Skip to main content

Advertisement

SpringerLink
Log in

Promoting the growth of Sulla flexuosa L. by endophytic root nodule bacteria authors and affiliations

  • Research
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Legume plants rely upon multipartite interactions between rhizobia and bacterial endophytes within root nodules to facilitate plant growth. This study aimed to isolate and identify indigenous endophytic bacteria from root nodules of Sulla aculeolata L. in Northeast Morocco. Based on their tri-calcium phosphate (TCP) solubilization capacity, five endophytes were chosen for further evaluation of their plant growth traits. All isolates were hydrogen cyanide (HCN) and siderophore producers, while only BCH24 tested positive for ACC deaminase activity. Indole-3-acetic acid (IAA) synthesis ranged from 1.27 mgL− 1 to 2.89 mgL− 1, while soluble phosphate concentrations was between 7.99 mg L− 1 and 110.58 mg L− 1. Additionally, all the endophytes were able to produce more than two lytic enzymes. Based on the analysis of 16 S rRNA gene sequences five isolates were identified as Enterobacter sp (BCH13, BCH2), Pseudomonas sp (BCH16, BCH24), and Serratia sp (BCH10). The strains inhibited the growth of three phytopathogenic fungi, with BCH13 exhibiting the highest rate against Aspergillus ochraceus (45%), followed by BCH24 against Fusarium oxysporum (40%) and Botrytis cinerea (35%), respectively. In vivo inoculation of halotolerant strains Enterobacter hormaechei (BCH13) and Pseudomonas moraviensis (BCH16) under gnotobiotic conditions revealed that co-inoculation with Rhizobium sullae KS6 improved plant development compared to single inoculation, making it a promising eco-friendly bio-inoculant for legume Sulla flexuosa L. production.

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

Data Availability

All data generated or analyzed during this study are included in this published article.

References

  • Aeron A, Dubey RC, Maheshwari DK (2020) Characterization of a plant-growth-promoting non-nodulating endophytic bacterium (Stenotrophomonas maltophilia) from the root nodules of Mucuna utilis var. capitata L. (Safed Kaunch). Can J Microbiol 66(11):670–677. https://doi.org/10.1139/cjm-2020-0196

    Article  CAS  PubMed  Google Scholar 

  • Afzal I, Shinwari ZK, Sikandar S, Shahzad S (2019) Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res 221:36–49. https://doi.org/10.1016/j.micres.2019.02.001

    Article  CAS  PubMed  Google Scholar 

  • Ali B, Hafeez A, Javed MA, Afridi MS, Abbasi HA, Qayyum A, Batool T, Ullah A, Marc RA, Jaouni SKA, Alkhalifah DHM, Selim S (2022) Role of endophytic bacteria in salinity stress amelioration by physiological and molecular mechanisms of defense: a comprehensive review. South Afr J Bot 151:33–46. https://doi.org/10.1016/j.sajb.2022.09.036

    Article  CAS  Google Scholar 

  • Almeida F, Rodrigues ML, Coelho C (2019) The still underestimated Problem of Fungal Diseases Worldwide. Front Microbiol 10:214. https://doi.org/10.3389/fmicb.2019.00214

    Article  PubMed  PubMed Central  Google Scholar 

  • Álvarez-Aragón R, Palacios JM, Ramírez-Parra E (2023) Rhizobial symbiosis promotes drought tolerance in Vicia sativa and Pisum sativum. Environ Exp Bot 208:105268. https://doi.org/10.1016/j.envexpbot.2023.105268

    Article  CAS  Google Scholar 

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods in Enzymology. Academic Press, pp 115–118

  • Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas SPP-mediated plant growth-stimulation. Soil Biol Biochem 19(4):451–457. https://doi.org/10.1016/0038-0717(87)90037-X

    Article  CAS  Google Scholar 

  • Benjelloun I, Thami Alami I, El Khadir M, Douira A, Udupa SM (2021) Co-Inoculation of Mesorhizobium ciceri with either Bacillus sp. or Enterobacter aerogenes on Chickpea improves Growth and Productivity in phosphate-deficient soils in dry areas of a Mediterranean Region. Plants 10(3):571. https://doi.org/10.3390/plants10030571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolívar-Anillo HJ, Garrido C, Collado IG (2020) Endophytic microorganisms for biocontrol of the phytopathogenic fungus Botrytis cinerea. Phytochem Rev 19(3):721–740. https://doi.org/10.1007/s11101-019-09603-5

