skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity

Abstract

Root microbiota is a crucial determinant of plant productivity and stress tolerance. Here, we hypothesize that the superior halo-tolerance of seepweed Suaeda salsa is tightly linked to a specialized belowground microbiome. To test this hypothesis, we performed a phylogenetic trait-based framework analysis based on bacterial 16S rRNA gene and fungal nuclear rRNA internal transcribed spacer profiling. Data showed that the dominant α-proteobacteria and γ-proteobacteria communities in bulk soil and root endosphere tend to be phylogenetically clustered and at the same time exhibit phylogenetic over-dispersion in rhizosphere. Likewise, the dominant fungal genera occurred at high phylogenetic redundancy. Interestingly, we found the genomes of rhizospheric and endophytic bacteria associated with S. salsa to be enriched in genes contributing to salt stress acclimatization, nutrient solubilization and competitive root colonization. A wide diversity of rhizobacteria with similarity to known halotolerant taxa further supported this interpretation. These findings suggest that an ecological patterned root-microbial interaction strategy has been adopted in S. salsa system to confront soil salinity. We also demonstrated that the potential core microbiome members improve non-host plants growth and salt tolerance. As a result, this work provides a platform to improve plant fitness with halophytes-microbial associates and novel insights into the functions ofmore » plant microbiome under salinity.« less

Authors:
 [1];  [2];  [3];  [4];  [1];  [5];  [6];  [3];  [6]
  1. Chinese Academy of Forestry, Hangzhou (People's Republic of China)
  2. Institute of Chemical Engineering, Vienna (Austria)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Adaptive Symbiotic Technologies, Seattle, WA (United States)
  5. Adaptive Symbiotic Technologies, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States)
  6. Zhejiang Univ. (People's Republic of China)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1325488
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal Issue: 10; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Yuan, Zhilin, Druzhinina, Irina S., Labbé, Jessy, Redman, Regina, Qin, Yuan, Rodriguez, Russell, Zhang, Chulong, Tuskan, Gerald A., and Lin, Fucheng. Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. United States: N. p., 2016. Web. doi:10.1038/srep32467.
Yuan, Zhilin, Druzhinina, Irina S., Labbé, Jessy, Redman, Regina, Qin, Yuan, Rodriguez, Russell, Zhang, Chulong, Tuskan, Gerald A., & Lin, Fucheng. Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. United States. doi:10.1038/srep32467.
Yuan, Zhilin, Druzhinina, Irina S., Labbé, Jessy, Redman, Regina, Qin, Yuan, Rodriguez, Russell, Zhang, Chulong, Tuskan, Gerald A., and Lin, Fucheng. Tue . "Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity". United States. doi:10.1038/srep32467. https://www.osti.gov/servlets/purl/1325488.
@article{osti_1325488,
title = {Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity},
author = {Yuan, Zhilin and Druzhinina, Irina S. and Labbé, Jessy and Redman, Regina and Qin, Yuan and Rodriguez, Russell and Zhang, Chulong and Tuskan, Gerald A. and Lin, Fucheng},
abstractNote = {Root microbiota is a crucial determinant of plant productivity and stress tolerance. Here, we hypothesize that the superior halo-tolerance of seepweed Suaeda salsa is tightly linked to a specialized belowground microbiome. To test this hypothesis, we performed a phylogenetic trait-based framework analysis based on bacterial 16S rRNA gene and fungal nuclear rRNA internal transcribed spacer profiling. Data showed that the dominant α-proteobacteria and γ-proteobacteria communities in bulk soil and root endosphere tend to be phylogenetically clustered and at the same time exhibit phylogenetic over-dispersion in rhizosphere. Likewise, the dominant fungal genera occurred at high phylogenetic redundancy. Interestingly, we found the genomes of rhizospheric and endophytic bacteria associated with S. salsa to be enriched in genes contributing to salt stress acclimatization, nutrient solubilization and competitive root colonization. A wide diversity of rhizobacteria with similarity to known halotolerant taxa further supported this interpretation. These findings suggest that an ecological patterned root-microbial interaction strategy has been adopted in S. salsa system to confront soil salinity. We also demonstrated that the potential core microbiome members improve non-host plants growth and salt tolerance. As a result, this work provides a platform to improve plant fitness with halophytes-microbial associates and novel insights into the functions of plant microbiome under salinity.},
doi = {10.1038/srep32467},
journal = {Scientific Reports},
issn = {2045-2322},
number = 10,
volume = 6,
place = {United States},
year = {2016},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance
journal, June 2014


