Skip to main content
SpringerLink
Log in

Identification of the symbiovar maamori in Mesorhizobium isolated from nodules of Ononis repens in the Maamora forest (Morocco)

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Ononis repens is a legume of the Fabaceae family with great ecological and medicinal importance that grows wild in the Maamora cork oak forest (Rabat, Morocco). The aim of this work was to analyze the diversity, phylogeny, and plant growth-promoting features of the plant root nodules microsymbionts. Out of twenty nodC-containing rhizobial bacteria, four strains, ORM6, ORM8.1, ORM 13.1, and ORM16, were selected for further molecular and phenotypic analyses. All four strains were able to metabolize a wide range of carbohydrates and amino acids as sole carbon and nitrogen sources, respectively, and grew in the presence of different pH, NaCl, and temperature conditions. They also solubilized inorganic phosphate and produced siderophores, and ORM16 was the only strain to produce indol acetic acid. The rrs gene sequence analysis showed that the four strains are members of the Mesorhizobium genus. The individual and concatenated sequences of the recA, glnII, and gyrB housekeeping genes revealed that the strains ORM6 and ORM 13.1 clustered with M. jarvisii ATCC 33,669T and M. intechii BD68 T, with which they share 93.3 and 93.7% similarity, respectively; that the strain ORM8.1 affiliated with a group of which the strain M. shonense AC39aT was the closest relative species with 84.3% similarity; and that the strain ORM16 clustered with M. australicum LMG24608T, with 80.5% similarity. These results suggest that the four O. repens-isolated strains could belong to three putative new genospecies. All four strains nodulated their original host as well as Astragalus gombiformis and A. armatus, but only the strain ORM16 was able to form nodules on Vachellia gummifera. Analysis of the symbiotic nodC gene phylogenies showed that the strains ORM6, ORM8.1, ORM 13.1, and ORM16 formed a group apart from the known symbiovars in the genus Mesorhizobium, for which the name maamori is proposed.

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
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).

References

  • Aafi A, El Kadmiri AA, Benabid B, Rochdi M (2005) Richesse et diversité floristique de la suberaie de la Mamora (Maroc). Acta Bot Malacit 30:127–138

    Article  Google Scholar 

  • Abdelguerfi A, Abdelguerfi-Laouar M (2004) Les ressources génétiques d’intérêt fourrager et/ou pastoral: Diversité, collecte et valorisation au niveau méditerranéen. Cah Opt Méd 62:29–41

    Google Scholar 

  • Abdel-Kader MS (2001) Phenolic constituents of Ononis vaginalis roots. Planta Med 67:388–390

    Article  CAS  Google Scholar 

  • Agulló JC, Juan A, Alonso M, Terrones A, Crespo MB (2013) Taxonomic status of Ononis tridentata (Fabaceae) from Morocco, resolved by multivariate morphometric analyses. Plant Biosystems 147:645–653. https://doi.org/10.1080/11263504.2013.776650

    Article  Google Scholar 

  • Alami S, Lamin H, Bennis M, Bouhnik O, Lamrabet M, El Hachimi ML, Abdelmoumen H, Bedmar EJ, El Idrissi M M (2021) Characterization of Retama sphaerocarpa microsymbionts in Zaida lead mine tailings in the moroccan middle Atlas. Syst appl microbiol 44(3):126207

    Article  CAS  Google Scholar 

  • Al-Bakri AG, Afifi FU (2007) Evaluation of antimicrobial activity of selected plant extracts by rapid XTT colorimetry and bacterial enumeration. J Microbiol Meth 68:19–25

    Article  CAS  Google Scholar 

  • Al-Qudah AM, Al-Ghoul AM, Trawenh IB, Al-Jaber H, Al Shboul TM, Abu Zarga MH, Abuorabi ST (2014) Antioxidant activity and chemical composition of essential oils from jordanian Ononis natrix L. and Ononis sicula Guss. TBAP 4:52–61

    CAS  Google Scholar 

  • Al-Snafi AE (2020) The traditional uses, constituents and pharmacological effects of Ononis spinosa. IOSR J Pharm 10(2):53–59

    CAS  Google Scholar 

  • Altanlar N, Saltan Çitoğlu GB, Yilmaz S (2006) Antilisterial activity of some plants used in folk medicine. Pharm Biol 44:91–94

    Article  Google Scholar 

  • Andrews M, Andrews ME (2017) Specificity in legume-rhizobia symbioses. Int j mol sci 18(4):705

