA1, 19: GRA4, 20: GRA5, 21: PYL1, 22: PYL9, 23: SLA1, 24: LAI5, 25: GRA2, 26: SLL4, 27: GRA3, 28: MIK 7, 29: MIK5, 30: JUM1, 31: MIK2, 32: LAI3, 33: GRA1, 34: LAI6, 35: LAI4, 36: OPA2, 37: MIK1 38: SLA4, 39: LAI8, 40: LAI7, 41: SLL5, 42: KAR4, 43: MIK4, 44: KAR5, 45: SLL13, 46: MIK6, 47: ERG1, 48: SLL2, 49: PYL10, 50: PYL11, 51: ORM5, 52: KAR10, 53: KAR11, 54: ORM6, 55: KAR12. Note that JUM1 is an isolate from Florina, an area close, but outside the Prespa lakes area (DOCX 328 kb)

S 3.

Agarose gel of the PCR products after MspI digestion. M: 100 base DNA ladder marker. 1: ERG1, 2: SLL11, 3: MIK6, 4: KAR3, 6: KAR6, 7: PYL5, 8: KAR1, 9: KAR4, 10: KAR7, 11: KAR9, 12: LAI6, 13: GRA1, 14: LAI7, 15: LAI1, 16: GRA1, 17: KAR5, 18: MIK4, 19: OPA1, 21: GRA2, 22: MIK5, 23: MIK2, 24: MIK7, 25: MIK3, 26: PYL2, 27: LAI3, 28: ERG2, 30: SLL3, 31: SLL7, 32: ORM1, 33: SLL4, 34: PYL4, 36: GRA2, 37: KAR2, 38: SLA1, 39: SLA1, 40: SLL1, 43: KAR3, 44: LAI2, 45: PYL6, 46: PYL7, 47: SLA2, 48: KAR8, 50: KAR9, 51: SLL7, 52: SLL12, 53: GRA3, 54: ERG1 (DOCX 200 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ipsilantis, I., Lotos, L. & Tsialtas, I.T. Diversity and nodulation effectiveness of rhizobia and mycorrhizal presence in climbing dry beans grown in Prespa lakes plain, Greece. Arch Microbiol 201, 1151–1161 (2019). https://doi.org/10.1007/s00203-019-01679-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-019-01679-z

Keywords

Navigation