Thermotolerance Generated by Plant/Fungal Symbiosis
journal, November 2002


Stress tolerance in plants via habitat-adapted symbiosis
journal, February 2008

  • Rodriguez, Rusty J.; Henson, Joan; Van Volkenburgh, Elizabeth
  • The ISME Journal, Vol. 2, Issue 4
  • DOI: 10.1038/ismej.2007.106

Enhancing Native Grass Productivity by Cocultivating With Endophyte-Laden Calli
journal, January 2008

  • Lucero, M. E.; Barrow, J. R.; Osuna, P.
  • Rangeland Ecology & Management, Vol. 61, Issue 1
  • DOI: 10.2111/06-144R3.1

Microbially Mediated Plant Functional Traits
journal, December 2011


Culturing a plant microbiome community at the cross‐Rhodes
journal, August 2012


Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013


The importance of the microbiome of the plant holobiont
journal, February 2015

  • Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13312

Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior
journal, January 2013

  • Badri, Dayakar V.; Zolla, Gaston; Bakker, Matthew G.
  • New Phytologist, Vol. 198, Issue 1
  • DOI: 10.1111/nph.12124

Rapid responses of soil microorganisms improve plant fitness in novel environments
journal, August 2012

  • Lau, J. A.; Lennon, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
  • DOI: 10.1073/pnas.1202319109

Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait: Root bacteria protect plants from drought
journal, March 2014

  • Rolli, Eleonora; Marasco, Ramona; Vigani, Gianpiero
  • Environmental Microbiology, Vol. 17, Issue 2
  • DOI: 10.1111/1462-2920.12439

Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative
journal, April 2014

  • Wagner, Maggie R.; Lundberg, Derek S.; Coleman-Derr, Devin
  • Ecology Letters, Vol. 17, Issue 6
  • DOI: 10.1111/ele.12276

Endophyte Microbiome Diversity in Micropropagated Atriplex canescens and Atriplex torreyi var griffithsii
journal, March 2011


A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming
journal, October 2012


Rhizosphere Microbes as Essential Partners for Plant Stress Tolerance
journal, March 2013

  • de Zelicourt, Axel; Al-Yousif, Mohamed; Hirt, Heribert
  • Molecular Plant, Vol. 6, Issue 2
  • DOI: 10.1093/mp/sst028

Properties of the halophyte microbiome and their implications for plant salt tolerance
journal, January 2013

  • Ruppel, Silke; Franken, Philipp; Witzel, Katja
  • Functional Plant Biology, Vol. 40, Issue 9
  • DOI: 10.1071/FP12355

Fungal Assemblages Associated with Roots of Halophytic and Non-halophytic Plant Species Vary Differentially Along a Salinity Gradient
journal, May 2012

  • Maciá-Vicente, Jose G.; Ferraro, Valeria; Burruano, Santella
  • Microbial Ecology, Vol. 64, Issue 3
  • DOI: 10.1007/s00248-012-0066-2

Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments
journal, June 2016

  • Mora-Ruiz, Merit del R.; Font-Verdera, Francisca; Orfila, Alejandro
  • FEMS Microbiology Ecology, Vol. 92, Issue 9
  • DOI: 10.1093/femsec/fiw145

Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L.
journal, January 2016


Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013

  • Peiffer, J. A.; Spor, A.; Koren, O.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
  • DOI: 10.1073/pnas.1302837110

Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015

  • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1414592112

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

Towards a holistic understanding of the beneficial interactions across the Populus microbiome
journal, November 2014

  • Hacquard, Stéphane; Schadt, Christopher W.
  • New Phytologist, Vol. 205, Issue 4
  • DOI: 10.1111/nph.13133

Microbial genome-enabled insights into plant–microorganism interactions
journal, September 2014

  • Guttman, David S.; McHardy, Alice C.; Schulze-Lefert, Paul
  • Nature Reviews Genetics, Vol. 15, Issue 12
  • DOI: 10.1038/nrg3748

Root surface as a frontier for plant microbiome research: Fig. 1.
journal, February 2015

  • van der Heijden, Marcel G. A.; Schlaeppi, Klaus
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1500709112

PHYMYCO-DB: A Curated Database for Analyses of Fungal Diversity and Evolution
journal, September 2012


Phylogenetic Clustering of Soil Microbial Communities by 16S rRNA but Not 16S rRNA Genes
journal, January 2012

  • DeAngelis, Kristen M.; Firestone, Mary K.
  • Applied and Environmental Microbiology, Vol. 78, Issue 7
  • DOI: 10.1128/AEM.07547-11

