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Title: Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus

Abstract

Mycorrhiza helper bacteria (MHB) are known to increase host root colonization by mycorrhizal fungi but the molecular mechanisms and potential tripartite trophic interactions are poorly understood. Through an effort to study Populus microbiome, we isolated 21 Pseudomonas strains from native Populus deltoides roots. These bacterial isolates were characterized and screened for MHB effectiveness on the Populus-Laccaria system. Two other Pseudomonas strains (i.e., Pf-5 and BBc6R8) from existing collections were also included as reference in the screening process. We analyzed Laccaria bicolor S238N growth rate, mycelial architecture and transcriptional changes induced by the contrasting Pseudomonas strains (i.e., inhibitory, neutral and beneficial). We characterized 17 out of the 21 Pseudomonas strains from the Populus rhizosphere with positive effects on L. bicolor S238N growth, as well as on Populus root architecture and colonization by L. bicolor S238N across three Populus species. Four of seven reporter genes, Tra1, Tectonin2, Gcn5 and Cipc1, thought to be specific to the interaction with strain BBc6R8, were induced or repressed while interacting with six (i.e., GM17, GM33, GM41, GM48, Pf-5 and BBc6R8) of the tested Pseudomonas strains. GM41 promoted the highest roots colonization across three Populus species but most notably in P. deltoides, which is otherwise, poorly colonizedmore » by L. bicolor. Here we report novel MHB strains isolated from native Populus that improve roots colonization. This tripartite relationship could be exploited in nursery production for target Populus species/genotypes as a means of improving establishment and survival in marginal lands.« less

Authors:
 [1];  [1];  [1];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Div.
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1185358
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal Issue: 579; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Mycorrhiza helper bacteria; mycorrhizal fungi; Laccaria bicolor; mutualistic interactions; fungal-bacterial-Populus interactions; Populus rhizosphere; Soil Microbiology

Citation Formats

Labbe, Jessy L., Weston, David J., Dunkirk, Nora, Pelletier, Dale A., and Tuskan, Gerald A. Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. United States: N. p., 2014. Web. doi:10.3389/fpls.2014.00579.
Labbe, Jessy L., Weston, David J., Dunkirk, Nora, Pelletier, Dale A., & Tuskan, Gerald A. Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. United States. https://doi.org/10.3389/fpls.2014.00579
Labbe, Jessy L., Weston, David J., Dunkirk, Nora, Pelletier, Dale A., and Tuskan, Gerald A. Fri . "Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus". United States. https://doi.org/10.3389/fpls.2014.00579. https://www.osti.gov/servlets/purl/1185358.
@article{osti_1185358,
title = {Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus},
author = {Labbe, Jessy L. and Weston, David J. and Dunkirk, Nora and Pelletier, Dale A. and Tuskan, Gerald A.},
abstractNote = {Mycorrhiza helper bacteria (MHB) are known to increase host root colonization by mycorrhizal fungi but the molecular mechanisms and potential tripartite trophic interactions are poorly understood. Through an effort to study Populus microbiome, we isolated 21 Pseudomonas strains from native Populus deltoides roots. These bacterial isolates were characterized and screened for MHB effectiveness on the Populus-Laccaria system. Two other Pseudomonas strains (i.e., Pf-5 and BBc6R8) from existing collections were also included as reference in the screening process. We analyzed Laccaria bicolor S238N growth rate, mycelial architecture and transcriptional changes induced by the contrasting Pseudomonas strains (i.e., inhibitory, neutral and beneficial). We characterized 17 out of the 21 Pseudomonas strains from the Populus rhizosphere with positive effects on L. bicolor S238N growth, as well as on Populus root architecture and colonization by L. bicolor S238N across three Populus species. Four of seven reporter genes, Tra1, Tectonin2, Gcn5 and Cipc1, thought to be specific to the interaction with strain BBc6R8, were induced or repressed while interacting with six (i.e., GM17, GM33, GM41, GM48, Pf-5 and BBc6R8) of the tested Pseudomonas strains. GM41 promoted the highest roots colonization across three Populus species but most notably in P. deltoides, which is otherwise, poorly colonized by L. bicolor. Here we report novel MHB strains isolated from native Populus that improve roots colonization. This tripartite relationship could be exploited in nursery production for target Populus species/genotypes as a means of improving establishment and survival in marginal lands.},
doi = {10.3389/fpls.2014.00579},
journal = {Frontiers in Plant Science},
number = 579,
volume = 5,
place = {United States},
year = {Fri Oct 24 00:00:00 EDT 2014},
month = {Fri Oct 24 00:00:00 EDT 2014}
}