    Article  Google Scholar 

  • Azani N, Babineau M, Bailey CD, Banks H, Barbosa AR, Pinto RB et al (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: the Legume phylogeny Working Group (LPWG). Taxon 66(1):44–77

    Article  Google Scholar 

  • Bagaram BM, Mounir F, Lahssini S, Ponette Q (2016) Site suitability analysis for cork oak regeneration using GIS based multi-criteria evaluation techniques in Maamora forest-Morocco. OA Lib J 3(03):1

    Google Scholar 

  • Bakhoum N, Galiana A, Le Roux C, Kane A, Duponnois R, Ndoye F, Fall D, Noba K, Sylla S, Diouf D (2015) Phylogeny of nodulation genes and symbiotic diversity of Acacia senegal (L.) Willd. and A. seyal (Del.) Mesorhizobium strains from different regions of Senegal. Microb Ecol 69(3):641–651

  • Bennis M, Perez-Tapia V, Alami S, Bouhnik O, Lamin H, Abdelmoumen H, Bedmar EJ, El Idrissi MM (2022) Characterization of plant growth-promoting bacteria isolated from the rhizosphere of Robinia pseudoacacia growing in metal-contaminated mine tailings in eastern Morocco. J Environ Manage 304:114321

    Article  CAS  Google Scholar 

  • Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. Microbiol 84(1):188–198. https://doi.org/10.1099/00221287-84-1-188

    Article  CAS  Google Scholar 

  • Beukes CW, Boshoff FS, Phalane FL, Hassen AI, Le Roux MM, Stȩpkowski T, Venter SN, Steenkamp ET (2019) Both alpha and beta-rhizobia occupy the root nodules of Vachellia karroo in South Africa. Front microbiol 10:1195

    Article  Google Scholar 

  • Bouhnik O, Alami S, Lamin H, Lamrabet M, Bennis M, Ouajdi M, Bellaka M, Antari S, Abbas Y, Abdelmoumen H, Bedmar EJ, El Missbah M (2021) The Fodder Legume Chamaecytisus albidus establishes functional symbiosis with different Bradyrhizobial Symbiovars in Morocco. Microb Ecol 1–14. https://doi.org/10.1007/s00248-021-01888-4

  • Broughton WJ, Dilworth M (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125(4):1075–1080

    Article  CAS  Google Scholar 

  • Castellano-Hinojosa A, Bedmar EJ (2017) 14 methods for evaluating plant growth promoting rhizobacteria traits. Advances in PGPR research 255. https://doi.org/10.1079/9781786390325.0255

  • Chen W, Kuo TT (1993) A simple and rapid method for the preparation of Gram negative bacterial genomic DNA. Nucleic Acids Res 21(9):2260

    Article  CAS  Google Scholar 

  • De Bruijn 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 58:21802187

    Article  Google Scholar 

  • De Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E, Kuzmanović N, Young P (2019) Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst appl microbiol 69(7):1852–1863

    Article  Google Scholar 

  • De Meyer SE, Andrews M, James EK, Willems A (2019) Mesorhizobium carmichaelinearum sp. nov., isolated from Carmichaelineae spp. root nodules. Int J Syst Evol Microbiol 69:146–152

    Article  Google Scholar 

  • De Meyer SE, Van Hoorde K, Vekeman B, Braeckman T, Willems A (2011) Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol Biochem 43(12):2384–2396

    Article  Google Scholar 

  • Diouf F, Diouf D, Klonowska A, Le Quere A, Bakhoum N, Fall D, Neyra M, Hugues P, Diouf M, Ndoye I, Moulin L (2015) Genetic and genomic diversity studies of Acacia symbionts in Senegal reveal new species of Mesorhizobium with a putative geographical pattern. PLoS ONE 10(2):e0117667. https://doi.org/10.1371/journal.pone.0117667

    Article  CAS  Google Scholar 

  • Djedidi S, Yokoyama T, Ohkama-Ohtsu N, Risal CP, Abdelly C, Sekimoto H (2011) Stress tolerance and symbiotic and phylogenic features of root nodule bacteria associated with Medicago species in different bioclimatic regions of Tunisia. Microbes Environ 26:36–45

    Article  Google Scholar 

  • El Attar I, Taha K, El Bekkay B, El Khadir M, Alami IT, Aurag J (2019) Screening of stress-tolerant bacterial strains possessing interesting multi-plant growth promoting traits isolated from root nodules of Phaseolus vulgaris L. Biocat Agric Biotechnol 20:101225

