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

Kristy, Brandon David; Carrell, Alyssa A.; Johnston, Eric R.; Cumming, Jonathan R.; Klingeman, Dawn Marie; Gwinn, Kimberly; Syring, Kimberly C.; Skalla, Caroline; Emrich, Scott; Cregger, Melissa A.

doi:10.1094/pbiomes-12-21-0076-r

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

Journal Article · 12 July 2022 · Phytobiomes Journal

DOI: https://doi.org/10.1094/pbiomes-12-21-0076-r · OSTI ID:1879964

^[1]; Carrell, Alyssa A. ^[2];

^[2]; Cumming, Jonathan R. ^[2];

^[2]; Gwinn, Kimberly ^[3]; Syring, Kimberly C. ^[4]; Skalla, Caroline ^[5]; Emrich, Scott ^[3]; Cregger, Melissa A. ^[2]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Oregon State Univ., Corvallis, OR (United States)
Kalamazoo College, MI (United States)

Populus trichocarpa is an ecologically important tree species and economically important biofeedstock. Belowground, P. trichocarpa interacts with diverse microorganisms in the rhizosphere and root endosphere. These plant-microbial interactions can bolster a variety of plant processes, ranging from pathogen suppression to drought tolerance, yet we know little about the impact of chronic drought stress on P. trichocarpa’s belowground microbiomes. To investigate the interactive effect of chronic drought on belowground microbial communities across genetically different P. trichocarpa hosts, we assessed archaeal/bacterial and fungal communities within the root endosphere, rhizosphere, and surrounding bulk soil of selected genotypes in a long-term drought experiment in Boardman, OR, USA. We sequenced the 16S rRNA and ITS2 gene region on samples collected from 16 distinct P. trichocarpa genotypes in plots with full or reduced irrigation. Eight of these genotypes have been previously identified as drought tolerant while the other eight genotypes were drought susceptible. While reduced irrigation influenced the composition of every archaeal/bacterial microbiome compartment, fungal communities were only affected in the rhizosphere and bulk soil compartments. Drought-tolerant bacteria, such as Actinobacteria, were differentially abundant in reduced irrigation across all belowground microbiomes. Host drought-tolerance influenced plant-associated microbiome compartments but had little impact on the bulk soil compartment. Drought-tolerant trees were enriched for potential growth-promoting microorganisms in the root endosphere and rhizosphere, including Sphingomonas bacteria and ectomycorrhizal fungi. Overall, associations of growth-promoting microbes in drought resistant P. trichocarpa genotypes can be leveraged to improve biofeedstock productivity in regions prone to periodic drought.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)

Sponsoring Organization:: Agriculture and Food Research Initiative (AFRI); National Institute of Food and Agriculture (NIFA); USDA; USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Workforce Development for Teachers and Scientists (WDTS)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1879964

Journal Information:: Phytobiomes Journal, Journal Name: Phytobiomes Journal Journal Issue: 4 Vol. 6; ISSN 2471-2906

Publisher:: American Phytopathological Society (APS)Copyright Statement

Country of Publication:: United States

Language:: English

References (78)

