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The plant-growth-promoting actinobacteria of the genus Nocardia induces root nodule formation in Casuarina glauca

  • Faten Ghodhbane-Gtari
  • Imen Nouioui
  • Karima Hezbri
  • Emily Lundstedt
  • Timothy D’Angelo
  • Zakkary McNutt
  • Laurent Laplaze
  • Hassen Gherbi
  • Virginie Vaissayre
  • Sergio Svistoonoff
  • Hela ben Ahmed
  • Abdelatif Boudabous
  • Louis S. Tisa
Original Paper

Abstract

Actinorhizal plants form a symbiotic association with the nitrogen-fixing actinobacteria Frankia. These plants have important economic and ecological benefits including land reclamation, soil stabilization, and reforestation. Recently, many non-Frankia actinobacteria have been isolated from actinorhizal root nodules suggesting that they might contribute to nodulation. Two Nocardia strains, BMG51109 and BMG111209, were isolated from Casuarina glauca nodules, and they induced root nodule-like structures in original host plant promoting seedling growth. The formed root nodule-like structures lacked a nodular root at the apex, were not capable of reducing nitrogen and had their cortical cells occupied with rod-shaped Nocardiae cells. Both Nocardia strains induced root hair deformation on the host plant. BMG111209 strain induced the expression of the ProCgNin:Gus gene, a plant gene involved in the early steps of the infection process and nodulation development. Nocardia strain BMG51109 produced three types of auxins (Indole-3-acetic acid [IAA], Indole-3-Byturic Acid [IBA] and Phenyl Acetic Acid [PAA]), while Nocardia BMG111209 only produced IAA. Analysis of the Nocardia genomes identified several important predicted biosynthetic gene clusters for plant phytohormones, secondary metabolites, and novel natural products. Co-infection studies showed that Nocardia strain BMG51109 plays a role as a “helper bacteria” promoting an earlier onset of nodulation. This study raises many questions on the ecological significance and functionality of Nocardia bacteria in actinorhizal symbioses.

Keywords

Non-Frankia actinobacteria Nocardia Plant infectivity Auxins Actinorhizal symbiosis Plant-growth-promotion 

Notes

Acknowledgements

This work was supported in part by CMCU (Comité Mixte Tuniso-Français pour la Coopération inter-Universitaire no 09G0916 to MG and LL) and the Agence Nationale de la Recherche (Grant ANR-08-JCJC-0070-01 to LL). FG-G was supported in part by the Visiting Scientist and Postdoctoral Scientist Program administered by the NH AES at the University of New Hampshire. This work was also supported by the USDA National Institute of Food and Agriculture Hatch 022821 (LST), Agriculture and Food Research Initiative Grant 2015-67014-22849 from the USDA National Institute of Food and Agriculture (LST), and the College of Life Science and Agriculture at the University of New Hampshire-Durham. A Summer Undergraduate Research Fellowship (SURF) from the University of New Hampshire-Durham supported EL. Partial funding was provided by the New Hampshire Agricultural Experiment Station. This is Scientific Contribution Number 2786.

Authors Contribution

FGG, LL, AB and LST conceived the study. FGG, IN, EL, TD, ZM, HK, VV, and HG performed the research. EL, TD, IN, FGG, and LST analysed the data. FGG, and LST wrote the manuscript. All the authors approved the paper.

Compliance with ethical standards

Conflict of interest

The authors have declared that they have no competing interest exists.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Faten Ghodhbane-Gtari
    • 1
  • Imen Nouioui
    • 1
  • Karima Hezbri
    • 1
  • Emily Lundstedt
    • 2
  • Timothy D’Angelo
    • 2
  • Zakkary McNutt
    • 2
  • Laurent Laplaze
    • 3
    • 4
    • 5
  • Hassen Gherbi
    • 3
  • Virginie Vaissayre
    • 6
  • Sergio Svistoonoff
    • 3
    • 4
    • 5
  • Hela ben Ahmed
    • 7
  • Abdelatif Boudabous
    • 1
  • Louis S. Tisa
    • 2
  1. 1.Laboratoire Microorganismes et Biomolécules ActivesUniversité Tunis El Manar (FST) & Université Carthage (INSAT)TunisTunisia
  2. 2.Department of Molecular, Cellular, and Biomedical SciencesUniversity of New HampshireDurhamUSA
  3. 3.LSTM, UMR 040 IRD/INRA/CIRAD/ Université Montpellier/Supagro, TA A-82/J, Campus International de BaillarguetMontpellierFrance
  4. 4.LCM, IRD/ISRA/UCAD, Centre de Recherche de Bel AirDakarSenegal
  5. 5.LMI LAPSE, Centre de Recherche de Bel AirDakarSenegal
  6. 6.ECOBIOFrench National Research Institute for Sustainable Development (IRD)MontpellierFrance
  7. 7.Unité d’Ecophysiologie et Nutrition des plantes, Département de Biologie, Faculté des Sciences de TunisTunisTunisia

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