Skip to main content

Advertisement

Log in

The Fodder Legume Chamaecytisus albidus Establishes Functional Symbiosis with Different Bradyrhizobial Symbiovars in Morocco

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In this work, we analyzed the symbiotic performance and diversity of rhizobial strains isolated from the endemic shrubby legume Chamaecytisus albidus grown in soils of three different agroforestry ecosystems representing arid and semi-arid forest areas in Morocco. The analysis of the rrs gene sequences from twenty-four representative strains selected after REP-PCR fingerprinting showed that all the strains belong to the genus Bradyrhizobium. Following multi-locus sequence analysis (MLSA) using the rrs, gyrB, recA, glnII, and rpoB housekeeping genes, five representative strains, CA20, CA61, CJ2, CB10, and CB61 were selected for further molecular studies. Phylogenetic analysis of the concatenated glnII, gyrB, recA, and rpoB genes showed that the strain CJ2 isolated from Sahel Doukkala soil is close to Bradyrhizobium canariense BTA-1 T (96.95%); that strains CA20 and CA61 isolated from the Amhach site are more related to Bradyrhizobium valentinum LmjM3T, with 96.40 and 94.57% similarity values; and that the strains CB10 and CB60 isolated from soil in the Bounaga site are more related to Bradyrhizobium murdochi CNPSo 4020 T and Bradyrhizobium. retamae Ro19T, with which they showed 95.45 and 97.34% similarity values, respectively. The phylogenetic analysis of the symbiotic genes showed that the strains belong to symbiovars lupini, genistearum, and retamae. All the five strains are able to nodulate Lupinus luteus, Retama monosperma, and Cytisus monspessilanus, but they do not nodulate Glycine max and Phaseolus vulgaris. The inoculation tests showed that the strains isolated from the 3 regions improve significantly the plant yield as compared to uninoculated plants. However, the strains of Bradyrhizobium sp. sv. retamae isolated from the site of Amhach were the most performing. The phenotypic analysis showed that the strains are able to use a wide range of carbohydrates and amino acids as sole carbon and nitrogen source. The strains isolated from the arid areas of Bounaga and Amhach were more tolerant to salinity and drought stress than strains isolated in the semi-arid area of Sahel Doukkala.

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
Fig. 3

Similar content being viewed by others

Data Availability

All the sequences described in this work are deposited in the Genbank depository of the National Center for Biotechnology Information (NCBI). Each sequence has an accession number and is easily available to all researchers worldwide.

References

  1. Schrire BD, Lavin M, Lewis GP (2005) Global distribution patterns of the Leguminosae: insights from recent phylogenies. In: Plant diversity and complexity patterns: local, regional and global dimensions. Proceedings of an International Symposium held at the Royal Danish Academy of Sciences and Letters in Copenhagen, Denmark, 25–28 May, 2003. Det Kongelige Danske Videnskabernes Selskab, pp 375–422

  2. Yahara T, Javadi F, Onoda Y et al (2013) Global legume diversity assessment: concepts, key indicators, and strategies. Taxon 62:249–266. https://doi.org/10.12705/622.12

    Article  Google Scholar 

  3. Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 215:40–56

    Article  CAS  PubMed  Google Scholar 

  4. Koenen EJM, Ojeda DI, Steeves R et al (2020) Large-scale genomic sequence data resolve the deepest divergences in the legume phylogeny and support a near-simultaneous evolutionary origin of all six subfamilies. New Phytol 225:1355–1369. https://doi.org/10.1111/nph.16290

    Article  CAS  PubMed  Google Scholar 

  5. González-Andrés F, Ortiz JM (1996) Potential of Cytisus and allied genera (Genisteae: Fabaceae) as forage shrubs: 1. Seed germination and agronomy. New Zeal J Agric Res 39:195–204. https://doi.org/10.1080/00288233.1996.9513178

    Article  Google Scholar 

  6. Sprent JI, Gehlot HS (2010) Nodulated legumes in arid and semi-arid environments: are they important? Plant Ecol Divers 3:211–219. https://doi.org/10.1080/17550874.2010.538740