    Article  Google Scholar 

  • El Boukhari EM, Brhadda N, Gmira N (2016) Contribution à l’étude de la régénération artificielle du chêne liège (Quercus suber L.) vis-à-vis du contenu minéral des feuilles et des paramètres physicochimiques des sols de la Maâmora (Maroc). Nat Technol 14:26–23

    Google Scholar 

  • Fall D, Diouf D, Ourarhi M, Faye A, Abdelmounen H, Neyra M, Sylla SN, Missbah El Idrissi M (2008) Phenotypic and genotypic characteristics of Acacia senegal (L.) Willd. Root-nodulating bacteria isolated from soils in the dryland part of Senegal. Let Appl Microbiol 47(2):85–97

    Article  CAS  Google Scholar 

  • Fennane M, Tattou MI (2008) Statistiques et commentaires sur l’inventaire actuel de la flore vasculaire du Maroc. Flora 1986:1989

  • Guerrouj K, Perez-Valera E, Chahboune R, Abdelmoumen H, Bedmar EJ, Missbah-El-Idrissi M (2013) Identification of the rhizobial symbiont of Astragalus gombiformis in Eastern Morocco as Mesorhizobium camelthorni. Ant Van Leeuwenhoek 104:187–198. https://doi.org/10.1007/s10482-013-9936

    Article  CAS  Google Scholar 

  • Gupta M, Kiran S, Gulati A, Singh B, Tewari R (2012) Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiol Res 167(6):358–363

    Article  CAS  Google Scholar 

  • Khbaya B, Neyra M, Normand P, Zerhari K, Filali-Maltouf A (1998) Genetic diversity and phylogeny of rhizobia that nodulate Acacia spp. in Morocco assessed by analysis of rRNA genes. Appl Environ Microbiol 64(12):4912–4917

    Article  CAS  Google Scholar 

  • Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiol 147(4):981–993

    Article  CAS  Google Scholar 

  • Lamin H, Alami S, Bouhnik O, Bennis M, Benkritly S, Abdelmoumen H, Bedmar EJ, Missbah-El Idrissi M (2021) Identification of the endosymbionts from Sulla spinosissima growing in a lead mine tailing in Eastern Morocco as Mesorhizobium camelthorni sv. Aridi. J Appl Microbiol 130(3):948–959

    Article  CAS  Google Scholar 

  • Lamin H, Alami S, Bouhnik O, ElFaik S, Abdelmoumen H, Bedmar EJ, Missbah-El Idrissi M (2019) Nodulation of Retama monosperma by Ensifer aridi in an abandonned lead mine soils in eastern morocco. Front Microbiol 10:1456. https://doi.org/10.3389/fmicb.2019.01456

    Article  Google Scholar 

  • Lamrabet M, ElFaik S, Laadraoui C, Bouhnik O, Lamin H, Alami S, Abdelmoumen H, Bedmar EJ, El Idrissi M M (2022) Phylogenetic and symbiotic diversity of Lupinus albus and L. angustifolius microsymbionts in the Maamora forest, Morocco. Syst Appl Microbiol 45(4):126338

    Article  CAS  Google Scholar 

  • Le Quéré A, Tak N, Gehlot HS, Lavire C, Meyer T, Chapulliot D, Rathi S, Sakrouhi I, Rocha M, Severac D, Filali Maltouf A, Munive JA (2017) Genomic characterization of Ensifer aridi, a proposed new species of nitrogen-fixing rhizobium recovered from asian, african and american deserts. BMC Genomics 18(1):1–24

    Article  Google Scholar 

  • Li Y, Liu G, Han K, Sun L, Gao K, Liu Wang E, Chen W (2022) Distribution and biodiversity of rhizobia nodulating Chamaecrista mimosoides in the Shandong peninsula of china. Syst appl Microbiol 45(1):126280

    Article  CAS  Google Scholar 

  • M’Hirit O, Maghnouj M (1997) Stratégie de conservation des ressources génétiques forestières au Maroc. In: Ressources phytogénétiques et développement durable (eds) A.Birouk et M.Rejdali. Actes Editions, Maroc pp 123–138

  • Mamedov N, Gardner Z, Craker LE (2005) Medicinal plants used in Russia and Central Asia for the treatment of selected skin conditions. J Herbs Spices Med Plants 11:191–222