    Article  CAS  Google Scholar 

  • Brígido C, Menéndez E, Paço A, Glick BR, Belo A, Félix MR, Oliveira S, Carvalho M (2019) Mediterranean native leguminous plants: a Reservoir of endophytic Bacteria with potential to Enhance Chickpea growth under stress conditions. Microorganisms 7(10):392. https://doi.org/10.3390/microorganisms7100392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoso P, Alves A, Silveira P, Sá C, Fidalgo C, Freitas R, Figueira E (2018) Bacteria from nodules of wild legume species: phylogenetic diversity, plant growth promotion abilities and osmotolerance. Sci Total Environ 645:1094–1102. https://doi.org/10.1016/j.scitotenv.2018.06.399

    Article  CAS  PubMed  Google Scholar 

  • Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for Plant growth–promoting Rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63(6):1670–1680. https://doi.org/10.2136/sssaj1999.6361670x

    Article  CAS  Google Scholar 

  • Chaiharn M, Chunhaleuchanon S, Kozo A, Lumyong S (2008) Screening of Rhizobacteria for their plant growth promoting activities. Curr Appl Sci Technol 8(1)

  • Cheng Z, Meng L, Yin T, Li Y, Zhang Y, Li S (2023) Changes in Soil Rhizobia Diversity and their Effects on the Symbiotic efficiency of soybean intercropped with maize. Agronomy 13(4):997. https://doi.org/10.3390/agronomy13040997

    Article  CAS  Google Scholar 

  • Chiboub M, Saadani O, Fatnassi IC, Abdelkrim S, Abid G, Jebara M, Jebara SH (2016) Characterization of efficient plant-growth-promoting bacteria isolated from Sulla coronaria resistant to cadmium and to other heavy metals. C R Biol 339(9):391–398. https://doi.org/10.1016/j.crvi.2016.04.015

    Article  PubMed  Google Scholar 

  • De vasconcelos martins ferreira, De carvalho L, Fonseca colombo andrade F J, Padua oliveira D, Vasconcelos de medeiros FH, De souza moreira FM (2020) co-inoculation of selected nodule endophytic rhizobacterial strains with Rhizobium tropici promotes plant growth and controls damping off in common bean. Pedosphere 30(1):98–108. https://doi.org/10.1016/S1002-0160(19)60825-8

  • del Barrio-Duque A, Ley J, Samad A, Antonielli L, Sessitsch A, Compant S (2019) Beneficial endophytic Bacteria-serendipita indica Interaction for Crop Enhancement and Resistance to Phytopathogens. Front Microbiol 10:2888. https://doi.org/10.3389/fmicb.2019.02888

    Article  PubMed  PubMed Central  Google Scholar 

  • del Orozco-Mosqueda C, Glick BR, Santoyo G (2020) ACC deaminase in plant growth-promoting bacteria (PGPB): An efficient mechanism to counter salt stress in crops. Microbiol Res 235:126439. https://doi.org/10.1016/j.micres.2020.126439

  • Dimkić I, Ćopić M, Petrović M, Stupar M, Savković Ž, Knežević A, Subakov Simić G, Ljaljević Grbić M, Unković N (2023) Bacteriobiota of the Cave Church of Sts. Peter and Paul in Serbia—Culturable and Non-Culturable Communities’ Assessment in the Bioconservation potential of a Peculiar Fresco painting. Int J Mol Sci 24(2):1016. https://doi.org/10.3390/ijms24021016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egamberdieva D, Wirth SJ, Shurigin VV, Hashem A, Abd_Allah EF (2017) Endophytic Bacteria improve Plant Growth, Symbiotic Performance of Chickpea (Cicer arietinum L.) and induce suppression of Root Rot caused by Fusarium solani under salt stress. Front Microbiol 8

  • El Aaraj C, Bakkali M, Infantino A, Arakrak A, Laglaoui A (2015) Mycotoxigenic Fungi in Cereals grains and coffee from the North of Morocco. Am J Res Commun

