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Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia

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Abstract

Actinobacterial isolates randomly obtained on nitrogen-free BAP medium from surface sterilized root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia sampled from fields were reported. They were assigned on the basis of partial 16S rRNA sequences to Micromonospora, Nocardia and Streptomyces genera. The isolates have been screened for hydrolytic activities, indole acetic acid (IAA) and siderophores production, phosphate solubilization and antagonistic activities. Results suggest putative traits as plant growth promoting bacteria proprieties of the isolates that occur in unique association in root nodules of the three analysed actinorhizal host species.

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References

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • 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 19:451–457

    Article  CAS  Google Scholar 

  • Barbieri P, Zanelli T, Galli E, Zanetti G (1986) Wheat inoculation with Azospirillum brasilense Sp6 and some mutants altered nitrogen fixation and indole-3-acetic acid production. FEMS Microbiol Lett 36:87–90

    Article  CAS  Google Scholar 

  • Barea J-M, Pozo MJ, Azco´n R, Azco´n-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  CAS  PubMed  Google Scholar 

  • Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319

    CAS  PubMed  Google Scholar 

  • Berg RH, Liu L, Dawson JO, Savka MA, Farrand SK (1992) Induction of pseudoactinorhizae by the plant pathogen Agrobacterium rhizogenes. Plant Physiol 98:777–779

    Article  PubMed  Google Scholar 

  • Callaham D, Del Tredici P, Torrey JG (1978) Isolation and cultivation in vitro of the actinomycete causing root nodulation in Comptonia. Science 199:899–902

    Article  PubMed  Google Scholar 

  • Capellano A, Dequatre B, Valla G, Moiroud A (1987) Root-nodule formation by Penicillium sp. on Alnus glutinosa and Alnus incana. Plant Soil 104:45–51

    Article  Google Scholar 

  • Chernin L, Ismailov Z, Haran S, Chet I (1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ Microbiol 61:1720–1726

    CAS  PubMed  Google Scholar 

  • Diem HG, Dommergues YR (1983) The isolation of Frankia from nodules of Casuarina. Can J Bot 61:2822–2825

    Article  Google Scholar 

  • Diem HG, Gauthier D, Dommergues YR (1982) Extranodular growth of Frankia on Casuarina equisetifolia. FEMS Microbiol Lett 15:181–184

    Article  Google Scholar 

  • Errakhi R, Bouteau F, Lebrihi A, Barakate M (2007) Evidences of biological control capacities of Streptomyces spp. against Sclerotium rolfsii responsible for damping-off disease in sugar beet (Beta vulgaris L.). World J Microbiol Biotechnol 23:1503–1509

    Article  CAS  Google Scholar 

  • Felsentein J (1985) Confidence limits on phylogeny: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Friedlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a β-1, 3 glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221

    Article  Google Scholar 

  • Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268

    Article  CAS  Google Scholar 

  • Gordon AS, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  Google Scholar 

  • Gtari M, Brusetti L, Gharbi S, Diego M, Boudabous A, Daffonchio D (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 234:349–355

    Article  CAS  PubMed  Google Scholar 

  • Gtari M, Brusetti L, Hassen A, Mora D, Daffonchio D, Boudabous A (2007) Genetic diversity among Elaeagnus compatible Frankia strains and sympatric related nitrogen fixing actinobacteria revealed by nifH sequence analysis. Soil Biol Biochem 39:372–377

    Article  CAS  Google Scholar 

  • Hamdali H, Bouizgarne B, Hafidi M, Lebrihi A, Virolle MJ, Ouhdouch Y (2008) Screening for rock phosphate-solubilizing Actinomycetes from Moroccan phosphate mines. Appl Soil Ecol 38:12–19

    Article  Google Scholar 

  • Jack RW, Tagg JR, Ray B (1995) Bacteriocins of gram-positive bacteria. Microbiol Rev 59:171–200

    CAS  PubMed  Google Scholar 

  • Kannenberg EL, Brewin NJ (1994) Host-plant invasion by Rhizobium: the role of cell-surface components. Trends Microbiol 2:277–283

    Article  CAS  PubMed  Google Scholar 

  • Kuhad RC, Kothamasi DM, Tripathi KK, Singh A (2004) Diversity and functions of soils microflora in development of plants. In: Varma A, Abbot L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, New York, pp 71–98

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146

    Article  CAS  Google Scholar 

  • Martinez-Noel GMA, Madrid EA, Bottini R, Lamattina L (2001) Indole acetic acid attenuates disease severity in potato-Phytophthora infestans interaction and inhibits the pathogen growth in vitro. Plant Physiol Biochem 39:815–823

    Article  CAS  Google Scholar 

  • Matthijs S, Tehrani KA, Laus G, Jackson RW, Cooper RM, Cornelis P (2007) Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-Pythium activity. Environ Microbiol 9:425–434

    Article  CAS  PubMed  Google Scholar 

  • Nazaret S, Simonet P, Normand P, Bardin R (1989) Genetic diversity among Frankia isolated from Casuarina nodules. Plant Soil 118:241–247

    Article  CAS  Google Scholar 

  • Niner BM, Brandt JP, Villegas MC, Marshall CR, Hirsch AM, Valdes M (1996) Analysis of partial sequences of genes coding for 16S rRNA of actinomycetes isolated from Casuarina equisetifolia nodules in Mexico. Appl Environ Microbiol 62:3034–3036