  • Menéndez E, Pérez-Yépez J, Hernández M, Rodríguez-Pérez A, Velázquez E, León-Barrios M (2020) Plant Growth Promotion Abilities of phylogenetically diverse Mesorhizobium strains: Effect in the Root colonization and development of Tomato Seedlings. Microorganisms 8(3):412

    Article  Google Scholar 

  • Meyer JM, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Microbiol 107(2):319–328. https://doi.org/10.1099/00221287-107-2-319

    Article  CAS  Google Scholar 

  • Missbah El Idrissi M, Abdelmoumen H (2008) Carbohydrates as carbon sources in rhizobia under salt stress. Symbiosis 46:33–44

    Google Scholar 

  • Missbah El Idrissi M, Bouhnik O, ElFaik S, Alami S, Lamin H, Bedmar EJ, Abdelmoumen H (2021) Characterization of Bradyrhizobium spp. nodulating Lupinus cosentinii and L. luteus microsymbionts in Morocco. Front Agron 3:661295. https://doi.org/10.3389/fagro.2021.661295

    Article  Google Scholar 

  • Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63(3):383–400. https://doi.org/10.1111/j.1574-6941.2007.00424.x

    Article  CAS  Google Scholar 

  • Murphy JA, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5

    Article  CAS  Google Scholar 

  • Öz BE, İşcan GS, Akkol EK, Süntar İ, Keleş H, Acıkara ÖB (2017) Wound healing and anti-inflammatory activity of some Ononis taxons. Biomed Pharmacotherapy 91:1096–1105

    Article  Google Scholar 

  • Page RR, da Vinha SG, Agnew ADQ (1985) The reaction of some sand-dune plant species to experimentally imposed environmental change: a reductionist approach to stability. Ecology of coastal vegetation. Springer, Dordrecht, pp 105–114. https://doi.org/10.1007/BF00039815

    Chapter  Google Scholar 

  • Patil A, Kale A, Ajane G, Sheikh R, Patil S (2017) Plant growth-promoting Rhizobium: mechanisms and biotechnological prospective. In: Hansen A, Choudhary D, Agrawal P, Varma A (eds) Rhizobium Biology and Biotechnology. Soil Biology, vol 50. Springer, Cham, pp 105–134

    Chapter  Google Scholar 

  • Payne SM (1994) [25] detection, isolation, and characterization of siderophores. Methods Enzymol 235:329–344

    Article  CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiol 17:362–370

    CAS  Google Scholar 

  • Richardson AMM (1975) Food, feeding rates and assimilation in the land snail Cepaea nemoralis L. Oecologia 19(1):59–70

    Article  CAS  Google Scholar 

  • Rincón A, Arenal F, González I, Manrique E, Lucas MM, Pueyo JJ (2008) Diversity of rhizobial bacteria isolated from nodules of the gypsophyte Ononis tridentata L. growing in spanish soils. Microb Ecol 56(2):223–233

    Article  Google Scholar 

  • Rogel MA, Ormeno-Orrillo E, Martínez-Romero E (2011) Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 34(2):96–104

    Article  Google Scholar 

  • Rosenblueth M, Ormeño-Orrillo E, López-López A, Rogel MA, Reyes-Hernández BJ, Martínez-Romero JC, Reddy P, Martínez-Romero E (2018) Nitrogen fixation in cereals. Front Microbiol 9:1794

    Article  Google Scholar 

  • Saeed A (2003) Stereoselective synthesis of (3R)-3, 4‐Dihydro‐6, 8‐dimethoxy‐3‐undecyl‐1H‐[2] benzopyran‐1‐one and derivatives, metabolites from Ononis natrix. Helv chim acta 86(2):377–383

    Article  CAS  Google Scholar 

  • Salesa D, Baeza MJ, Pérez-Ferrándiz E, Santana VM (2022) Longer summer seasons after fire induce permanent drought legacy effects on Mediterranean plant communities dominated by obligate seeders. Sci Total Environ 822:153655

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Sprent JI, Ardley J, James EK (2017) Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol 215:40–56. https://doi.org/10.1111/nph.14474

    Article  CAS  Google Scholar 

  • Talib WH, Mahasneh AM (2010) Antimicrobial, cytotoxicity and phytochemical screening of jordanian plants used in traditional medicine. Molecules 15:1811–1824

    Article  CAS  Google Scholar 

  • Thakur M, Nanda V (2020) Composition and functionality of bee pollen: a review. Trends Food Sc Technol 98:82–106