Economic impact of yield and composition variation in bioenergy crops: Populus trichocarpa Happs, Renee M.; Bartling, Andrew W.; Doeppke, Crissa Biofuels, Bioproducts and Biorefining, Vol. 15, Issue 1 https://doi.org/10.1002/bbb.2148	journal	October 2020
Exploring variation in phyllosphere microbial communities across four hemlock species Rogers, Timothy J.; Leppanen, Christy; Brown, Veronica Ecosphere, Vol. 9, Issue 12 https://doi.org/10.1002/ecs2.2524	journal	December 2018
Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods Gehring, Catherine A.; Mueller, Rebecca C.; Whitham, Thomas G. Oecologia, Vol. 149, Issue 1 https://doi.org/10.1007/s00442-006-0437-9	journal	April 2006
Paxillus involutus mycorrhiza attenuate NaCl-stress responses in the salt-sensitive hybrid poplar Populus×canescens Langenfeld-Heyser, R.; Gao, J.; Ducic, T. Mycorrhiza, Vol. 17, Issue 2 https://doi.org/10.1007/s00572-006-0084-3	journal	November 2006
Impact of plant domestication on rhizosphere microbiome assembly and functions Pérez-Jaramillo, Juan E.; Mendes, Rodrigo; Raaijmakers, Jos M. Plant Molecular Biology, Vol. 90, Issue 6 https://doi.org/10.1007/s11103-015-0337-7	journal	June 2015
Rhizodeposition under drought and consequences for soil communities and ecosystem resilience Preece, Catherine; Peñuelas, Josep Plant and Soil, Vol. 409, Issue 1-2 https://doi.org/10.1007/s11104-016-3090-z	journal	November 2016
Microbiome data science Shetty, Sudarshan A.; Lahti, Leo Journal of Biosciences, Vol. 44, Issue 5 https://doi.org/10.1007/s12038-019-9930-2	journal	September 2019
Enhanced Drought and Salt Stress Tolerance in Arabidopsis by Flavobacterium crocinum HYN0056T Kim, Jeong-eun; Woo, Og-Geum; Bae, Yoowon Journal of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1007/s12374-020-09236-8	journal	February 2020
FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild Nguyen, Nhu H.; Song, Zewei; Bates, Scott T. Fungal Ecology, Vol. 20 https://doi.org/10.1016/j.funeco.2015.06.006	journal	April 2016
Greater than the sum of their parts: characterizing plant microbiomes at the community-level Lebeis, Sarah L. Current Opinion in Plant Biology, Vol. 24 https://doi.org/10.1016/j.pbi.2015.02.004	journal	April 2015
Arbuscular mycorrhizal fungal responses to abiotic stresses: A review Lenoir, Ingrid; Fontaine, Joël; Lounès-Hadj Sahraoui, Anissa Phytochemistry, Vol. 123 https://doi.org/10.1016/j.phytochem.2016.01.002	journal	March 2016
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
Complete genome sequence of Sphingomonas sp. Cra20, a drought resistant and plant growth promoting rhizobacteria Luo, Yang; Zhou, Meng; Zhao, Qi Genomics, Vol. 112, Issue 5 https://doi.org/10.1016/j.ygeno.2020.04.013	journal	September 2020
Drought and host selection influence bacterial community dynamics in the grass root microbiome Naylor, Dan; DeGraaf, Stephanie; Purdom, Elizabeth The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.118	journal	July 2017
Host genotype and age shape the leaf and root microbiomes of a wild perennial plant Wagner, Maggie R.; Lundberg, Derek S.; del Rio, Tijana G. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12151	journal	July 2016
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Soil bacterial networks are less stable under drought than fungal networks de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05516-7	journal	August 2018
Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops Grady, Keara L.; Sorensen, Jackson W.; Stopnisek, Nejc Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11974-4	journal	September 2019
Prolonged drought imparts lasting compositional changes to the rice root microbiome Santos-Medellín, Christian; Liechty, Zachary; Edwards, Joseph Nature Plants, Vol. 7, Issue 8 https://doi.org/10.1038/s41477-021-00967-1	journal	July 2021
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Conditioned soils reveal plant-selected microbial communities that impact plant drought response Monohon, Samantha J.; Manter, Daniel K.; Vivanco, Jorge M. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-00593-z	journal	October 2021
Profiling, isolation and characterisation of beneficial microbes from the seed microbiomes of drought tolerant wheat Hone, Holly; Mann, Ross; Yang, Guodong Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-91351-8	journal	June 2021