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Works referenced in this record:

Interactions between mycorrhizal fungi and other soil organisms
journal, February 1994


The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types
journal, July 2011

  • Gottel, Neil R.; Castro, Hector F.; Kerley, Marilyn
  • Applied and Environmental Microbiology, Vol. 77, Issue 17
  • DOI: 10.1128/AEM.05255-11

Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5
journal, June 2005

  • Paulsen, Ian T.; Press, Caroline M.; Ravel, Jacques
  • Nature Biotechnology, Vol. 23, Issue 7
  • DOI: 10.1038/nbt1110

Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation
journal, February 2004

  • Wu, J.; Zhang, N.; Hayes, A.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
  • DOI: 10.1073/pnas.0308321100

Symbiotic fungal associations in ‘lower’ land plants
journal, June 2000

  • Read, D. J.; Duckett, J. G.; Francis, R.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1398
  • DOI: 10.1098/rstb.2000.0617

Symbiotic sequencing for the Populus mesocosm
journal, February 2004


Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries
journal, October 1999

  • Frey-Klett, Pascale; Churin, Jean-Louis; Pierrat, Jean-Claude
  • Soil Biology and Biochemistry, Vol. 31, Issue 11
  • DOI: 10.1016/S0038-0717(99)00079-6

16S ribosomal DNA amplification for phylogenetic study.
journal, January 1991


Genome Sequence of the Plant Growth Promoting Endophytic Bacterium Enterobacter sp. 638
journal, May 2010


Populus : A Model System for Plant Biology
journal, June 2007


Micropropagation of Populus trichocarpa ‘Nisqually-1’: the genotype deriving the Populus reference genome
journal, September 2009

  • Kang, Byung-guk; Osburn, Lori; Kopsell, Dean
  • Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 99, Issue 3
  • DOI: 10.1007/s11240-009-9596-9

Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family
journal, March 2004


Pseudomonas fluorescens Induces Strain-Dependent and Strain-Independent Host Plant Responses in Defense Networks, Primary Metabolism, Photosynthesis, and Fitness
journal, June 2012

  • Weston, David J.; Pelletier, Dale A.; Morrell-Falvey, Jennifer L.
  • Molecular Plant-Microbe Interactions, Vol. 25, Issue 6
  • DOI: 10.1094/MPMI-09-11-0253

The mycorrhiza helper bacteria revisited
journal, October 2007


Atomic Force Microscope Controlled Topographical Imaging and Proximal Probe Thermal Desorption/Ionization Mass Spectrometry Imaging
journal, December 2013

  • Ovchinnikova, Olga S.; Kjoller, Kevin; Hurst, Gregory B.
  • Analytical Chemistry, Vol. 86, Issue 2
  • DOI: 10.1021/ac4026576

Bacteria Helping Mycorrhiza Development
book, January 2006


The possible role of trehalose in the mycorrhiza helper bacterium effect
journal, June 2006

  • Duponnois, Robin; Kisa, Marija
  • Canadian Journal of Botany, Vol. 84, Issue 6
  • DOI: 10.1139/b06-053

Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

Cloning and Characterization of Physarum polycephalum Tectonins : HOMOLOGUES OF LIMULUS LECTIN L-6
journal, March 1998

  • Huh, Chang-Goo; Aldrich, Joan; Mottahedeh, Jack
  • Journal of Biological Chemistry, Vol. 273, Issue 11
  • DOI: 10.1074/jbc.273.11.6565