    Article  Google Scholar 

  7. Lefroy EC, Dann PR, Wildin JH et al (1992) Trees and shrubs as sources of fodder in Australia. Agrofor Syst 20:117–139. https://doi.org/10.1007/BF00055307

    Article  Google Scholar 

  8. König D (1992) The potential of agroforestry methods for erosion control in Rwanda. Soil Technol 5:167–176

    Article  Google Scholar 

  9. Heywood VH, Frodin DG (1968) Chamaecytisus Link. In: Tutin TG, Heywood VH, Burges NA et al (eds) Flora Europaea: Rosaceae to Umbelliferae. Cambridge University Press, Flora Europaea, pp 90–93

    Google Scholar 

  10. Cristofolini G (1991) Taxonomic revision of Cytisus desf. sect. Tubocytisus DC. (Fabaceae). Webbia 45:187–219. https://doi.org/10.1080/00837792.1991.10670496

    Article  Google Scholar 

  11. Francisco-Ortega J, Jackson MT, Santos-Guerra A, Fernández-Galván M (1991) Historical aspects of the origin and distribution of tagasaste (Chamaecytisus proliferus (L. fil.) Link ssp. palmensis (Christ) Kunkel), a fodder tree from the Canary Islands. J Adelaide Bot Gard 14:67–76

    Google Scholar 

  12. Snook LC (1995) Tagasaste: A productive browse shrub for sustainable agriculture, 2nd ed. Agrovision

  13. Zhigunova SN, Fedorov NI, Mihaylenko OI (2013) Distribution and productivity of Chamaecytisus ruthenicus (Fabaceae) in plant communities of Bashkortostan Republic. Rastit Resur 49:353–359

    Google Scholar 

  14. Naggar M (1993) Place des arbustes fourragers dans les aménagements sylvo-pastoraux. Cas de l’arbuste Chamaecytisus albidus dans les parcours du Sahel des Doukkala et du Nord d’Abda (Province d’El Jadida et Safi Maroc). For méd 14(3):256–264

  15. Skawińska M, Łotocka B, Ruszkowski T et al (2017) Root nodule structure in Chamaecytisus podolicus. Acta Agrobot 70:1716. https://doi.org/10.5586/aa.1716

  16. Fennan M, Ibn Tattou M, Ouyahya A, Jalal E (2007) Flore pratique du Maroc : Manuel de détermination des plantes vasculaires. Vol 2, Trav Inst Sci, sér. Bot. 38, Rabat Institut. Morocco

  17. Bammi J, Mouhiddine M, Fassi D, Douira A (2014) Contribution à la connaissance de la végétation des Doukkala-Abda (Maroc Atlantique): Approche éco-géomorphologique. J Anim Plant Sci 20:3202–3211

    Google Scholar 

  18. Tellal R, Qarro M, Barbero M (1999) Productivité herbacée des périmètres améliorés du Sahel marocain. I : Effet des conditions stationnelles, climatiques et du rythme de coupe. Fourrag 149–156

  19. Vinuesa P, León-Barrios M, Silva C et al (2005) Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Brady. Int J Syst Evol Microbiol 55:569–575. https://doi.org/10.1099/ijs.0.63292-0

    Article  CAS  PubMed  Google Scholar 

  20. Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume - rhizobial mutualism. Cell Microbiol 14:334–342. https://doi.org/10.1111/j.1462-5822.2011.01736.x

    Article  CAS  PubMed  Google Scholar 

  21. Andrews M, Andrews ME (2017) Specificity in legume-rhizobia symbioses. Int J Mol Sci 18:705. https://doi.org/10.3390/ijms18040705

    Article  CAS  PubMed Central  Google Scholar 

  22. Estrada-de los Santos P, Palmer M, Chávez-Ramírez B et al (2018) Whole genome analyses suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes (Basel) 9:389. https://doi.org/10.3390/genes9080389

    Article  CAS  Google Scholar 

  23. Velázquez E, García-Fraile P, Ramírez-Bahena M-H et al (2017) Current status of the taxonomy of bacteria able to establish nitrogen-fixing legume symbiosis. In: Zaidi A, Khan MS, Musarrat J (eds) Microbes for Legume Improvement, 2nd ed. Springer, Cham, pp 1–43

