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

Yuan, Zhilin; Druzhinina, Irina S.; Labbé, Jessy; Redman, Regina; Qin, Yuan; Rodriguez, Russell; Zhang, Chulong; Tuskan, Gerald A.; Lin, Fucheng

doi:10.1038/srep32467

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

Journal Article · Tue Aug 30 00:00:00 EDT 2016 · Scientific Reports

DOI:https://doi.org/10.1038/srep32467· OSTI ID:1325488

Yuan, Zhilin ^[1]; Druzhinina, Irina S. ^[2]; Labbé, Jessy ^[3]; Redman, Regina ^[4]; Qin, Yuan ^[1]; Rodriguez, Russell ^[5]; Zhang, Chulong ^[6]; Tuskan, Gerald A. ^[3]; Lin, Fucheng ^[6]

Chinese Academy of Forestry, Hangzhou (People's Republic of China)
Institute of Chemical Engineering, Vienna (Austria)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Adaptive Symbiotic Technologies, Seattle, WA (United States)
Adaptive Symbiotic Technologies, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States)
Zhejiang Univ. (People's Republic of China)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1325488

Journal Information:: Scientific Reports, Vol. 6, Issue 10; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 121 works

Citation information provided by
Web of Science

References (84)

STAMP: statistical analysis of taxonomic and functional profiles Parks, Donovan H.; Tyson, Gene W.; Hugenholtz, Philip Bioinformatics, Vol. 30, Issue 21 https://doi.org/10.1093/bioinformatics/btu494	journal	July 2014
Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments Mora-Ruiz, Merit del R.; Font-Verdera, Francisca; Orfila, Alejandro FEMS Microbiology Ecology, Vol. 92, Issue 9 https://doi.org/10.1093/femsec/fiw145	journal	June 2016
Contrasting Patterns of Community Assembly in the Stratified Water Column of Great Salt Lake, Utah Meuser, Jonathan E.; Baxter, Bonnie K.; Spear, John R. Microbial Ecology, Vol. 66, Issue 2 https://doi.org/10.1007/s00248-013-0180-9	journal	January 2013
A meta-analysis of plant responses to dark septate root endophytes Newsham, K. K. New Phytologist, Vol. 190, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03611.x	journal	January 2011
Microbial genome-enabled insights into plant–microorganism interactions Guttman, David S.; McHardy, Alice C.; Schulze-Lefert, Paul Nature Reviews Genetics, Vol. 15, Issue 12 https://doi.org/10.1038/nrg3748	journal	September 2014
Stress tolerance in plants via habitat-adapted symbiosis Rodriguez, Rusty J.; Henson, Joan; Van Volkenburgh, Elizabeth The ISME Journal, Vol. 2, Issue 4 https://doi.org/10.1038/ismej.2007.106	journal	February 2008
Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance Coleman-Derr, Devin; Tringe, Susannah G. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00283	journal	June 2014
Enhancing Native Grass Productivity by Cocultivating With Endophyte-Laden Calli Lucero, M. E.; Barrow, J. R.; Osuna, P. Rangeland Ecology & Management, Vol. 61, Issue 1 https://doi.org/10.2111/06-144R3.1	journal	January 2008
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory Nature Biotechnology, Vol. 31, Issue 9 https://doi.org/10.1038/nbt.2676	journal	August 2013
Beyond the Venn diagram: the hunt for a core microbiome: The hunt for a core microbiome Shade, Ashley; Handelsman, Jo Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02585.x	journal	October 2011
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Rapid responses of soil microorganisms improve plant fitness in novel environments Lau, J. A.; Lennon, J. T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1202319109	journal	August 2012
Thermotolerance Generated by Plant/Fungal Symbiosis Redman, R. S. Science, Vol. 298, Issue 5598 https://doi.org/10.1126/science.1072191	journal	November 2002
Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response Becker, Erin A.; Seitzer, Phillip M.; Tritt, Andrew PLoS Genetics, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pgen.1004784	journal	November 2014
Thermotolerance Generated by Plant/Fungal Symbiosis Redman, Regina S.; Sheehan, Kathy B.; Stout, Richard G. Science, Vol. 298, Issue 5598 https://doi.org/10.1126/science.1078055	journal	November 2002
Microbial consortium-mediated plant defense against phytopathogens: Readdressing for enhancing efficacy Sarma, Birinchi Kumar; Yadav, Sudheer Kumar; Singh, Surendra Soil Biology and Biochemistry, Vol. 87 https://doi.org/10.1016/j.soilbio.2015.04.001	journal	August 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Diversity and dissimilarity coefficients: A unified approach Rao, C. Radhakrishna Theoretical Population Biology, Vol. 21, Issue 1 https://doi.org/10.1016/0040-5809(82)90004-1	journal	February 1982
Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups Placella, S. A.; Brodie, E. L.; Firestone, M. K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1204306109	journal	June 2012
Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata Printzen, Christian; Fernández-Mendoza, Fernando; Muggia, Lucia FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01358.x	journal	April 2012
Comparative and genetic analysis of the four sequenced Paenibacillus polymyxa genomes reveals a diverse metabolism and conservation of genes relevant to plant-growth promotion and competitiveness Eastman, Alexander W.; Heinrichs, David E.; Yuan, Ze-Chun BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-851	journal	January 2014
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Characterization of NADH Dehydrogenases of Pseudomonas fluorescens WCS365 and Their Role in Competitive Root Colonization Camacho Carvajal, Margarita M.; Wijfjes, André H. M.; Mulders, Ine H. M. Molecular Plant-Microbe Interactions, Vol. 15, Issue 7 https://doi.org/10.1094/mpmi.2002.15.7.662	journal	July 2002
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities Ihrmark, Katarina; Bödeker, Inga T. M.; Cruz-Martinez, Karelyn FEMS Microbiology Ecology, Vol. 82, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01437.x	journal	July 2012
Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior Badri, Dayakar V.; Zolla, Gaston; Bakker, Matthew G. New Phytologist, Vol. 198, Issue 1 https://doi.org/10.1111/nph.12124	journal	January 2013
A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota Bodenhausen, Natacha; Bortfeld-Miller, Miriam; Ackermann, Martin ETH Zurich https://doi.org/10.3929/ethz-b-000084841	text	January 2014
Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L. Szymańska, Sonia; Płociniczak, Tomasz; Piotrowska-Seget, Zofia Microbiological Research, Vol. 182 https://doi.org/10.1016/j.micres.2015.09.007	journal	January 2016
The potential for give and take in plantâ€“microbiome relationships Lebeis, Sarah L. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00287	journal	June 2014
A New Fungal Endophyte, Scolecobasidium humicola, Promotes Tomato Growth under Organic Nitrogen Conditions Mahmoud, Rola S.; Narisawa, Kazuhiko PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078746	journal	November 2013
Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem Lakshmanan, V.; Selvaraj, G.; Bais, H. P. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.245811	journal	July 2014
An introduction to the analysis of shotgun metagenomic data Sharpton, Thomas J. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00209	journal	June 2014
Defining the core Arabidopsis thaliana root microbiome E., Ley, Ruth; Julien, Tremblay,; L., Dangl, Jeffery The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/w03e-5q36	text	January 2012
Rhizosphere Microbes as Essential Partners for Plant Stress Tolerance de Zelicourt, Axel; Al-Yousif, Mohamed; Hirt, Heribert Molecular Plant, Vol. 6, Issue 2 https://doi.org/10.1093/mp/sst028	journal	March 2013
Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping Santhanam, Rakesh; Luu, Van Thi; Weinhold, Arne Proceedings of the National Academy of Sciences, Vol. 112, Issue 36 https://doi.org/10.1073/pnas.1505765112	journal	August 2015
A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota Bodenhausen, Natacha; Bortfeld-Miller, Miriam; Ackermann, Martin PLoS Genetics, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pgen.1004283	journal	April 2014
Seeking the elusive function of the root-colonising dark septate endophytic fungi Mandyam, Keerthi; Jumpponen, Ari Studies in Mycology, Vol. 53 https://doi.org/10.3114/sim.53.1.173	journal	January 2005
High-Throughput Sequencing: A Roadmap Toward Community Ecology Poisot, Timothée; Péquin, Bérangère; Gravel, Dominique Ecology and Evolution, Vol. 3, Issue 4 https://doi.org/10.1002/ece3.508	journal	March 2013
Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts Martin, Kendall J.; Rygiewicz, Paul T. BMC Microbiology, Vol. 5, Issue 1, p. 28 https://doi.org/10.1186/1471-2180-5-28	journal	May 2005
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
Phylocom: software for the analysis of phylogenetic community structure and trait evolution Webb, Campbell O.; Ackerly, David D.; Kembel, Steven W. Bioinformatics, Vol. 24, Issue 18 https://doi.org/10.1093/bioinformatics/btn358	journal	August 2008