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture
journal, April 2004


Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor : Is fungal auxin the trigger?
journal, July 2010

  • Felten, Judith; Legué, Valérie; Anicet Ditengou, Franck
  • Plant Signaling & Behavior, Vol. 5, Issue 7
  • DOI: 10.4161/psb.5.7.11896

Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads
journal, October 2004


Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238
journal, November 1996


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Twenty-One Genome Sequences from Pseudomonas Species and 19 Genome Sequences from Diverse Bacteria Isolated from the Rhizosphere and Endosphere of Populus deltoides
journal, October 2012

  • Brown, S. D.; Utturkar, S. M.; Klingeman, D. M.
  • Journal of Bacteriology, Vol. 194, Issue 21
  • DOI: 10.1128/JB.01243-12

Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro
journal, September 2001


The enhancement of plant growth by free-living bacteria
journal, February 1995

  • Glick, Bernard R.
  • Canadian Journal of Microbiology, Vol. 41, Issue 2
  • DOI: 10.1139/m95-015

Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: The characterisation of isolates with potential to enhance phytoremediation
journal, November 2006

  • Moore, Fiona Porteous; Barac, Tanja; Borremans, Brigitte
  • Systematic and Applied Microbiology, Vol. 29, Issue 7
  • DOI: 10.1016/j.syapm.2005.11.012

Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013


Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria
journal, July 2005


Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant
journal, October 2008


Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth
journal, January 2006


Characterisation of bacteria from Pinus sylvestris–Suillus luteus mycorrhizas and their effects on root–fungus interactions and plant growth
journal, March 2002


Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management: A U.S. case study
journal, April 2001

  • Tuskan, Gerald A.; Walsh, Marie E.
  • The Forestry Chronicle, Vol. 77, Issue 2
  • DOI: 10.5558/tfc77259-2

Emerging Model Systems in Plant Biology: Poplar (Populus) as A Model Forest Tree
journal, September 2000

  • Bradshaw, H. D.; Ceulemans, Reinhart; Davis, John
  • Journal of Plant Growth Regulation, Vol. 19, Issue 3
  • DOI: 10.1007/s003440000030

Suppression of plant defence response by a mycorrhiza helper bacterium
journal, June 2007


Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

Emerging Model Systems in Plant Biology: Poplar (Populus) as A Model Forest Tree
journal, September 2000

  • Bradshaw, H. D.; Ceulemans, Reinhart; Davis, John
  • Journal of Plant Growth Regulation, Vol. 19, Issue 3
  • DOI: 10.1007/s003440000030

Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013


Micropropagation of Populus trichocarpa ‘Nisqually-1’: the genotype deriving the Populus reference genome
journal, September 2009

  • Kang, Byung-guk; Osburn, Lori; Kopsell, Dean
  • Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 99, Issue 3
  • DOI: 10.1007/s11240-009-9596-9

Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture
journal, April 2004


Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: The characterisation of isolates with potential to enhance phytoremediation
journal, November 2006

  • Moore, Fiona Porteous; Barac, Tanja; Borremans, Brigitte
  • Systematic and Applied Microbiology, Vol. 29, Issue 7
  • DOI: 10.1016/j.syapm.2005.11.012

Atomic Force Microscope Controlled Topographical Imaging and Proximal Probe Thermal Desorption/Ionization Mass Spectrometry Imaging
journal, December 2013

  • Ovchinnikova, Olga S.; Kjoller, Kevin; Hurst, Gregory B.
  • Analytical Chemistry, Vol. 86, Issue 2
  • DOI: 10.1021/ac4026576

The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5
journal, June 2005

  • Paulsen, Ian T.; Press, Caroline M.; Ravel, Jacques
  • Nature Biotechnology, Vol. 23, Issue 7
  • DOI: 10.1038/nbt1110

Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro
journal, September 2001


Global analysis of nutrient control of gene expression in Saccharomyces cerevisiae during growth and starvation
journal, February 2004

  • Wu, J.; Zhang, N.; Hayes, A.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
  • DOI: 10.1073/pnas.0308321100

