Skip to main content

Advertisement

SpringerLink
Log in

Symbiotic efficiency of Bradyrhizobium symbiovars on Chamaecytisus albidus plants grown under water stress and acidic pH

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

In this work, we analyzed the effect of water stress and acid pH on the growth of the endemic fodder legume Chamaecytisus albidus, inoculated with four strains of Bradyrhizobium, from three different symbiovars previously isolated from the plant grown in different eco-geographical areas of Morocco. We also assessed the competitiveness of the three symbiovars for plant nodulation under water stress and acidity. We analyzed the strain’s nodulation ability, rates of nodules occupancy, shoot, and root dry weights of plants grown at -100, -80, and − 60 MPa water potential, and 6.0 and 7.0 pH values. The strains CM64 and CJ2 belong to the symbiovar genistearum and strains CA20 and CB10 to the symbiovars retamae and lupini, respectively. The strains CB10 and CJ2 were the most infective regardless of the pH and water potential at which the plants were grown. The strain CB10 was also the most abundant in nodules from plants grown at any conditions examined. Reductions in the water potential altered the nodulation ability, the strains CB10 and CJ2 still being the more infective. These strains were also the most infective at pH 6.0 and 7.0. The highest values of shoot and root dry weights were recorded in plants inoculated with strain CA20 under all the irrigation regimes used. The reduction from 100% to 80 and 60% field capacity decreased the shoot dry weight of the plants by 31.23 and 67.06%, respectively. Moreover, there was a 37.95 and 61.74% decrease in plant root dry weight when grown at 80 and 60% of field capacity, respectively. Despite variations in the efficiency of each strain, overall, the pH did not affect either the SDW or the RDW of the plants. The inoculation of C. albidus with a mix of the four strains did not result in further improvement of nodulation or symbiotic efficiency. These results show that water deficiency drastically affects the growth of C. albidus and that the retamae symbiovar was the most effective under the conditions examined. This is the first report on the competitiveness of symbiovars for the nodulation of a legume under stress.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andrews M, De Meyer S, James EK et al (2018) Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes (Basel) 9:321

    Article  PubMed  Google Scholar 

  • Bakhoum N, Ndoye F, Kane A et al (2012) Impact of rhizobial inoculation on Acacia senegal (L.) Willd. Growth in greenhouse and soil functioning in relation to seed provenance and soil origin. World J Microbiol Biotechnol 28:2567–2579

    Article  PubMed  Google Scholar 

  • 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 

  • Benlaribi M, Monneveux P, Grignac P (1990) Étude Des caractères D’enracinement et de leur rôle dans l’adaptation Au déficit hydrique chez le blé dur (Triticum durum Desf). Agronomie 10:305–322

    Article  Google Scholar 

  • Bhatia NP, Adholeya A, Sharma A (1998) Biomass production and changes in soil productivity during longterm cultivation of Prosopis juliflora (Swartz) DC inoculated with VA Mycorrhiza and Rhizobium spp. in a semi-arid wasteland. Biol Fertil Soils 26:208–214. https://doi.org/10.1007/s003740050369

    Article  CAS  Google Scholar 

  • Bhatla SC, Lal MA (2018) Plant physiology, development and metabolism. Springer

  • Boivin S, Ait Lahmidi N, Sherlock D et al (2020) Host-specific competitiveness to form nodules in Rhizobium leguminosarum symbiovar viciae. New Phytol 226:555–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouhnik O, Alami S, Lamin H et al (2021a) The Fodder Legume Chamaecytisus albidus establishes functional symbiosis with different Bradyrhizobial Symbiovars in Morocco. Microb Ecol. https://doi.org/10.1007/s00248-021-01888-4

    Article  PubMed  Google Scholar 

  • Bouhnik O, Lamin H, Alami S et al (2021b) The endemic Chamaecytisus albidus is nodulated by symbiovar genistearum of Bradyrhizobium in the Moroccan Maamora Forest. Syst Appl Microbiol 126197. https://doi.org/10.1016/j.syapm.2021.126197

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

  • 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 

  • Chouhan B, Tak N, Bissa G et al (2022) Evolution of novel strains of Ensifer nodulating the invasive legume Leucaena leucocephala (Lam.) De Wit in different climatic regions of India through lateral gene transfer. FEMS Microbiol Ecol 98:fiac086

    Article  PubMed  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 58:2180–2187. https://doi.org/http://aem.asm.org/cgi/reprint/58/7/2180