    Google Scholar 

  24. Leon-Barrios M, Gutierrez-Navarro AM, Perez-Galdona R, Corzo J (1991) Characterization of canary island isolates of Bradyrhizobium sp. (Chamaecytisus proliferus). Soil Biol Biochem 23:487–489. https://doi.org/10.1016/0038-0717(91)90015-C

    Article  CAS  Google Scholar 

  25. Bouhnik O, Lamin H, Alami S, et al (2021) The endemic Chamaecytisus albidus is nodulated by symbiovar genistearum of Bradyrhizobium in the Moroccan Maamora Forest. Syst Appl Microbiol 126197

  26. Ouhamdouch S, Bahir M (2017) Climate change impact on future rainfall and temperature in semi-arid areas (Essaouira Basin, Morocco). Environ Process 4:975–990. https://doi.org/10.1007/s40710-017-0265-4

    Article  Google Scholar 

  27. Choukrani G, Hamimsa A, Saidi ME, Babqiqi A (2018) Diagnosis and future projection of climate change in arid zone. Case of Marrakech-Safi region (Morocco). LARHYSS J P-ISSN 1112–3680/E-ISSN 2521–9782 59–63

  28. Ekouele Mbaki VR, Boukdir A, Menga Okandza P, et al (2016) Quantitative analysis of the water potential in the region of Sahel Doukkala (Morocco). J Water Sci Environ Technol 1:

  29. Hungria M, O’Hara GW, Zilli JE, et al (2016) Isolation and growth of rhizobia. In: Howieson JG, Dilworth MJ (eds) Working with rhizobia. Australian Centre for International Agricultural Research, pp 39–60

  30. Guerrouj K, Pérez-Valera E, Chahboune R et al (2013) Identification of the rhizobial symbiont of Astragalus glombiformis in Eastern Morocco as Mesorhizobium camelthorni. Antonie Van Leeuwenhoek 104:187–198

    Article  CAS  PubMed  Google Scholar 

  31. Mohamed SH, Smouni A, Neyra M et al (2000) Phenotypic characteristics of root-nodulating bacteria isolated from Acacia spp. grown in Libya. Plant Soil 224:171–183. https://doi.org/10.1023/A:1004838218642

    Article  CAS  Google Scholar 

  32. Chen W, Kuo T (1993) A simple and rapid method for the preparation of gram- negative bacterial genomic DNA. Nucleic Acids Res 21:2260. https://doi.org/10.1093/nar/21.9.2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. DeBruijn FJ (1992) Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl Environ Microbiol 58:2180–2187

    Article  CAS  Google Scholar 

  34. Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302

    Article  Google Scholar 

  35. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stępkowski T, Moulin L, Krzyżańska A et al (2005) European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl Environ Microbiol 71:7041–7052

    Article  PubMed  PubMed Central  Google Scholar 

  37. Martens M, Dawyndt P, Coopman R et al (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214

    Article  CAS  PubMed  Google Scholar 

  38. Vinuesa P, Silva C, Werner D, Martínez-Romero E (2005) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29–54. https://doi.org/10.1016/j.ympev.2004.08.020

    Article  CAS  PubMed  Google Scholar 

  39. Laguerre G, Nour SM, Valérie M, et al (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 981–993

  40. Chaintreuil C, Boivin C, Dreyfus B, Giraud E (2001) Characterization of the common nodulation genes of the photosynthetic Bradyrhizobium sp. ORS285 reveals the presence of a new insertion sequence upstream of nodA. FEMS Microbiol Lett 194:83–86. https://doi.org/10.1016/S0378-1097(00)00512-7

    Article  CAS  PubMed  Google Scholar 

  41. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  42. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 461–464

  44. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  45. Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 1075–1080

  46. Kalita M, Małek W, Coutinho TA (2020) Putative novel Bradyrhizobium and Phyllobacterium species isolated from root nodules of Chamaecytisus ruthenicus. Syst Appl Microbiol 43:126056. https://doi.org/10.1016/j.syapm.2020.126056

    Article  CAS  PubMed  Google Scholar 

  47. Yao Y, Sui XH, Zhang XX et al (2015) Bradyrhizobium erythrophlei sp. nov. and Bradyrhizobium ferriligni sp. nov., isolated from effective nodules of Erythrophleum fordii. Int J Syst Evol Microbiol 65:1831–1837. https://doi.org/10.1099/ijs.0.000183