  • Elnahal ASM, El-Saadony MT, Saad AM, Desoky E-SM, El-Tahan AM, Rady MM, AbuQamar SF, El-Tarabily KA (2022) The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: a review. Eur J Plant Pathol 162(4):759–792. https://doi.org/10.1007/s10658-021-02393-7

    Article  Google Scholar 

  • Elyemlahi A, Arakrak A, Laglaoui A, Ayadi M, Bakkali M (2019) Nutritional evaluation of Sulla (Hedysarum flexuosum L.) ecotypes grown in Northwest region of Morocco. Moroc J Biol 16(2019):19–29

    Google Scholar 

  • Elyemlahi A, Omar B, Mohammed B, Amine L, Abdelhay A, Idrissi MME (2022) Nodulation of Sulla flexuosa ecotypes by Rhizobium sullae symbiovar sullae (sv. Nov) in Northern Morocco. In Review

  • Enquahone S, van Marle G, Simachew A (2022) Plant growth-promoting characteristics of halotolerant endophytic bacteria isolated from Sporobolus specatus (Vahr) Kunth and Cyperus laevigatus L. of ethiopian rift valley lakes. Arch Microbiol 204(7):403. https://doi.org/10.1007/s00203-022-03021-6

    Article  CAS  PubMed  Google Scholar 

  • Etesami H, Beattie GA (2017) Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics and Plant Health. Springer, Singapore, pp 163–200

    Chapter  Google Scholar 

  • Ferchichi N, Toukabri W, Boularess M, Smaoui A, Mhamdi R, Trabelsi D (2019) Isolation, identification and plant growth promotion ability of endophytic bacteria associated with lupine root nodule grown in tunisian soil. Arch Microbiol 201(10):1333–1349. https://doi.org/10.1007/s00203-019-01702-3

    Article  CAS  PubMed  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26(1):192–195. https://doi.org/10.1104/pp.26.1.192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groom A (2010) IUCN Red list of threatened species: Hedysarum flexuosum. IUCN Red List Threat Species

  • Guerrouj K, Pérez-Valera E, Chahboune R, Abdelmoumen H, Bedmar EJ, El Idrissi MM (2013) Identification of the rhizobial symbiont of Astragalus glombiformis in Eastern Morocco as Mesorhizobium camelthorni. Antonie Van Leeuwenhoek 104(2):187–198. https://doi.org/10.1007/s10482-013-9936-y

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Samant K, Sahu A (2012) Isolation of cellulose-degrading bacteria and determination of their cellulolytic potential. Int J Microbiol 2012:578925. https://doi.org/10.1155/2012/578925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hnini M, Taha K, Aurag J (2022) Molecular identification and characterization of phytobeneficial osmotolerant endophytic bacteria inhabiting root nodules of the Saharan tree Vachellia tortilis subsp. raddiana. Arch Microbiol 205(1):45. https://doi.org/10.1007/s00203-022-03358-y

    Article  CAS  PubMed  Google Scholar 

  • Iličić R, Pivic R, Dinić Z, Dragana L, Vlajić S, Josic D (2017) The enhancement of soybean growth and yield in a field trial through introduction of mixtures of Bradyrhizobium japonicum, Bacillus sp. and Pseudomonas chlororaphis. Not Sci Biol 9:274. https://doi.org/10.15835/nsb9210081

    Article  CAS  Google Scholar 

  • Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 40(12):1019–1025. https://doi.org/10.1139/m94-162

    Article  CAS  Google Scholar 

  • Kammoun R, Naili B, Bejar S (2008) Application of a statistical design to the optimization of parameters and culture medium for alpha-amylase production by aspergillus oryzae CBS 819.72 grown on gruel (wheat grinding by-product). Bioresour Technol 99(13):5602–5609. https://doi.org/10.1016/j.biortech.2007.10.045

    Article  CAS  PubMed  Google Scholar 

  • Kang S-M, Shahzad R, Bilal S, Khan AL, Park Y-G, Lee K-E, Asaf S, Khan MA, Lee I-J (2019) Indole-3-acetic-acid and ACC deaminase producing Leclercia adecarboxylata MO1 improves Solanum lycopersicum L. growth and salinity stress tolerance by endogenous secondary metabolites regulation. BMC Microbiol 19(1):80. https://doi.org/10.1186/s12866-019-1450-6