    Article  PubMed  PubMed Central  Google Scholar 

  • dos Santos JGD, Aguiar A, das CF, Junior EMS et al (2011) Soil management and efficiency of rhizobia strains of cowpea Vigna unguiculata (L.) Walp. In the tropics. Chil J Agric Res 71:594

    Article  Google Scholar 

  • Egamberdieva D, Wirth S, Jabborova D, Räsänen LA, Liao H (2017) Coordination between Bradyrhizobium and Pseudomonas alleviates salt stress in soybean through altering root system architecture. J Plant Int 12(1):100–107. https://doi.org/10.1080/17429145.2017.1294212

    Article  CAS  Google Scholar 

  • Fennan M, Ibn Tattou M, Ouyahya A, Jalal E (2007) Flore Pratique Du Maroc: Manuel De détermination Des plantes vasculaires. Rabat, Ins

    Google Scholar 

  • Herrera MA, Salamanca CP, Barea J (1993) Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified Mediterranean ecosystems. Appl Environ Microbiol 59:129–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hungria M, Stacey G (1997) Molecular signals exchanged between host plants and rhizobia: basic aspects and potential application in agriculture. Soil Biol Biochem 29:819–830

    Article  CAS  Google Scholar 

  • Hurd EA (1968) Growth of roots of seven varieties of Spring Wheat at High and low moisture levels 1. Agron J 60:201–205

    Article  Google Scholar 

  • Karmakar K, Rana A, Rajwar A et al (2015) Legume-rhizobia symbiosis under stress. Plant microbes symbiosis: applied facets. Springer, pp 241–258

  • Khaldoun A, Chery J, Monneveux P (1990) Study of rooting characteristics and their role in adaptation to water deficit in barley (Hordeum vulgare L). Agronomie 10:369–379

    Article  Google Scholar 

  • Kunert KJ, Vorster BJ, Fenta BA et al (2016) Drought stress responses in soybean roots and nodules. Front Plant Sci 7:1–7. https://doi.org/10.3389/fpls.2016.01015

    Article  Google Scholar 

  • Laguerre G, Louvrier P, Allard M-R, Amarger N (2003) Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Appl Environ Microbiol 69:2276–2283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavorel S, Canadell J, Rambal S, Terradas J (1998) Mediterranean terrestrial ecosystems: research priorities on global change effects. Glob Ecol Biogeogr Lett 7:157–166

    Article  Google Scholar 

  • Lynch J, van Beem JJ (1993) Growth and architecture of seedling roots of common bean genotypes. Crop Sci 33:1253–1257

    Article  Google Scholar 

  • Marinković J, Bjelić D, Đorđević V et al (2019) Performance of different Bradyrhizobium strains in root nodule symbiosis under drought stress. Acta Physiol Plant 41:1–13

    Article  Google Scholar 

  • Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169:609–615. https://doi.org/10.1016/j.micres.2013.10.001

    Article  CAS  PubMed  Google Scholar 

  • McKenzie RH, Middleton AB, Solberg ED et al (2001) Response of pea to rhizobia inoculation and starter nitrogen in Alberta. Can J Plant Sci 81:637–643

    Article  Google Scholar 

  • Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51(5):914–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miransari M, Balakrishnan P, Smith D et al (2006) Overcoming the stressful effect of low pH on soybean root hair curling using lipochitooligosacharides. Commun Soil Sci Plant Anal 37:1103–1110

    Article  CAS  Google Scholar 

  • Morón B, Soria-Díaz ME, Ault J et al (2005) Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem Biol 12:1029–1040

    Article  PubMed  Google Scholar 

  • Mrabet R, Badraoui M, Moussadek R, Soudi B (2017) Challenges of soil organic carbon sequestration in drylands. In: Proceedings of the Global Symposium on Soil Organic Carbon 2017, Rome, Italy, 21–23 March, 2017. Food and Agriculture Organization of the United Nations (FAO), pp 501–505

  • 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). Forêt méditerranéenne

  • Ogaya R, Peñuelas J (2021) Climate change effects in a mediterranean forest following 21 consecutive years of experimental drought. Forests 12. https://doi.org/10.3390/f12030306

  • Park C-E, Jeong S-J, Joshi M et al (2018) Keeping global warming within 1.5 C constrains emergence of aridification. Nat Clim Chang 8:70–74

    Article  Google Scholar 

  • Peñuelas J, Sardans J, Filella I et al (2017) Impacts of global change on Mediterranean forests and their services. Forests 8:1–37. https://doi.org/10.3390/f8120463

