Interactions between plants and soil shaping the root microbiome under abiotic stress

Hartman, Kyle; Tringe, Susannah G.

doi:10.1042/bcj20180615

Title: Interactions between plants and soil shaping the root microbiome under abiotic stress

Journal Article · Fri Oct 11 00:00:00 EDT 2019 · Biochemical Journal

DOI:https://doi.org/10.1042/bcj20180615· OSTI ID:1572857

Hartman, Kyle ^[1];

^[2]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

AbstractPlants growing in soil develop close associations with soil microorganisms, which inhabit the areas around, on, and inside their roots. These microbial communities and their associated genes — collectively termed the root microbiome — are diverse and have been shown to play an important role in conferring abiotic stress tolerance to their plant hosts. In light of growing concerns over the threat of water and nutrient stress facing terrestrial ecosystems, especially those used for agricultural production, increased emphasis has been placed on understanding how abiotic stress conditions influence the composition and functioning of the root microbiome and the ultimate consequences for plant health. However, the composition of the root microbiome under abiotic stress conditions will not only reflect shifts in the greater bulk soil microbial community from which plants recruit their root microbiome but also plant responses to abiotic stress, which include changes in root exudate profiles and morphology. Exploring the relative contributions of these direct and plant-mediated effects on the root microbiome has been the focus of many studies in recent years. Here, we review the impacts of abiotic stress affecting terrestrial ecosystems, specifically flooding, drought, and changes in nitrogen and phosphorus availability, on bulk soil microbial communities and plants that interact to ultimately shape the root microbiome. We conclude with a perspective outlining possible directions for future research needed to advance our understanding of the complex molecular and biochemical interactions between soil, plants, and microbes that ultimately determine the composition of the root microbiome under abiotic stress.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Nebraska, Lincoln, NE (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0014395

OSTI ID:: 1572857

Alternate ID(s):: OSTI ID: 1775455

Journal Information:: Biochemical Journal, Vol. 476, Issue 19; ISSN 0264-6021

Publisher:: Biochemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 134 works

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References (207)

Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat Hamonts, Kelly; Clough, Tim J.; Stewart, Alison FEMS Microbiology Ecology, Vol. 83, Issue 3 https://doi.org/10.1111/1574-6941.12015	journal	October 2012
Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants Reddy, Attipalli Ramachandra; Chaitanya, Kolluru Viswanatha; Vivekanandan, Munusamy Journal of Plant Physiology, Vol. 161, Issue 11 https://doi.org/10.1016/j.jplph.2004.01.013	journal	November 2004
Design of synthetic bacterial communities for predictable plant phenotypes Herrera Paredes, Sur; Gao, Tianxiang; Law, Theresa F. PLOS Biology, Vol. 16, Issue 2 https://doi.org/10.1371/journal.pbio.2003962	journal	February 2018
Ethanol Concentration in Tomato Plants during Soil Flooding1 Bolton, E. F.; Erickson, A. E. Agronomy Journal, Vol. 62, Issue 2 https://doi.org/10.2134/agronj1970.00021962006200020013x	journal	January 1970
Roles, Regulation, and Agricultural Application of Plant Phosphate Transporters Wang, Duoliya; Lv, Sulian; Jiang, Ping Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00817	journal	May 2017
Phosphorus availability and microbial community in the rhizosphere of intercropped cereal and legume along a P-fertilizer gradient Tang, Xiaoyan; Placella, Sarah A.; Daydé, Florent Plant and Soil, Vol. 407, Issue 1-2 https://doi.org/10.1007/s11104-016-2949-3	journal	June 2016
Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture Berg, Gabriele Applied Microbiology and Biotechnology, Vol. 84, Issue 1 https://doi.org/10.1007/s00253-009-2092-7	journal	July 2009
Plant‐mediated effects of soil phosphorus on the root‐associated fungal microbiota in Arabidopsis thaliana Fabiańska, Izabela; Gerlach, Nina; Almario, Juliana New Phytologist, Vol. 221, Issue 4 https://doi.org/10.1111/nph.15538	journal	November 2018
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
Petunia- and Arabidopsis-Specific Root Microbiota Responses to Phosphate Supplementation Bodenhausen, Natacha; Somerville, Vincent; Desirò, Alessandro Phytobiomes Journal, Vol. 3, Issue 2 https://doi.org/10.1094/pbiomes-12-18-0057-r	journal	January 2019
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
Responses of woody plants to flooding and salinity Kozlowski, T. T. Tree Physiology, Vol. 17, Issue 7 https://doi.org/10.1093/treephys/17.7.490	journal	July 1997
Correction to: Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming Hartman, Kyle; van der Heijden, Marcel G. A.; Wittwer, Raphaël A. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0456-x	journal	April 2018
Responses of soil biological traits and bacterial communities to nitrogen fertilization mediate maize yields across three soil types Yu, Hailing; Ling, Ning; Wang, Tingting Soil and Tillage Research, Vol. 185 https://doi.org/10.1016/j.still.2018.08.017	journal	January 2019
Soil Microorganisms Mediating Phosphorus Availability Update on Microbial Phosphorus Richardson, Alan E.; Simpson, Richard J. Plant Physiology, Vol. 156, Issue 3 https://doi.org/10.1104/pp.111.175448	journal	May 2011
Origin of diderm (Gram-negative) bacteria: antibiotic selection pressure rather than endosymbiosis likely led to the evolution of bacterial cells with two membranes Gupta, Radhey S. Antonie van Leeuwenhoek, Vol. 100, Issue 2 https://doi.org/10.1007/s10482-011-9616-8	journal	June 2011
Metabolite Profiling of Root Exudates of Common Bean under Phosphorus Deficiency Tawaraya, Keitaro; Horie, Ryota; Saito, Saki Metabolites, Vol. 4, Issue 3 https://doi.org/10.3390/metabo4030599	journal	July 2014
Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition Coskun, Devrim; Britto, Dev T.; Shi, Weiming Nature Plants, Vol. 3, Issue 6 https://doi.org/10.1038/nplants.2017.74	journal	June 2017
Response of microbial communities to water stress in irrigated and drought-prone tallgrass prairie soils Williams, Mark A. Soil Biology and Biochemistry, Vol. 39, Issue 11 https://doi.org/10.1016/j.soilbio.2007.05.025	journal	November 2007
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
Nitrification Inhibition by Monoterpenoids: Theoretical Mode of Action Based on Molecular Structures White, Carleton S. Ecology, Vol. 69, Issue 5 https://doi.org/10.2307/1941663	journal	October 1988
Impact of flooding on soil bacterial communities associated with poplar (Populus sp.) trees Graff, Andrea; Conrad, Ralf FEMS Microbiology Ecology, Vol. 53, Issue 3 https://doi.org/10.1016/j.femsec.2005.01.009	journal	August 2005
Rice rhizodeposition and its utilization by microbial groups depends on N fertilization Ge, Tida; Li, Baozhen; Zhu, Zhenke Biology and Fertility of Soils, Vol. 53, Issue 1 https://doi.org/10.1007/s00374-016-1155-z	journal	October 2016