  • Knežević M, Berić T, Buntić A, Delić D, Nikolić I, Stanković S, Stajković-Srbinović O (2021) Potential of root nodule nonrhizobial endophytic bacteria for growth promotion of Lotus corniculatus L. and Dactylis glomerata L. J Appl Microbiol 131(6):2929–2940. https://doi.org/10.1111/jam.15152

    Article  CAS  PubMed  Google Scholar 

  • Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, El Hamss H, Belabess Z, Barka EA (2022) Biological Control of Plant Pathogens: A Global Perspective. Microorganisms 10(3):596. https://doi.org/10.3390/microorganisms10030596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucero CT, Lorda GS, Anzuay MS, Ludueña LM, Taurian T (2021) Peanut endophytic phosphate solubilizing Bacteria increase growth and P content of soybean and maize plants. Curr Microbiol 78(5):1961–1972. https://doi.org/10.1007/s00284-021-02469-x

    Article  CAS  PubMed  Google Scholar 

  • Maheshwari DK, Kumar S, Kumar B, Pandey P (2010) Co-inoculation of Urea and DAP Tolerant Sinorhizobium meliloti and Pseudomonas aeruginosa as Integrated Approach for Growth Enhancement of Brassica juncea. Indian J Microbiol 50(4):425–431. https://doi.org/10.1007/s12088-011-0085-6

    Article  CAS  PubMed  Google Scholar 

  • Martínez Alcántara V, Medina R, Gauna JM, Balatti PA, Martínez Alcántara V, Medina R, Gauna JM, Balatti PA (2020) Bacterial endophytes diversity of tree legumes from Argentina. Agrociencia Urug 24(SPE2). https://doi.org/10.31285/agro.24.411

  • Muluneh MG (2021) Impact of climate change on biodiversity and food security: a global perspective—a review article. Agric Food Secur 10(1):36. https://doi.org/10.1186/s40066-021-00318-5

    Article  Google Scholar 

  • Naveed M, Aziz MZ, Yaseen M (2017) Perspectives of using endophytic microbes for Legume Improvement. In: Zaidi A, Khan MS, Musarrat J (eds) Microbes for Legume Improvement. Springer International Publishing, Cham, pp 277–299

    Chapter  Google Scholar 

  • Nichols P, Norton M (2016) Improvement of pasture and forage legumes and grasses for Mediterranean climate zones. Options Méditerranéennes 114:157–168

    Google Scholar 

  • Pal R, Gokarn K (2010) Siderophores and pathogenecity of microorganisms. J Biosci Technologie, pp 127–134

  • Pikovskaya RI (1948) Mobilization of Phosphorus in Soil connection with the vital activity of some Microbial Species. Microbiology 17

  • Raja S, Sugitha T, Sivakumar U (2019) Non-rhizobial nodule Associated Bacteria (NAB) from Blackgram (Vigna mungo L.) and their possible role in plant growth promotion. Madras Agric J 106:7–9. https://doi.org/10.29321/MAJ.2019.000291

    Article  Google Scholar 

  • Rawat P, Das S, Shankhdhar D, Shankhdhar SC (2021) Phosphate-solubilizing microorganisms: mechanism and their role in phosphate solubilization and uptake. J Soil Sci Plant Nutr 21(1):49–68. https://doi.org/10.1007/s42729-020-00342-7

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56. https://doi.org/10.1016/0003-2697(87)90612-9

    Article  CAS  PubMed  Google Scholar 

  • Sepúlveda-Caamaño M, Gerding M, Vargas M, Moya-Elizondo E, Oyarzúa P, Campos J (2018) Lentil (Lens culinaris L.) growth promoting rhizobacteria and their effect on nodulation in coinoculation with rhizobia. Arch Agron Soil Sci 64(2):244–256. https://doi.org/10.1080/03650340.2017.1342034

    Article  CAS  Google Scholar 

  • Sharma A, Kaushik N, Sharma A, Bajaj A, Rasane M, Shouche YS, Marzouk T, Djébali N (2021) Screening of Tomato seed bacterial endophytes for antifungal activity reveals lipopeptide producing Bacillus siamensis strain NKIT9 as a potential Bio-Control Agent. Front Microbiol 12

  • Shrivastava M, Srivastava PC, D’Souza SF (2018) Phosphate-solubilizing microbes: diversity and phosphates solubilization mechanism. In: Meena VS (ed) Role of Rhizospheric Microbes in Soil: volume 2: Nutrient Management and Crop Improvement. Springer, Singapore, pp 137–165