    Article  CAS  Google Scholar 

  • Vargas LK, Volpiano CG, Lisboa BB, Giongo A, Beneduzi A, Passaglia LMP (2017) Potential of Rhizobia as Plant Growth-Promoting Rhizobacteria. In: Zaidi A et al (eds) Microbes for Legume Improvement. Springer, Cham, pp 153–174. https://doi.org/10.1007/978-3-319-59174-2_7

    Chapter  Google Scholar 

  • Vasconcelos M, Grusak M, Pinto E, Gomes A, Ferreira H, Balazs B, Centofanti T, Ntatsi G, Savvas D, Karkanis A, Williams M, Vandenberg A, Toma L, Shrestha S, Akaichi F, Barrios CO, Gruber S, James EK, Maluk M, Iannetta P (2020) The biology of legumes and their agronomic, economic, and social impact. The Plant Family Fabaceae. Springer, Singapore, pp 3–25

    Chapter  Google Scholar 

  • Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831

    Article  CAS  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of the root-nodule bacteria. Blackwell, London

    Google Scholar 

  • Wang ET, Tian CF, Chen WF, Young JPW, Chen WX (2019) Ecology and Evolution of Rhizobia. Springer, Singapore

    Book  Google Scholar 

  • Wdowiak-Wróbel S, Marek-Kozaczuk M, Kalita M, Karaś M, Wójcik M, Małek W (2017) Diversity and plant growth promoting properties of rhizobia isolated from root nodules of Ononis arvensis. Ant Van Leeuwenh 110(8):1087–1103

    Article  Google Scholar 

  • Willis JC (1973) A dictionary of the flowering plants and ferns. Cambridge University Press, London

    Google Scholar 

  • Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel JC, Gillis M, Dreyfus B, De Lajudie P (2004) Characterization of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Syst Appl Microbiol 27(3):380–395

    Article  Google Scholar 

  • Zerhari K, Aurag J, Khbaya B, Kharchaf D, Filali-Maltouf A (2000) Phenotypic characteristics of rhizobia isolate nodulating Acacia species in the arid and saharan regions of Morocco. Let Appl Microbiol 30(5):351–357

    Article  CAS  Google Scholar 

  • Zhang H, Yasmin F, Song BH (2019) Neglected treasures in the wild-legume wild relatives in food security and human health. Cur Opin Plant Biol 49:17–26

    Article  Google Scholar 

  • Zhu YJ, Lu JK, Chen YL, Wang SK, Sui XH, Kang LH (2015) Mesorhizobium acaciae sp. nov., isolated from root nodules of Acacia melanoxylon R. Br. Int J Syst Evol Microbiol 65(10):3558–3563. https://doi.org/10.1099/ijsem.0.000455

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by Hassan II Academy of Sciences and Technology, in Morocco. Grant P18-RT-1401 from Junta de Andalucía is also acknowledged. The authors want to thank all the persons who contributed to this work.

Author information

Authors and Affiliations

  1. Centre de Biotechnologies Végétale et Microbienne, Biodiversité et Environnement, Faculté des Sciences, Université Mohammed V de Rabat, 4, Avenue Ibn Battouta, Rabat, Morocco

    Chaima Laadraoui, Soufiane Alami, Mouad Lamrabet, Meryeme Bennis, Omar Bouhnik, Hanaa Abdelmoumen & Mustapha Missbah El Idrissi

  2. Laboratory of Legumes. Centre of Biotechnology, Technopol of Borj-Cédria, BP 901, 2050, Hammam-lif, Tunisia

    Bacem Mnasri

  3. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín-CSIC E-419, 18080, Granada, Spain

    Eulogio J Bedmar

Authors
  1. Chaima Laadraoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soufiane Alami
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mouad Lamrabet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meryeme Bennis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Omar Bouhnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bacem Mnasri
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hanaa Abdelmoumen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eulogio J Bedmar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mustapha Missbah El Idrissi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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

Corresponding author

Correspondence to Mustapha Missbah El Idrissi.

Ethics declarations

Competing Interests

The authors declare there are no competing financial interests in relation to the work described.

Additional information

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.

Supplementary Material 1

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

Laadraoui, C., Alami, S., Lamrabet, M. et al. Identification of the symbiovar maamori in Mesorhizobium isolated from nodules of Ononis repens in the Maamora forest (Morocco). Symbiosis 89, 95–106 (2023). https://doi.org/10.1007/s13199-022-00890-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-022-00890-9

Keywords

Search

Navigation