    Article  Google Scholar 

  • Pierret A, Moran CJ (2011) Plant roots and soil structure. In: Gliński J, Horabik J, Lipiec J (eds) Encyclopedia of Agrophysics. Springer Netherlands, Dordrecht, pp 628–632

    Chapter  Google Scholar 

  • Prudent M, Salon C, Souleimanov A et al (2015) Soybean is less impacted by water stress using Bradyrhizobium japonicum and thuricin-17 from Bacillus thuringiensis. Agron Sustain Dev 35:749–757. https://doi.org/10.1007/s13593-014-0256-z

    Article  CAS  Google Scholar 

  • Ramos MLG, Gordon AJ, Minchin FR et al (1999) Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean (Phaseolus vulgaris L). Ann Bot 83:57–63

    Article  CAS  Google Scholar 

  • Ramos MLG, Parsons R, Sprent JI, James EK (2003) Effect of water stress on nitrogen fixation and nodule structure of common bean. Pesqui Agropecuária Bras 38:339–347

    Article  Google Scholar 

  • Rathi S, Tak N, Bissa G et al (2018) Selection of Bradyrhizobium or Ensifer symbionts by the native Indian caesalpinioid legume Chamaecrista pumila depends on soil pH and other edaphic and climatic factors. FEMS Microbiol Ecol 94:fiy180

    Article  CAS  Google Scholar 

  • 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 

  • Samarah N H (2005). Effects of drought stress on growth and yield of barley. Agronomy for sustainable development, 25(1), 145–149.

  • Seleiman MF, Al-Suhaibani N, Ali N et al (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10:259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Stern DI, Kaufmann RK (2014) Anthropogenic and natural causes of climate change. Clim Change 122:257–269

    Article  Google Scholar 

  • Wang ET, Tian CF, Chen WF et al (2019) Ecology and evolution of rhizobia. Springer

  • Wardell GE, Hynes MF, Young PJ, Harrison E (2022) Why are rhizobial symbiosis genes mobile? Philos Trans R Soc B 377:20200471

    Article  CAS  Google Scholar 

  • Xing P, Zhao Y, Guan D, Li L, Zhao B, Ma M, Jiang X, Tian C, Cao F, Li J (2022) Effects of Bradyrhizobium co-inoculated with Bacillus and Paenibacillus on the structure and functional genes of soybean Rhizobacteria Community. Genes 13:1922. https://doi.org/10.3390/genes13111922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yosef G, Walko R, Avisar R et al (2018) Large-scale semi-arid afforestation can enhance precipitation and carbon sequestration potential. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-19265-6

    Article  CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zerhari K, Aurag J, Khbaya B et al (2000) Phenotypic characteristics of rhizobia isolates nodulating Acacia species in the arid and saharan regions of Morocco. Lett Appl Microbiol 30:351–357

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors want to thank all the persons who contributed to the achievement of this work. Support was obtained from Hassan II Academy of Sciences and Technology, in Morocco (AH2ST). Dr Bouhnik obtained a grant from the Hassan II Academy of Sciences and Technology.

Author information

Authors and Affiliations

  1. Centre de Biotechnologies végétales et microbiennes, Biodiversité et Environnement, Faculty of Sciences, Mohammed V University in Rabat, 4 Avenue Ibn Battouta, Agdal, Rabat, Morocco

    Omar Bouhnik, Zohra Chaddad, Soufiane Alami, Mouad Lamrabet, Meryeme Bennis, Hanane Lamin, Hanaa Abdelmoumen & Mustapha Missbah El Idrissi

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

    Bacem Mnasri

  3. Department of Soil Microbiology and Symbiotic Systems, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas (CSIC), Granada, E-419, Spain

    Eulogio J. Bedmar

Authors
  1. Omar Bouhnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zohra Chaddad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Soufiane Alami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mouad Lamrabet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Meryeme Bennis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hanane Lamin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bacem Mnasri
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hanaa Abdelmoumen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Eulogio J. Bedmar
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mustapha Missbah El Idrissi
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

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

Bouhnik, O., Chaddad, Z., Alami, S. et al. Symbiotic efficiency of Bradyrhizobium symbiovars on Chamaecytisus albidus plants grown under water stress and acidic pH. Symbiosis (2024). https://doi.org/10.1007/s13199-024-00989-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13199-024-00989-1

Keywords

Search

Navigation