    Article  CAS  PubMed  Google Scholar 

  48. Vinuesa P, Rademaker JLW, De Bruijn FJ, Werner D (1998) Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the canary islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S–23S rDNA intergenic spacers, repetitive extr. Appl Environ Microbiol 64:2096–2104. https://doi.org/10.1128/aem.64.6.2096-2104.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Helene LCF, Klepa MS, O’hara G, Hungria M, (2020) Bradyrhizobium archetypum sp. Nov., Bradyrhizobium australiense sp. nov. and Bradyrhizobium murdochi sp. nov., isolated from nodules of legumes indigenous to Western Australia. Int J Syst Evol Microbiol 70:4623–4636. https://doi.org/10.1099/ijsem.0.004322

    Article  CAS  PubMed  Google Scholar 

  50. Guerrouj K, Ruíz-Díez B, Chahboune R et al (2013) Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 36:218–223

    Article  CAS  PubMed  Google Scholar 

  51. Msaddak A, Rejili M, Durán D et al (2018) Definition of two new symbiovars, sv. lupini and sv. mediterranense, within the genera Bradyrhizobium and Phyllobacterium efficiently nodulating Lupinus micranthus in Tunisia. Syst Appl Microbiol 41:487–493

    Article  PubMed  Google Scholar 

  52. Chahboune R, Carro L, Peix A et al (2012) Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst Appl Microbiol 35:302–305

    Article  CAS  PubMed  Google Scholar 

  53. Sprent JI, Odee DW, Dakora FD (2010) African legumes: a vital but under-utilized resource. J Exp Bot 61:1257–1265. https://doi.org/10.1093/jxb/erp342

    Article  CAS  PubMed  Google Scholar 

  54. Polain Le, de Waroux Y, Lambin EF (2012) Monitoring degradation in arid and semi-arid forests and woodlands: The case of the argan woodlands (Morocco). Appl Geogr 32:777–786. https://doi.org/10.1016/j.apgeog.2011.08.005

    Article  Google Scholar 

  55. El Aboudi A, Peltier JP, Doche B (1992) La carte de la végétation des Aït-Baha (Anti-Atlas occidental, Maroc) et son intérêt pour l’édaphologie. Feddes Repert 103:121–126

    Article  Google Scholar 

  56. Menna P, Pereira AA, Bangel EV, Hungria M (2009) Rep-PCR of tropical rhizobia for strain fingerprinting, biodiversity appraisal and as a taxonomic and phylogenetic tool. Symbiosis 48:120–130

    Article  CAS  Google Scholar 

  57. Binde DR, Menna P, Bangel EV et al (2009) rep-PCR fingerprinting and taxonomy based on the sequencing of the 16S rRNA gene of 54 elite commercial rhizobial strains. Appl Microbiol Biotechnol 83:897–908. https://doi.org/10.1007/s00253-009-1927-6

    Article  CAS  PubMed  Google Scholar 

  58. Baimiev AK, Ivanova ES, Gumenko RS et al (2015) Analysis of symbiotic genes of leguminous root nodule bacteria grown in the southern Urals. Russ J Genet 51:1172–1180. https://doi.org/10.1134/S1022795415110034

    Article  CAS  Google Scholar 

  59. Menna P, Barcellos FG, Hungria M (2009) Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int J Syst Evol Microbiol 59:2934–2950. https://doi.org/10.1099/ijs.0.009779-0

    Article  CAS  PubMed  Google Scholar 

  60. Zhang YM, Tian CF, Sui XH et al (2012) Robust markers reflecting phylogeny and taxonomy of rhizobia. PLoS ONE 7:7–12. https://doi.org/10.1371/journal.pone.0044936

    Article  CAS  Google Scholar 

  61. DeLajudie PM, Andrews M, Ardley J et al (2019) Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst Evol Microbiol 69:1852–1863. https://doi.org/10.1099/ijsem.0.003426