The Genomic Sequence of Pseudomonas fluorescens Pf-5: Insights Into Biological Control
journal, February 2007

  • Loper, Joyce E.; Kobayashi, Donald Y.; Paulsen, Ian T.
  • Phytopathology, Vol. 97, Issue 2
  • DOI: 10.1094/phyto-97-2-0233

Symbiotic fungal associations in ‘lower’ land plants
journal, June 2000

  • Read, D. J.; Duckett, J. G.; Francis, R.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1398
  • DOI: 10.1098/rstb.2000.0617

Symbiotic sequencing for the Populus mesocosm
journal, February 2004


Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads
journal, October 2004


The mycorrhiza helper bacteria revisited
journal, October 2007


Characterisation of bacteria from Pinus sylvestris–Suillus luteus mycorrhizas and their effects on root–fungus interactions and plant growth
journal, March 2002


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Location and Survival of Mycorrhiza Helper Pseudomonas fluorescens during Establishment of Ectomycorrhizal Symbiosis between Laccaria bicolor and Douglas Fir.
journal, January 1997


Impact on Arbuscular Mycorrhiza Formation ofPseudomonas Strains Used as Inoculants for Biocontrol of Soil-Borne Fungal Plant Pathogens
journal, June 1998


Isolation from the Sorghum bicolorMycorrhizosphere of a Bacterium Compatible with Arbuscular Mycorrhiza Development and Antagonistic towards Soilborne Fungal Pathogens
journal, November 1999


16S ribosomal DNA amplification for phylogenetic study.
journal, January 1991


The possible role of trehalose in the mycorrhiza helper bacterium effect
journal, June 2006

  • Duponnois, Robin; Kisa, Marija
  • Canadian Journal of Botany, Vol. 84, Issue 6
  • DOI: 10.1139/b06-053

The enhancement of plant growth by free-living bacteria
journal, February 1995

  • Glick, Bernard R.
  • Canadian Journal of Microbiology, Vol. 41, Issue 2
  • DOI: 10.1139/m95-015

Populus : A Model System for Plant Biology
journal, June 2007


Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress
journal, October 2021


Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management: A U.S. case study
journal, April 2001

  • Tuskan, Gerald A.; Walsh, Marie E.
  • The Forestry Chronicle, Vol. 77, Issue 2
  • DOI: 10.5558/tfc77259-2

Works referencing / citing this record:

Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms
journal, September 2016

  • Werner, Stephanie; Polle, Andrea; Brinkmann, Nicole
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 20
  • DOI: 10.1007/s00253-016-7792-1

Pseudomonas fluorescens increases mycorrhization and modulates expression of antifungal defense response genes in roots of aspen seedlings
journal, January 2019


Dynamics of Aspen Roots Colonization by Pseudomonads Reveals Strain-Specific and Mycorrhizal-Specific Patterns of Biofilm Formation
journal, May 2018

  • Noirot-Gros, Marie-Francoise; Shinde, Shalaka; Larsen, Peter E.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.00853

The Influence of Microfungi on the Mycelial Growth of Ectomycorrhizal Fungus Tricholoma matsutake
journal, June 2019


Root bacterial endophytes alter plant phenotype, but not physiology
journal, January 2016

  • Henning, Jeremiah A.; Weston, David J.; Pelletier, Dale A.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2606

Microbial interactions within the plant holobiont
journal, March 2018


Increasing access to microfluidics for studying fungi and other branched biological structures
journal, June 2019

  • Millet, Larry J.; Aufrecht, Jayde; Labbé, Jessy
  • Fungal Biology and Biotechnology, Vol. 6, Issue 1
  • DOI: 10.1186/s40694-019-0071-z

Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange
journal, October 2019

  • Uehling, Jessie K.; Entler, Matthew R.; Meredith, Hannah R.
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.02163

Root bacterial endophytes alter plant phenotype, but not physiology
journal, January 2016

  • Henning, Jeremiah A.; Weston, David J.; Pelletier, Dale A.
  • PeerJ, Vol. 4
  • DOI: 10.7717/peerj.2606