    Chapter  Google Scholar 

  • Singh B, Boukhris I, Pragya, Kumar V, Yadav AN, Farhat-khemakhem A, Kumar A, Singh D, Blibech M, Chouayekh H, Alghamdi OA (2020) Contribution of microbial phytases to the improvement of plant growth and nutrition: a review. Pedosphere 30(3):295–313. https://doi.org/10.1016/S1002-0160(20)60010-8

    Article  CAS  Google Scholar 

  • Thami Alami I, El Mzouri E (2000) Etude de l’efficacité et de la persistance des souches de sulla. Sulas Ed Legum Mediterr forage crops Pastures Altern uses (Cahiers Options Méditerranéennes; n. 45):321–325

  • Thaware DS, Kohire OD, Gholve VM (2016) In vitro efficacy of fungal and bacterial antagonists against Fusarium oxysporum f. sp. ciceri causing chickpea wilt. Int J Agric Sci 12(2):215–218. https://doi.org/10.15740/HAS/IJAS/12.2/215-218

    Article  Google Scholar 

  • Tiru M, Muleta D, Berecha G, Adugna G (2013) Antagonistic Effects of Rhizobacteria against Coffee Wilt Disease caused by Gibberella xylarioides. Asian J Plant Pathol 7(3):109–122. https://doi.org/10.3923/ajppaj.2013.109.122

    Article  Google Scholar 

  • Tsai S-H, Liu C-P, Yang S-S (2007) Microbial conversion of food wastes for biofertilizer production with thermophilic lipolytic microbes. Renew Energy 32(6):904–915. https://doi.org/10.1016/j.renene.2006.04.019

    Article  CAS  Google Scholar 

  • Tsitsigiannis D, Dimakopoulou M, Antoniou P, Tjamos E (2012) Biological control strategies of mycotoxigenic fungi and associated mycotoxins in Mediterranean basin crops. Phytopathol Mediterr 51(1):158–174. https://doi.org/10.14601/Phytopathol_Mediterr-9497

    Article  CAS  Google Scholar 

  • Tufail MA, Bejarano A, Shakoor A, Naeem A, Arif MS, Dar AA, Farooq TH, Pertot I, Puopolo G (2021) Can bacterial endophytes be used as a Promising Bio-Inoculant for the mitigation of salinity stress in crop plants?—A global Meta-analysis of the last decade (2011–2020). Microorganisms 9(9):1861. https://doi.org/10.3390/microorganisms9091861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. IBP Handbk 15 Oxford and Edinburgh: Blackwell Scientific Publications, p pp.164

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703. https://doi.org/10.1128/jb.173.2.697-703.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zirmi-Zembri N (2021) Caractérisation d’Hedysarum flexuosum pour son utilisation en alimentation animale. Thesis, Universite Mouloud MAMMERI Tizi-Ouzou

Download references

Acknowledgements

The authors would like to thank all the persons who contributed to the achievement of this work.

Funding

No funding was received to assist with the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Biotechnology and Biomolecular Engineering Research Team, FSTT, Abdelmalek Essaâdi University, Tetouan, Morocco

    Samia Hamane, Anass El yemlahi, Mounir Hassani Zerrouk, Ouiam El Galiou, Amin Laglaoui, Mohammed Bakkali & Abdelhay Arakrak

  2. Tetouan, Morocco

    Samia Hamane

Authors
  1. Samia Hamane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anass El yemlahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mounir Hassani Zerrouk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ouiam El Galiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amin Laglaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohammed Bakkali
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abdelhay Arakrak
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Samia HAMANE, Anas EL YEMLAHI and Ouiam EL GALIOU. The first draft of the manuscript was written by Samia HAMANE and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Abdelhay Arakrak.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Competing interests

The authors declare that they have no conflicting interests.

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

Hamane, S., El yemlahi, A., Hassani Zerrouk, M. et al. Promoting the growth of Sulla flexuosa L. by endophytic root nodule bacteria authors and affiliations. World J Microbiol Biotechnol 39, 253 (2023). https://doi.org/10.1007/s11274-023-03699-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-023-03699-w

Keywords

Search

Navigation