Contrasting Patterns of Community Assembly in the Stratified Water Column of Great Salt Lake, Utah
journal, January 2013


Phylogenetic Clustering and Overdispersion in Bacterial Communities
journal, July 2006


Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups
journal, June 2012

  • Placella, S. A.; Brodie, E. L.; Firestone, M. K.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1204306109

Beyond the Venn diagram: the hunt for a core microbiome: The hunt for a core microbiome
journal, October 2011


High-Throughput Sequencing: A Roadmap Toward Community Ecology
journal, March 2013

  • Poisot, Timothée; Péquin, Bérangère; Gravel, Dominique
  • Ecology and Evolution, Vol. 3, Issue 4
  • DOI: 10.1002/ece3.508

A Two-Component System Plays an Important Role in the Root-Colonizing Ability of Pseudomonas fluorescens Strain WCS365
journal, January 1998

  • Dekkers, Linda C.; Bloemendaal, Cees Jan P.; de Weger, Letty A.
  • Molecular Plant-Microbe Interactions, Vol. 11, Issue 1
  • DOI: 10.1094/MPMI.1998.11.1.45

A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365
journal, June 1998

  • Dekkers, L. C.; Phoelich, C. C.; van der Fits, L.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.7051

Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems
journal, June 2008

  • Davidson, A. L.; Dassa, E.; Orelle, C.
  • Microbiology and Molecular Biology Reviews, Vol. 72, Issue 2
  • DOI: 10.1128/MMBR.00031-07

Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related Proteobacteria
journal, September 2014

  • Bruto, Maxime; Prigent-Combaret, Claire; Muller, Daniel
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep06261

Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response
journal, November 2014


Characterization of NADH Dehydrogenases of Pseudomonas fluorescens WCS365 and Their Role in Competitive Root Colonization
journal, July 2002

  • Camacho Carvajal, Margarita M.; Wijfjes, André H. M.; Mulders, Ine H. M.
  • Molecular Plant-Microbe Interactions, Vol. 15, Issue 7
  • DOI: 10.1094/MPMI.2002.15.7.662

Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia
journal, June 2015

  • Cleary, Daniel F. R.; de Voogd, Nicole J.; Polónia, Ana R. M.
  • Microbial Ecology, Vol. 70, Issue 4
  • DOI: 10.1007/s00248-015-0632-5

Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection
journal, June 2007


Inoculants of plant growth-promoting bacteria for use in agriculture
journal, July 1998


Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem
journal, July 2014

  • Lakshmanan, V.; Selvaraj, G.; Bais, H. P.
  • PLANT PHYSIOLOGY, Vol. 166, Issue 2
  • DOI: 10.1104/pp.114.245811

The potential for give and take in plant–microbiome relationships
journal, June 2014


A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota
journal, April 2014


Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping
journal, August 2015

  • Santhanam, Rakesh; Luu, Van Thi; Weinhold, Arne
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 36
  • DOI: 10.1073/pnas.1505765112

Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities: Synthetic microbial ecosystems
journal, December 2013

  • De Roy, Karen; Marzorati, Massimo; Van den Abbeele, Pieter
  • Environmental Microbiology, Vol. 16, Issue 6
  • DOI: 10.1111/1462-2920.12343

Microbial consortium-mediated plant defense against phytopathogens: Readdressing for enhancing efficacy
journal, August 2015


Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils
journal, January 2015


A meta-analysis of plant responses to dark septate root endophytes
journal, January 2011


Seeking the elusive function of the root-colonising dark septate endophytic fungi
journal, January 2005


The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte
journal, July 2014

  • Xu, Xi-Hui; Su, Zhen-Zhu; Wang, Chen
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep05783

Identity, Diversity, and Molecular Phylogeny of the Endophytic Mycobiota in the Roots of Rare Wild Rice (Oryza granulate) from a Nature Reserve in Yunnan, China
journal, December 2009

  • Yuan, Z. -l.; Zhang, C. -l.; Lin, F. -c.
  • Applied and Environmental Microbiology, Vol. 76, Issue 5
  • DOI: 10.1128/AEM.01911-09

Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana
journal, February 2013


Capturing Greater 16S rRNA Gene Sequence Diversity within the Domain Bacteria
journal, June 2012

  • Winsley, T.; van Dorst, J. M.; Brown, M. V.
  • Applied and Environmental Microbiology, Vol. 78, Issue 16
  • DOI: 10.1128/AEM.01299-12