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data Librado, P.; Rozas, J. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp187	journal	April 2009
Fungal Assemblages Associated with Roots of Halophytic and Non-halophytic Plant Species Vary Differentially Along a Salinity Gradient Maciá-Vicente, Jose G.; Ferraro, Valeria; Burruano, Santella Microbial Ecology, Vol. 64, Issue 3 https://doi.org/10.1007/s00248-012-0066-2	journal	May 2012
Endophyte Microbiome Diversity in Micropropagated Atriplex canescens and Atriplex torreyi var griffithsii Lucero, Mary E.; Unc, Adrian; Cooke, Peter PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017693	journal	March 2011
A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming Marasco, Ramona; Rolli, Eleonora; Ettoumi, Besma PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0048479	journal	October 2012
Root surface as a frontier for plant microbiome research: Fig. 1. van der Heijden, Marcel G. A.; Schlaeppi, Klaus Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1500709112	journal	February 2015
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related Proteobacteria Bruto, Maxime; Prigent-Combaret, Claire; Muller, Daniel Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06261	journal	September 2014
Composition and Predictive Functional Analysis of Bacterial Communities in Seawater, Sediment and Sponges in the Spermonde Archipelago, Indonesia Cleary, Daniel F. R.; de Voogd, Nicole J.; Polónia, Ana R. M. Microbial Ecology, Vol. 70, Issue 4 https://doi.org/10.1007/s00248-015-0632-5	journal	June 2015
Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana Bodenhausen, Natacha; Horton, Matthew W.; Bergelson, Joy PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056329	journal	February 2013
Properties of the halophyte microbiome and their implications for plant salt tolerance Ruppel, Silke; Franken, Philipp; Witzel, Katja Functional Plant Biology, Vol. 40, Issue 9 https://doi.org/10.1071/FP12355	journal	January 2013
Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems Davidson, A. L.; Dassa, E.; Orelle, C. Microbiology and Molecular Biology Reviews, Vol. 72, Issue 2 https://doi.org/10.1128/MMBR.00031-07	journal	June 2008
Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative S., Lundberg, Derek; Thomas, Mitchell-Olds,; G., Tringe, Susannah The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/xdb1-mm42	text	January 2014
Culturing a plant microbiome community at the cross‐Rhodes Lebeis, Sarah L.; Rott, Matthias; Dangl, Jeffery L. New Phytologist, Vol. 196, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04336.x	journal	August 2012
Species and geographic specificity between endophytic fungi and host supported by parasitic Cynomorium songaricum and its host Nitraria tangutorum distributed in desert Miao, Shuang-Man; Zhang, Yan-Yan; Cui, Jin-Long Archives of Microbiology, Vol. 203, Issue 5 https://doi.org/10.1007/s00203-021-02224-7	journal	March 2021
A Two-Component System Plays an Important Role in the Root-Colonizing Ability of Pseudomonas fluorescens Strain WCS365 Dekkers, Linda C.; Bloemendaal, Cees Jan P.; de Weger, Letty A. Molecular Plant-Microbe Interactions, Vol. 11, Issue 1 https://doi.org/10.1094/MPMI.1998.11.1.45	journal	January 1998
Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils White, James F.; Chen, Qiang; Torres, Mónica S. AoB PLANTS, Vol. 7 https://doi.org/10.1093/aobpla/plu093	journal	January 2015
Structure and Functions of the Bacterial Microbiota of Plants Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120106	journal	April 2013
Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait: Root bacteria protect plants from drought Rolli, Eleonora; Marasco, Ramona; Vigani, Gianpiero Environmental Microbiology, Vol. 17, Issue 2 https://doi.org/10.1111/1462-2920.12439	journal	March 2014
Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types Gottel, Neil R.; Castro, Hector F.; Kerley, Marilyn Applied and Environmental Microbiology, Vol. 77, Issue 17 https://doi.org/10.1128/AEM.05255-11	journal	July 2011
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 Yuan, Z. -l.; Zhang, C. -l.; Lin, F. -c. Applied and Environmental Microbiology, Vol. 76, Issue 5 https://doi.org/10.1128/aem.01911-09	journal	December 2009
The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte Xu, Xi-Hui; Su, Zhen-Zhu; Wang, Chen Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep05783	journal	July 2014
A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods Kaplan, Drora; Maymon, Maskit; Agapakis, Christina M. American Journal of Botany, Vol. 100, Issue 9 https://doi.org/10.3732/ajb.1200615	journal	September 2013