Specialized Microbiome of a Halophyte and its Role in Helping Non-Host Plants to Withstand Salinity Yuan, Zhilin; Druzhinina, Irina S.; Labbé, Jessy Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32467	journal	August 2016
Interactions between plants and soil shaping the root microbiome under abiotic stress Hartman, Kyle; Tringe, Susannah G. Biochemical Journal, Vol. 476, Issue 19 https://doi.org/10.1042/BCJ20180615	journal	October 2019
Ectomycorrhizal fungus (Paxillus involutus) and hydrogels affect performance of Populus euphratica exposed to drought stress Luo, Zhi-Bin; Li, Ke; Jiang, Xiangning Annals of Forest Science, Vol. 66, Issue 1 https://doi.org/10.1051/forest:2008073	journal	January 2009
Tree genetics defines fungal partner communities that may confer drought tolerance Gehring, Catherine A.; Sthultz, Christopher M.; Flores-Rentería, Lluvia Proceedings of the National Academy of Sciences, Vol. 114, Issue 42 https://doi.org/10.1073/pnas.1704022114	journal	September 2017
Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition Almario, Juliana; Jeena, Ganga; Wunder, Jörg Proceedings of the National Academy of Sciences, Vol. 114, Issue 44 https://doi.org/10.1073/pnas.1710455114	journal	October 2017
Assembly and ecological function of the root microbiome across angiosperm plant species Fitzpatrick, Connor R.; Copeland, Julia; Wang, Pauline W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1717617115	journal	January 2018
Metagenomic Analysis of Rhizosphere Bacteria in Desert Plant Calotropis procera Ramadan, Ahmed M.; Nazar, Mohammad A. H.; Gadallah, Nour O. Geomicrobiology Journal, Vol. 38, Issue 5 https://doi.org/10.1080/01490451.2020.1860166	journal	December 2020
Auxin production by rhizobacteria was associated with improved yield of wheat (Triticum aestivum L.) under drought stress Raheem, Asif; Shaposhnikov, Alexander; Belimov, Andrey A. Archives of Agronomy and Soil Science, Vol. 64, Issue 4 https://doi.org/10.1080/03650340.2017.1362105	journal	August 2017
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Clonal and seasonal differences in leaf osmotic potential and organic solutes of five hybrid poplar clones grown under field conditions Gebre, G. M.; Tschaplinski, T. J.; Tuskan, G. A. Tree Physiology, Vol. 18, Issue 10 https://doi.org/10.1093/treephys/18.10.645	journal	October 1998
Phenotypic variation and quantitative trait locus identification for osmotic potential in an interspecific hybrid inbred F2 poplar pedigree grown in contrasting environments Tschaplinski, T. J.; Tuskan, G. A.; Sewell, M. M. Tree Physiology, Vol. 26, Issue 5 https://doi.org/10.1093/treephys/26.5.595	journal	May 2006
Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling Barchet, G. L. H.; Dauwe, R.; Guy, R. D. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt080	journal	October 2013
Plant–Microbe Interactions: From Genes to Ecosystems Using Populus as a Model System Cregger, Melissa A.; Carper, Dana L.; Christel, Stephan Phytobiomes Journal, Vol. 5, Issue 1 https://doi.org/10.1094/PBIOMES-01-20-0009-FI	journal	January 2021
Regional Differences in the Structure of Juglans nigra Phytobiome Reflect Geographical Differences in Thousand Cankers Disease Severity Onufrak, Aaron J.; Williams, Geoffrey M.; Klingeman, William E. Phytobiomes Journal, Vol. 4, Issue 4 https://doi.org/10.1094/PBIOMES-05-20-0044-R	journal	January 2020
Managing Plant Microbiomes for Sustainable Biofuel Production Zhalnina, Kateryna; Hawkes, Christine; Shade, Ashley Phytobiomes Journal, Vol. 5, Issue 1 https://doi.org/10.1094/PBIOMES-12-20-0090-E	journal	January 2021
Bacterial community composition of divergent soil habitats in a polar desert Geyer, Kevin M.; Altrichter, Adam E.; Takacs-Vesbach, Cristina D. FEMS Microbiology Ecology, Vol. 89, Issue 2 https://doi.org/10.1111/1574-6941.12306	journal	March 2014
Analysis of large 16S rRNA Illumina data sets: Impact of singleton read filtering on microbial community description Auer, Lucas; Mariadassou, Mahendra; O'Donohue, Michael Molecular Ecology Resources, Vol. 17, Issue 6 https://doi.org/10.1111/1755-0998.12700	journal	August 2017
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
The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters Abarenkov, Kessy; Henrik Nilsson, R.; Larsson, Karl-Henrik New Phytologist, Vol. 186, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03160.x	journal	March 2010
Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere: Plant species, soil type and rhizosphere communities Berg, Gabriele; Smalla, Kornelia FEMS Microbiology Ecology, Vol. 68, Issue 1 https://doi.org/10.1111/j.1574-6941.2009.00654.x	journal	April 2009
Drought stress and plant ecotype drive microbiome recruitment in switchgrass rhizosheath Liu, Tie‐Yuan; Ye, Nenghui; Wang, Xinyu Journal of Integrative Plant Biology, Vol. 63, Issue 10 https://doi.org/10.1111/jipb.13154	journal	August 2021
Diffuse symbioses: roles of plant-plant, plant-microbe and microbe-microbe interactions in structuring the soil microbiome Bakker, Matthew G.; Schlatter, Daniel C.; Otto-Hanson, Lindsey Molecular Ecology, Vol. 23, Issue 6 https://doi.org/10.1111/mec.12571	journal	November 2013
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
Plant root exudation under drought: implications for ecosystem functioning Williams, Alex; Vries, Franciska T. New Phytologist, Vol. 225, Issue 5 https://doi.org/10.1111/nph.16223	journal	October 2019
Enabling sustainable agriculture through understanding and enhancement of microbiomes Trivedi, Pankaj; Mattupalli, Chakradhar; Eversole, Kellye New Phytologist, Vol. 230, Issue 6 https://doi.org/10.1111/nph.17319	journal	April 2021
Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus × canescens: Ectomycorrhizas enhance poplar Cd tolerance Ma, Yonglu; He, Jiali; Ma, Chaofeng Plant, Cell & Environment, Vol. 37, Issue 3 https://doi.org/10.1111/pce.12183	journal	September 2013
Insights into the plant responses to drought and decoding the potential of root associated microbiome for inducing drought tolerance Mathur, Piyush; Roy, Swarnendu Physiologia Plantarum, Vol. 172, Issue 2 https://doi.org/10.1111/ppl.13338	journal	February 2021
Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome Carrión, Víctor J.; Perez-Jaramillo, Juan; Cordovez, Viviane Science, Vol. 366, Issue 6465 https://doi.org/10.1126/science.aaw9285	journal	October 2019
Harnessing rhizosphere microbiomes for drought-resilient crop production de Vries, Franciska T.; Griffiths, Rob I.; Knight, Christopher G. Science, Vol. 368, Issue 6488 https://doi.org/10.1126/science.aaz5192	journal	April 2020
Deciphering the Root Endosphere Microbiome of the Desert Plant Alhagi sparsifolia for Drought Resistance-Promoting Bacteria Zhang, Lei; Zhang, Weipeng; Li, Qiqi Applied and Environmental Microbiology, Vol. 86, Issue 11 https://doi.org/10.1128/AEM.02863-19	journal	May 2020
A Meta-Analysis Approach to Defining the Culturable Core of Plant Endophytic Bacterial Communities Riva, Valentina; Mapelli, Francesca; Bagnasco, Agnese Applied and Environmental Microbiology, Vol. 88, Issue 6 https://doi.org/10.1128/aem.02537-21	journal	March 2022
Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes Santos-Medellín, Christian; Edwards, Joseph; Liechty, Zachary mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mBio.00764-17	journal	July 2017
Influence of Plant Fraction, Soil, and Plant Species on Microbiota: a Multikingdom Comparison Tkacz, Andrzej; Bestion, Eloïne; Bo, Zhiyan mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mBio.02785-19	journal	February 2020
Abiotic Stresses Shift Belowground Populus-Associated Bacteria Toward a Core Stress Microbiome Timm, Collin M.; Carter, Kelsey R.; Carrell, Alyssa A. mSystems, Vol. 3, Issue 1 https://doi.org/10.1128/mSystems.00070-17	journal	January 2018
Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought Veach, Allison M.; Chen, Huaihai; Yang, Zamin K. mSystems, Vol. 5, Issue 3 https://doi.org/10.1128/mSystems.00092-20	journal	June 2020
Unifying Species Diversity, Phylogenetic Diversity, Functional Diversity, and Related Similarity and Differentiation Measures Through Hill Numbers Chao, Anne; Chiu, Chun-Huo; Jost, Lou Annual Review of Ecology, Evolution, and Systematics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-ecolsys-120213-091540	journal	November 2014
The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome Cregger, M. A.; Veach, A. M.; Yang, Z. K. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0413-8	journal	February 2018
Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin Bokulich, Nicholas A.; Kaehler, Benjamin D.; Rideout, Jai Ram Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0470-z	journal	May 2018