The composition of phyllosphere fungal assemblages of E uropean beech ( F agus sylvatica ) varies significantly along an elevation gradient
journal, August 2012


New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities
journal, July 2012


Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape
journal, July 2012

  • Zimmerman, N. B.; Vitousek, P. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 32
  • DOI: 10.1073/pnas.1209872109

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
journal, April 2009


Phylocom: software for the analysis of phylogenetic community structure and trait evolution
journal, August 2008


Conservation evaluation and phylogenetic diversity
journal, January 1992


Phylogenies and Community Ecology
journal, November 2002


Diversity and dissimilarity coefficients: A unified approach
journal, February 1982


Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata
journal, April 2012


An introduction to the analysis of shotgun metagenomic data
journal, June 2014


Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013

  • Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
  • Nature Biotechnology, Vol. 31, Issue 9
  • DOI: 10.1038/nbt.2676

STAMP: statistical analysis of taxonomic and functional profiles
journal, July 2014


A New Fungal Endophyte, Scolecobasidium humicola, Promotes Tomato Growth under Organic Nitrogen Conditions
journal, November 2013


    Works referencing / citing this record:

    Plant Host-Associated Mechanisms for Microbial Selection
    journal, July 2019


    Revegetation on abandoned salt ponds relieves the seasonal fluctuation of soil microbiomes
    journal, June 2019


    Halophytes in biosaline agriculture: Mechanism, utilization, and value addition
    journal, November 2017

    • Nikalje, Ganesh C.; Srivastava, Ashish K.; Pandey, Girdhar K.
    • Land Degradation & Development, Vol. 29, Issue 4
    • DOI: 10.1002/ldr.2819

    Revegetation on abandoned salt ponds relieves the seasonal fluctuation of soil microbiomes
    journal, June 2019


    Plant Host-Associated Mechanisms for Microbial Selection
    journal, July 2019


    Salt-Tolerant Halophyte Rhizosphere Bacteria Stimulate Growth of Alfalfa in Salty Soil
    journal, August 2019


    Endophytic Bacteria in Plant Salt Stress Tolerance: Current and Future Prospects
    journal, November 2018

    • Vaishnav, Anukool; Shukla, Awadhesh K.; Sharma, Anjney
    • Journal of Plant Growth Regulation, Vol. 38, Issue 2
    • DOI: 10.1007/s00344-018-9880-1

    An endophytic fungus, Gibberella moniliformis from Lawsonia inermis L. produces lawsone, an orange-red pigment
    journal, March 2017

    • Sarang, Hatnagar; Rajani, Pijakala; Vasanthakumari, Madhugiri Mallaiah
    • Antonie van Leeuwenhoek, Vol. 110, Issue 7
    • DOI: 10.1007/s10482-017-0858-y

    Deploying root microbiome of halophytes to improve salinity tolerance of crops
    journal, January 2020


    Strengthening desert plant biotechnology research in the United Arab Emirates: a viewpoint
    journal, May 2018

    • Gairola, Sanjay; Al Shaer, Khawla I.; Al Harthi, Eman K.
    • Physiology and Molecular Biology of Plants, Vol. 24, Issue 4
    • DOI: 10.1007/s12298-018-0551-2

    Potential of a halophyte-associated endophytic fungus for sustaining Chinese white poplar growth under salinity
    journal, February 2018


    Building plant microbiome vault: a future biotechnological resource
    journal, September 2018


    Distinct endophytes are used by diverse plants for adaptation to karst regions
    journal, March 2019


    Salt-tolerant and plant-growth-promoting bacteria isolated from high-yield paddy soil
    journal, December 2018

    • Zhang, Shiying; Fan, Cong; Wang, Yongxia
    • Canadian Journal of Microbiology, Vol. 64, Issue 12
    • DOI: 10.1139/cjm-2017-0571

    Research priorities for harnessing plant microbiomes in sustainable agriculture
    journal, March 2017


    The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response
    journal, November 2019


    Specialized core bacteria associate with plants adapted to adverse environment with high calcium contents
    journal, March 2018


    Salt tolerance of Cressa cretica and its rhizosphere microbiota
    journal, February 2020


    Mining Halophytes for Plant Growth-Promoting Halotolerant Bacteria to Enhance the Salinity Tolerance of Non-halophytic Crops
    journal, February 2018


    Bacterial Diversity Associated With the Rhizosphere and Endosphere of Two Halophytes: Glaux maritima and Salicornia europaea
    journal, November 2018


    Marine cyanolichens from different littoral zones are associated with distinct bacterial communities
    journal, January 2018