The composition of phyllosphere fungal assemblages of E uropean beech ( F agus sylvatica ) varies significantly along an elevation gradient Cordier, Tristan; Robin, Cécile; Capdevielle, Xavier New Phytologist, Vol. 196, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04284.x	journal	August 2012
PHYMYCO-DB: A Curated Database for Analyses of Fungal Diversity and Evolution Mahé, Stéphane; Duhamel, Marie; Le Calvez, Thomas PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0043117	journal	September 2012
Phylogenies and Community Ecology Webb, Campbell O.; Ackerly, David D.; McPeek, Mark A. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.010802.150448	journal	November 2002
Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection Mercado-Blanco, Jesús; Bakker, Peter A. H. M. Antonie van Leeuwenhoek, Vol. 92, Issue 4 https://doi.org/10.1007/s10482-007-9167-1	journal	June 2007
Towards a holistic understanding of the beneficial interactions across the Populus microbiome Hacquard, Stéphane; Schadt, Christopher W. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13133	journal	November 2014
Phylogenetic Clustering and Overdispersion in Bacterial Communities Horner-Devine, M. Claire; Bohannan, Brendan J. M. Ecology, Vol. 87, Issue sp7 https://doi.org/10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2	journal	July 2006
The importance of the microbiome of the plant holobiont Vandenkoornhuyse, Philippe; Quaiser, Achim; Duhamel, Marie New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13312	journal	February 2015
Conservation evaluation and phylogenetic diversity Faith, Daniel P. Biological Conservation, Vol. 61, Issue 1 https://doi.org/10.1016/0006-3207(92)91201-3	journal	January 1992
Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape Zimmerman, N. B.; Vitousek, P. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 32 https://doi.org/10.1073/pnas.1209872109	journal	July 2012
Capturing Greater 16S rRNA Gene Sequence Diversity within the Domain Bacteria Winsley, T.; van Dorst, J. M.; Brown, M. V. Applied and Environmental Microbiology, Vol. 78, Issue 16 https://doi.org/10.1128/aem.01299-12	journal	June 2012
Microbially Mediated Plant Functional Traits Friesen, Maren L.; Porter, Stephanie S.; Stark, Scott C. Annual Review of Ecology, Evolution, and Systematics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev-ecolsys-102710-145039	journal	December 2011
A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365 Dekkers, L. C.; Phoelich, C. C.; van der Fits, L. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.7051	journal	June 1998
Inoculants of plant growth-promoting bacteria for use in agriculture Bashan, Yoav Biotechnology Advances, Vol. 16, Issue 4 https://doi.org/10.1016/S0734-9750(98)00003-2	journal	July 1998
Multivariate and Phylogenetic Analyses Assessing the Response of Bacterial Mat Communities from an Ancient Oligotrophic Aquatic Ecosystem to Different Scenarios of Long-Term Environmental Disturbance Pajares, Silvia; Souza, Valeria; Eguiarte, Luis E. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0119741	journal	March 2015
Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana Bodenhausen, Natacha; Horton, Matthew W.; Bergelson, Joy ETH Zurich https://doi.org/10.3929/ethz-b-000075849	text	January 2013
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11336	journal	August 2012
Diversity and heritability of the maize rhizosphere microbiome under field conditions Z., Jin,; S., Buckler, E.; O., Koren, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/rzga-0c56	text	January 2013
Diversity and heritability of the maize rhizosphere microbiome under field conditions Peiffer, J. A.; Spor, A.; Koren, O. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1302837110	journal	April 2013
Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities: Synthetic microbial ecosystems De Roy, Karen; Marzorati, Massimo; Van den Abbeele, Pieter Environmental Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/1462-2920.12343	journal	December 2013
Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative Wagner, Maggie R.; Lundberg, Derek S.; Coleman-Derr, Devin Ecology Letters, Vol. 17, Issue 6 https://doi.org/10.1111/ele.12276	journal	April 2014
Halophilic Bacteria: Potentials and Applications in Biotechnology Mohammadipanah, Fatemeh; Hamedi, Javad; Dehhaghi, Mona Sustainable Development and Biodiversity https://doi.org/10.1007/978-3-319-14595-2_11	book	January 2015