    Article  CAS  Google Scholar 

  62. Durán D, Rey L, Navarro A et al (2014) Bradyrhizobium valentinum sp. nov., isolated from effective nodules of Lupinus mariae-josephae, a lupine endemic of basic-lime soils in Eastern Spain. Syst Appl Microbiol 37:336–341

    Article  PubMed  Google Scholar 

  63. Yates RJ, Howieson JG, Nandasena KG, O’Hara GW (2004) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 36:1319–1329. https://doi.org/10.1016/j.soilbio.2004.04.013

    Article  CAS  Google Scholar 

  64. Ormeno-Orrillo E, Vinuesa P, Zuniga-Davila D, Martínez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Peru. Syst Appl Microbiol 29:253–262

    Article  CAS  PubMed  Google Scholar 

  65. Duran D, Rey L, Mayo J et al (2014) Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 64:2072–2078

    Article  PubMed  Google Scholar 

  66. El Adnani I, Younsi A, Namr KI, El Achheb A (2020) Assessment of seasonal and spatial variation of groundwater quality in the coastal Sahel of Doukkala, Morocco. Nat Environ Pollut Technol 19:17–28

    Google Scholar 

  67. Cherki K (2013) Analyse de la répartition spatiale des incendies de forêt en fonction des facteurs anthropiques, écologiques et biophysiques Le cas de la forêt de la Mâamora (Maroc septentrional). Études caribéennes. https://doi.org/10.4000/etudescaribeennes.10978

    Article  Google Scholar 

  68. Raza S, Jørnsgård B, Abou-Taleb H, Christiansen JL (2001) Tolerance of Bradyrhizobium sp. (Lupini) strains to salinity, pH, CaCO3 and antibiotics. Lett Appl Microbiol 32:379–383. https://doi.org/10.1046/j.1472-765X.2001.00925.x

    Article  CAS  PubMed  Google Scholar 

  69. Suzuki Y, Adhikari D, Itoh K, Suyama K (2014) Effects of temperature on competition and relative dominance of Bradyrhizobium japonicum and Bradyrhizobium elkanii in the process of soybean nodulation. Plant Soil 374:915–924. https://doi.org/10.1007/s11104-013-1924-5

    Article  CAS  Google Scholar 

  70. Puozaa DK, Jaiswal SK, Dakora FD (2017) African origin of Bradyrhizobium populations nodulating Bambara groundnut (Vigna subterranea L. Verdc) in Ghanaian and South African soils. PLoS ONE 12:1–23. https://doi.org/10.1371/journal.pone.0184943

    Article  CAS  Google Scholar 

  71. Clúa J, Roda C, Zanetti ME, Blanco FA (2018) Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis. Genes (Basel) 9:125

    Article  Google Scholar 

  72. Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: From saprophytes to endosymbionts. Nat Rev Microbiol 16:291–303. https://doi.org/10.1038/nrmicro.2017.171

    Article  CAS  PubMed  Google Scholar 

  73. Okazaki S, Noisangiam R, Okubo T et al (2015) Genome analysis of a novel Bradyrhizobium sp. DOA9 carrying a symbiotic plasmid. PLoS ONE 10:e0117392

    Article  PubMed  PubMed Central  Google Scholar 

  74. Moulin L, Béna G, Boivin-Masson C, Stępkowski T (2004) Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol 30:720–732

    Article  CAS  PubMed  Google Scholar 

  75. Menna P, Hungria M (2011) Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer. Int J Syst Evol Microbiol 61:3052–3067

    Article  CAS  PubMed  Google Scholar 

  76. Rogel MA, Ormeño-Orrillo E, Martinez Romero E (2011) Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 34:96–104. https://doi.org/10.1016/j.syapm.2010.11.015

    Article  PubMed  Google Scholar 

  77. Stępkowski T, Hughes CE, Law IJ et al (2007) Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Environ Microbiol 73:3254–3264

    Article  PubMed  PubMed Central  Google Scholar 

  78. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial Associations with Legumes. CRC Crit Rev Plant Sci 34:17–42. https://doi.org/10.1080/07352689.2014.897899

    Article  Google Scholar 

  79. Delamuta JRM, Menna P, Ribeiro RA, Hungria M (2017) Phylogenies of symbiotic genes of Bradyrhizobium symbionts of legumes of economic and environmental importance in Brazil support the definition of the new symbiovars pachyrhizi and sojae. Syst Appl Microbiol 40:254–265