    CAS  PubMed  Google Scholar 

  • Norovsuren ZH, Zenova GM, Mosina LV (2005) Actinomycetes in the rhizosphere of semidesert Soils of Mongolia. Euras Soil Sc 40:415–418

    Article  Google Scholar 

  • Ouzari H, Khsairi A, Raddadi N, Jaoua L, Hassen A, Zarrouk M, Daffonchio D, Boudabous A (2008) Diversity of auxin-producing bacteria associated to Pseudomonas savastanoi-induced olive knots. J Basic Microbiol 48:370–377

    Article  CAS  PubMed  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Saad H, Janse JD, Akkermans ADL (1998) Root nodules of Ceanothus caeruleus contain both the N2-fixing Frankia endophyte and a phylogenetically related Nod–/Fix–actinomycete. Can J Microbiol 44:140–148

    Article  CAS  Google Scholar 

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  PubMed  Google Scholar 

  • Saitou RR, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 44:406–425

    Google Scholar 

  • Sambrook J, Fritsh EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press

  • Sequerra J, Capellano A, Faure-Raynard M, Moiround A (1994) Root hair infection process and myconodule formation on Alnus incana by Penicillium nodositatum. Can J Bot 72:955–962

    Article  Google Scholar 

  • Solans M (2007) Discaria trinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250

    Article  PubMed  Google Scholar 

  • Solans M, Vobis G (2003) Actinomycetes saprophíticos asociados a la rizósfera de Discaria trinervis. Ecol Aust 13:97–107

    Google Scholar 

  • Taechowisan T, Peberdy JF, Lumyong S (2004) PCR cloning and heterologous expression of chitinase gene of endophytic Streptomyces aureofaciens CMUAc130. J Gen Appl Microbiol 50:177–182

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Trujillo ME, Kroppenstedt RE, Schumann P, Carro L, Martinez-Molina E (2006) Micromonospora coriariae sp. nov., isolated from root nodules of Coriaria myrtifolia. Int J Syst Evol Microbiol 56:2381–2385

    Article  CAS  PubMed  Google Scholar 

  • Trujillo ME, Kroppenstedt RE, Fernandez-Molinero C, Schumann P, Martinez-Molina E (2007) Micromonospora lupine sp.nov. and Micromonospora saelicesensis sp. nov., isolated from root nodules of Lupinus angustifolius. Int J Syst Evol Microbiol 57:2799–2804

    Article  CAS  PubMed  Google Scholar 

  • Valdés M, Cayetano A, Leyva MA, Camacho AD (2004) Promoción del crecimiento de Casuarina equisetifolia (L.) por diferentes microorganismos simbiontes. Terra 22:207–215

    Google Scholar 

  • Valdés M, Pérez NM, de los Santo PE, Mellado JC, Cabrielas JJP, Normand P, Hirsh M (2004) Non-Frankia Actinomycetes isolated from surface sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466

    Article  PubMed  Google Scholar 

  • Valdés D, Huss-Danell K, Lavire C, Normand P, Wall L (2006) Further characterization of new symbiotic nitrogen fixing non-Frankia actiomycetes isolated from nodules of Alnus acuminata. The 14th International Meeting on Frankia and Actinorhizal Plants. Department of Plant Physiology, UPSC, Umea University, Umea, Sweden

  • Van Rhijn P, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59:124–142

    PubMed  Google Scholar 

  • Wolters DJ, van Dijk C, Akkermans A, Woldendorp JW (1999) Ineffective Frankia and host resistance in natural populations of Alnus glutinosa (L.) Gaertn. Acta Oecol 20:71–79

    Article  Google Scholar 

  • Xiao K, Samac DA, Kinkel LL (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23:285–295

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Tunisian Minister of High Education, Scientific Research and Technology (LabMBA grants).

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Authors and Affiliations

  1. Laboratoire Microorganismes et Biomolécules Actives, Département de Biologie, Faculté des Sciences de Tunis, Campus Universitaire, 2092, Tunis, Tunisia

    Faten Ghodhbane-Gtari, Imene Essoussi, Mayssa Chattaoui, Atef Jaouani, Abdellatif Boudabous & Maher Gtari

  2. Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche, Università degli Studi, via Celoria 2, 20133, Milano, Italy

    Bessem Chouaia & Daniele Daffonchio

Authors
  1. Faten Ghodhbane-Gtari
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  2. Imene Essoussi
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  3. Mayssa Chattaoui
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  4. Bessem Chouaia
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  5. Atef Jaouani
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  6. Daniele Daffonchio
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  7. Abdellatif Boudabous
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  8. Maher Gtari
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Correspondence to Maher Gtari.

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Presented at the 15th International Frankia and Actinorhizal Plants Meeting, Bariloche, Argentina, October 19–23, 2008.

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Ghodhbane-Gtari, F., Essoussi, I., Chattaoui, M. et al. Isolation and characterization of non-Frankia actinobacteria from root nodules of Alnus glutinosa, Casuarina glauca and Elaeagnus angustifolia . Symbiosis 50, 51–57 (2010). https://doi.org/10.1007/s13199-009-0029-7

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