Cited By (30)

Research priorities for harnessing plant microbiomes in sustainable agriculture Alison, Bennett,; Mustafa, Morsy,; E., Leach, Jan The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/bt3a-tr35	text	January 2017
Marine cyanolichens from different littoral zones are associated with distinct bacterial communities West, Nyree J.; Parrot, Delphine; Fayet, Claire PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5208	journal	January 2018
Diversity and community of culturable endophytic fungi from stems and roots of desert halophytes in northwest China Li, Jia-Long; Sun, Xiang; Zheng, Yong MycoKeys, Vol. 62 https://doi.org/10.3897/mycokeys.62.38923	journal	February 2020
Strengthening desert plant biotechnology research in the United Arab Emirates: a viewpoint Gairola, Sanjay; Al Shaer, Khawla I.; Al Harthi, Eman K. Physiology and Molecular Biology of Plants, Vol. 24, Issue 4 https://doi.org/10.1007/s12298-018-0551-2	journal	May 2018
Microbial Communities and Their Predicted Metabolic Functions in Growth Laminae of a Unique Large Conical Mat from Lake Untersee, East Antarctica Koo, Hyunmin; Mojib, Nazia; Hakim, Joseph A. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01347	journal	August 2017
Deploying root microbiome of halophytes to improve salinity tolerance of crops Akyol, Turgut Yigit; Sato, Shusei; Turkan, Ismail Plant Biotechnology Reports, Vol. 14, Issue 2 https://doi.org/10.1007/s11816-020-00594-w	journal	January 2020
Efficient colonization of the endophytes Herbaspirillum huttiense RCA24 and Enterobacter cloacae RCA25 influences the physiological parameters of Oryza sativa L. cv. Baldo rice Andreozzi, Anna; Prieto, Pilar; Mercado‐Blanco, Jesús Environmental Microbiology, Vol. 21, Issue 9 https://doi.org/10.1111/1462-2920.14688	journal	August 2018
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response Finkel, Omri M.; Salas-González, Isai; Castrillo, Gabriel PLOS Biology, Vol. 17, Issue 11 https://doi.org/10.1371/journal.pbio.3000534	journal	November 2019
Distinct endophytes are used by diverse plants for adaptation to karst regions Li, Fei; He, Xiaohong; Sun, Yuanyuan Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-41802-0	journal	March 2019
The Microbiome and Mosquito Vectorial Capacity: Rich Potential for Discovery and Translation Cansado-Utrilla, Cintia; Zhao, Serena; McCall, Philip Preprints.org https://doi.org/10.20944/preprints202012.0554.v1	posted_content	December 2020
Salt-tolerant and plant-growth-promoting bacteria isolated from high-yield paddy soil Zhang, Shiying; Fan, Cong; Wang, Yongxia Canadian Journal of Microbiology, Vol. 64, Issue 12 https://doi.org/10.1139/cjm-2017-0571	journal	December 2018
Plant Host-Associated Mechanisms for Microbial Selection Jones, Piet; Garcia, Benjamin J.; Furches, Anna Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00862	journal	July 2019
Bacterial Diversity Associated With the Rhizosphere and Endosphere of Two Halophytes: Glaux maritima and Salicornia europaea Yamamoto, Kosuke; Shiwa, Yuh; Ishige, Taichiro Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02878	journal	November 2018
An endophytic fungus, Gibberella moniliformis from Lawsonia inermis L. produces lawsone, an orange-red pigment Sarang, Hatnagar; Rajani, Pijakala; Vasanthakumari, Madhugiri Mallaiah Antonie van Leeuwenhoek, Vol. 110, Issue 7 https://doi.org/10.1007/s10482-017-0858-y	journal	March 2017
Specialized core bacteria associate with plants adapted to adverse environment with high calcium contents Li, Fei; Zhang, Ximin; Gong, Jiyi PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0194080	journal	March 2018
Halophytes in biosaline agriculture: Mechanism, utilization, and value addition Nikalje, Ganesh C.; Srivastava, Ashish K.; Pandey, Girdhar K. Land Degradation & Development, Vol. 29, Issue 4 https://doi.org/10.1002/ldr.2819	journal	November 2017
Building plant microbiome vault: a future biotechnological resource Gopal, Murali; Gupta, Alka Symbiosis, Vol. 77, Issue 1 https://doi.org/10.1007/s13199-018-0574-z	journal	September 2018