    Article  CAS  PubMed  Google Scholar 

  80. Bromfield ESP, Cloutier S (2021) Bradyrhizobium septentrionale sp. Nov. (sv. septentrionale) and Bradyrhizobium quebecense sp. nov. (sv. septentrionale) associated with legumes native to canada possess rearranged symbiosis genes and numerous insertion sequences. Int J Syst Evol Microbiol 71:. https://doi.org/10.1099/ijsem.0.004831

  81. Ferraz Helene LC, O’Hara G, Hungria M (2020) Characterization of Bradyrhizobium strains indigenous to Western Australia and South Africa indicates remarkable genetic diversity and reveals putative new species. Syst Appl Microbiol 43:126053. https://doi.org/10.1016/j.syapm.2020.126053

    Article  CAS  PubMed  Google Scholar 

  82. Klepa MS, Helene LCF, O’hara G, Hungria M (2021) Bradyrhizobium agreste sp. Nov., Bradyrhizobium glycinis sp. nov. and Bradyrhizobium diversitatis sp. nov., isolated from a biodiversity hotspot of the genus glycine in Western Australia. Int J Syst Evol Microbiol 71:. https://doi.org/10.1099/ijsem.0.004742

  83. Chahboune R, Carro L, Peix A et al (2011) Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus. Int J Syst Evol Microbiol 61:2922–2927

    Article  PubMed  Google Scholar 

  84. Bourebaba Y, Durán D, Boulila F et al (2016) Diversity of Bradyrhizobium strains nodulating Lupinus micranthus on both sides of the Western Mediterranean: Algeria and Spain. Syst Appl Microbiol 39:266–274

    Article  PubMed  Google Scholar 

  85. Ahnia H, Bourebaba Y, Durán D et al (2018) Bradyrhizobium algeriense sp. nov., a novel species isolated from effective nodules of Retama sphaerocarpa from Northeastern Algeria. Syst Appl Microbiol 41:333–339. https://doi.org/10.1016/j.syapm.2018.03.004

    Article  PubMed  Google Scholar 

  86. Ormeño-Orrillo E, Martínez-Romero E (2013) Phenotypic tests in Rhizobium species description: an opinion and (a sympatric speciation) hypothesis. Syst Appl Microbiol 36:145–147. https://doi.org/10.1016/j.syapm.2012.11.009

    Article  PubMed  Google Scholar 

  87. Bejarano A, Silva LR, Andrade P et al (2016) Different effects on Vigna unguiculata plants after the inoculation with strains from two Bradyrhizobium symbiovars. In: González-Andrés F, James E (eds) Biological Nitrogen Fixation and Beneficial Plant-Microbe Interaction. Springer, Cham, pp 131–140

    Chapter  Google Scholar 

Download references

Acknowledgements

The authors want to thank all the people who contributed to the achievement of this study.

Funding

Financial support was obtained from Académie Hassan II des Sciences et Techniques (in Morocco). Mr Omar Bouhnik received a grant from the Hassan II Academy of Science and Technology.

Author information

Authors and Affiliations

Authors

Contributions

OB carried out the experiments and participated in the analysis and interpretation of data and writing the manuscript. SA, HA, ML, MB, MO, MB, YA, and SE participated in the samplings and the acquisition and interpretation of the results. HA participated to the design of the work and interpretation of results. EJB contributed to the acquisition of data and revising the manuscript critically for important intellectual content. MME contributed to the conception and design of the work, interpretation of the data, writing the paper, and revising it. All the authors contributed to the final version of the paper.

Corresponding author

Correspondence to Omar Bouhnik.

Ethics declarations

Consent for publication

The authors all contributed to this work and agree to publish the results.

Competing Interests

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 884 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bouhnik, O., Alami, S., Lamin, H. et al. The Fodder Legume Chamaecytisus albidus Establishes Functional Symbiosis with Different Bradyrhizobial Symbiovars in Morocco. Microb Ecol 84, 794–807 (2022). https://doi.org/10.1007/s00248-021-01888-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01888-4

Keywords

Navigation