Soil origin and plant genotype structure distinct microbiome compartments in the model legume Medicago truncatula Brown, Shawn P.; Grillo, Michael A.; Podowski, Justin C. Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00915-9	journal	September 2020
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
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
Host Genotype Shapes the Foliar Fungal Microbiome of Balsam Poplar (Populus balsamifera) Bálint, Miklós; Tiffin, Peter; Hallström, Björn PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053987	journal	January 2013
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Heat and Drought Stresses in Crops and Approaches for Their Mitigation Lamaoui, Mouna; Jemo, Martin; Datla, Raju Frontiers in Chemistry, Vol. 6 https://doi.org/10.3389/fchem.2018.00026	journal	February 2018
The Effects of Cropping Regimes on Fungal and Bacterial Communities of Wheat and Faba Bean in a Greenhouse Pot Experiment Differ between Plant Species and Compartment Granzow, Sandra; Kaiser, Kristin; Wemheuer, Bernd Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00902	journal	May 2017
Current Insights into the Role of Rhizosphere Bacteria in Disease Suppressive Soils Gómez Expósito, Ruth; de Bruijn, Irene; Postma, Joeke Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02529	journal	December 2017
Drought Legacy Effects on the Composition of Soil Fungal and Prokaryote Communities Meisner, Annelein; Jacquiod, Samuel; Snoek, Basten L. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00294	journal	March 2018
Pea (Pisum sativum l.) Plant Shapes Its Rhizosphere Microbiome for Nutrient Uptake and Stress Amelioration in Acidic Soils of the North-East Region of India Chaudhari, Diptaraj; Rangappa, Krishnappa; Das, Anup Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00968	journal	June 2020
Microbiome Variation Across Two Hemlock Species With Hemlock Woolly Adelgid Infestation Dove, Nicholas C.; Rogers, Timothy J.; Leppanen, Christy Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01528	journal	July 2020
Effects of Rare Microbiome Taxa Filtering on Statistical Analysis Cao, Quy; Sun, Xinxin; Rajesh, Karun Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.607325	journal	January 2021
Microbe to Microbiome: A Paradigm Shift in the Application of Microorganisms for Sustainable Agriculture Ray, Prasun; Lakshmanan, Venkatachalam; Labbé, Jessy L. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.622926	journal	December 2020
Drought Stress and Root-Associated Bacterial Communities Naylor, Dan; Coleman-Derr, Devin Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02223	journal	January 2018
Effect of Long-Term Farming Practices on Agricultural Soil Microbiome Members Represented by Metagenomically Assembled Genomes (MAGs) and Their Predicted Plant-Beneficial Genes Nelkner, Johanna; Henke, Christian; Lin, Timo Wentong Genes, Vol. 10, Issue 6 https://doi.org/10.3390/genes10060424	journal	June 2019
Drought Influences Fungal Community Dynamics in the Grapevine Rhizosphere and Root Microbiome Carbone, María Julia; Alaniz, Sandra; Mondino, Pedro Journal of Fungi, Vol. 7, Issue 9 https://doi.org/10.3390/jof7090686	journal	August 2021
Microbial Diversity of Upland Rice Roots and Their Influence on Rice Growth and Drought Tolerance Pang, Zhiqiang; Zhao, Ying; Xu, Peng Microorganisms, Vol. 8, Issue 9 https://doi.org/10.3390/microorganisms8091329	journal	August 2020
The role of abiotic factors modulating the plant-microbe-soil interactions: toward sustainable agriculture. A review Santoyo, Gustavo; Hernández-Pacheco, Claudia; Hernández-Salmerón, Julie Spanish Journal of Agricultural Research, Vol. 15, Issue 1 https://doi.org/10.5424/sjar/2017151-9990	journal	April 2017

Similar Records

Sweet Sorghum Genotypes Tolerant and Sensitive to Nitrogen Stress Select Distinct Root Endosphere and Rhizosphere Bacterial Communities

Journal Article · 2021 · Microorganisms · OSTI ID:1797618

Lopes, Lucas Dantas; Chai, Yen Ning; Marsh, Ellen L.; +3 more

Plant Hosts Modify Belowground Microbial Community Response to Extreme Drought

Journal Article · 2020 · mSystems · OSTI ID:1649570

Veach, Allison M.; Chen, Huaihai; Yang, Zamin Koo; +4 more

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

Journal Article · 2012 · PLoS ONE · OSTI ID:1097482

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

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (78)

Similar Records

Related Subjects