Revegetation on abandoned salt ponds relieves the seasonal fluctuation of soil microbiomes Tran, Huyen-Trang; Wang, Hao-Chu; Hsu, Tsai-Wen BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5875-y	journal	June 2019
Research priorities for harnessing plant microbiomes in sustainable agriculture Busby, Posy E.; Soman, Chinmay; Wagner, Maggie R. PLOS Biology, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pbio.2001793	journal	March 2017
Potential of Bacopa monnieri (L.) Wettst and Sesuvium verrucosum Raf. as an agronomic management alternative to recover the productivity of saline soils Lastiri-Hernández, Marcos A.; Álvarez-Bernal, Dioselina; Ochoa-Estrada, Salvador International Journal of Phytoremediation, Vol. 22, Issue 4 https://doi.org/10.1080/15226514.2019.1663484	journal	September 2019
Salt tolerance of Cressa cretica and its rhizosphere microbiota Etemadi, Nematollah; Müller, Maria; Etemadi, Mohammad Biologia, Vol. 75, Issue 3 https://doi.org/10.2478/s11756-020-00416-y	journal	February 2020
Salt-Tolerant Halophyte Rhizosphere Bacteria Stimulate Growth of Alfalfa in Salty Soil Kearl, Jennifer; McNary, Caitlyn; Lowman, J. Scott Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01849	journal	August 2019
Endophytic Bacteria in Plant Salt Stress Tolerance: Current and Future Prospects Vaishnav, Anukool; Shukla, Awadhesh K.; Sharma, Anjney Journal of Plant Growth Regulation, Vol. 38, Issue 2 https://doi.org/10.1007/s00344-018-9880-1	journal	November 2018
The Combination of Trichoderma harzianum and Chemical Fertilization Leads to the Deregulation of Phytohormone Networking, Preventing the Adaptive Responses of Tomato Plants to Salt Stress Rubio, M. B.; Hermosa, Rosa; Vicente, Rubén Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00294	journal	March 2017
Mining Halophytes for Plant Growth-Promoting Halotolerant Bacteria to Enhance the Salinity Tolerance of Non-halophytic Crops Etesami, Hassan; Beattie, Gwyn A. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00148	journal	February 2018
Marine cyanolichens from different littoral zones are associated with distinct bacterial communities West, Nyree J.; Parrot, Delphine; Fayet, Claire bioRxiv https://doi.org/10.1101/209320	posted_content	June 2018
Ecological and functional adaptations to water management in a semiarid agroecosystem: a soil metaproteomics approach Starke, Robert; Bastida, Felipe; Abadía, Joaquín Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09973-w	journal	August 2017
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response G., Castrillo,; P. J. P. L., Teixeira,; S., Spaepen, Public Library of Science https://doi.org/10.17615/khqf-c670	text	January 2019
Mining the roots of various species of the halophyte Suaeda for halotolerant nitrogen-fixing endophytic bacteria with the potential for promoting plant growth Alishahi, Frashad; Alikhani, Hossein Ali; Khoshkholgh-Sima, Nayer Azam International Microbiology, Vol. 23, Issue 3 https://doi.org/10.1007/s10123-019-00115-y	journal	January 2020
Potential of a halophyte-associated endophytic fungus for sustaining Chinese white poplar growth under salinity Pan, Xueyu; Qin, Yuan; Yuan, Zhilin Symbiosis, Vol. 76, Issue 2 https://doi.org/10.1007/s13199-018-0541-8	journal	February 2018

Similar Records

Insight into a highly polymorphic endophyte isolated from the roots of the halophytic seepweed Suaeda salsa: Laburnicola rhizohalophila sp. nov. (Didymosphaeriaceae, Pleosporales)

Journal Article · Wed Oct 16 00:00:00 EDT 2019 · Fungal Biology · OSTI ID:1325488

Yuan, Zhilin; Druzhinina, Irina S.; Wang, Xinyu; +3 more

Chronic drought differentially alters the belowground microbiome of drought tolerant and drought susceptible genotypes of Populus trichocarpa

Journal Article · Wed Jul 13 00:00:00 EDT 2022 · Phytobiomes Journal · OSTI ID:1325488

Kristy, Brandon David; Carrell, Alyssa A.; Johnston, Eric R.; +7 more

A multifactor analysis of fungal and bacterial community structure of the root microbiome of mature Populus deltoides trees

Journal Article · Tue Jan 01 00:00:00 EST 2013 · PLoS ONE · OSTI ID:1325488

Shakya, Migun; Gottel, Neil R; Castro Gonzalez, Hector F; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (84)

Cited By (30)

Similar Records

Related Subjects