Morphological Responses of Sugarcane to Long-Term Flooding Gilbert, Robert A.; Rainbolt, Curtis R.; Morris, Dolen R. Agronomy Journal, Vol. 99, Issue 6 https://doi.org/10.2134/agronj2007.0085	journal	January 2007
Understanding and exploiting plant beneficial microbes Finkel, Omri M.; Castrillo, Gabriel; Herrera Paredes, Sur Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.018	journal	August 2017
Linking rhizosphere microbiome composition of wild and domesticated Phaseolus vulgaris to genotypic and root phenotypic traits Pérez-Jaramillo, Juan E.; Carrión, Víctor J.; Bosse, Mirte The ISME Journal, Vol. 11, Issue 10 https://doi.org/10.1038/ismej.2017.85	journal	June 2017
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1508382112	journal	August 2015
Global flood risk under climate change Hirabayashi, Yukiko; Mahendran, Roobavannan; Koirala, Sujan Nature Climate Change, Vol. 3, Issue 9 https://doi.org/10.1038/nclimate1911	journal	June 2013
Going back to the roots: the microbial ecology of the rhizosphere Philippot, Laurent; Raaijmakers, Jos M.; Lemanceau, Philippe Nature Reviews Microbiology, Vol. 11, Issue 11 https://doi.org/10.1038/nrmicro3109	journal	September 2013
Phosphorus Uptake by Plants: From Soil to Cell Schachtman, Daniel P.; Reid, Robert J.; Ayling, S. M. Plant Physiology, Vol. 116, Issue 2 https://doi.org/10.1104/pp.116.2.447	journal	February 1998
Inorganic Nitrogen Application Affects Both Taxonomical and Predicted Functional Structure of Wheat Rhizosphere Bacterial Communities Kavamura, Vanessa N.; Hayat, Rifat; Clark, Ian M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01074	journal	May 2018
Impact of root system architecture on rhizosphere and root microbiome Saleem, Muhammad; Law, Audrey D.; Sahib, Mohammad Radhi Rhizosphere, Vol. 6 https://doi.org/10.1016/j.rhisph.2018.02.003	journal	June 2018
Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil: Summer drought effects on heathland fungi Toberman, Hannah; Freeman, Chris; Evans, Chris FEMS Microbiology Ecology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1574-6941.2008.00560.x	journal	November 2008
Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S. The ISME Journal, Vol. 6, Issue 5 https://doi.org/10.1038/ismej.2011.159	journal	December 2011
Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe Peñuelas, Josep; Poulter, Benjamin; Sardans, Jordi Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3934	journal	December 2013
AMF-induced tolerance to drought stress in citrus: A review Wu, Qiang-Sheng; Srivastava, A. K.; Zou, Ying-Ning Scientia Horticulturae, Vol. 164 https://doi.org/10.1016/j.scienta.2013.09.010	journal	December 2013
Linking Plant Nutritional Status to Plant-Microbe Interactions Carvalhais, Lilia C.; Dennis, Paul G.; Fan, Ben PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0068555	journal	July 2013
Roots Shaping Their Microbiome: Global Hotspots for Microbial Activity Reinhold-Hurek, Barbara; Bünger, Wiebke; Burbano, Claudia Sofía Annual Review of Phytopathology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev-phyto-082712-102342	journal	August 2015
Plant growth promotion by phosphate solubilizing fungi – current perspective Khan, Mohammad Saghir; Zaidi, Almas; Ahemad, Munees Archives of Agronomy and Soil Science, Vol. 56, Issue 1 https://doi.org/10.1080/03650340902806469	journal	February 2010
Changes in Crested Wheatgrass Root Exudation Caused by Flood, Drought, and Nutrient Stress Henry, Amelia; Doucette, William; Norton, Jeanette Journal of Environment Quality, Vol. 36, Issue 3 https://doi.org/10.2134/jeq2006.0425sc	journal	January 2007
Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents Ochoa-Hueso, Raúl; Collins, Scott L.; Delgado-Baquerizo, Manuel Global Change Biology, Vol. 24, Issue 7 https://doi.org/10.1111/gcb.14113	journal	March 2018
High-Throughput Single-Cell Transcriptome Profiling of Plant Cell Types Shulse, Christine N.; Cole, Benjamin J.; Ciobanu, Doina Cell Reports, Vol. 27, Issue 7 https://doi.org/10.1016/j.celrep.2019.04.054	journal	May 2019
Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil Chhabra, Sagar; Brazil, Dina; Morrissey, John Biology and Fertility of Soils, Vol. 49, Issue 1 https://doi.org/10.1007/s00374-012-0693-2	journal	May 2012
Root exudation and rhizoplane bacterial abundance of barley (Hordeum vulgare L.) in relation to nitrogen fertilization and root growth Liljeroth, E.; Bååth, E.; Mathiasson, I. Plant and Soil, Vol. 127, Issue 1 https://doi.org/10.1007/BF00010839	journal	September 1990
Root traits contributing to plant productivity under drought Comas, Louise H.; Becker, Steven R.; Cruz, Von Mark V. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00442	journal	January 2013
Phosphorus: a limiting nutrient for humanity? Elser, James J. Current Opinion in Biotechnology, Vol. 23, Issue 6 https://doi.org/10.1016/j.copbio.2012.03.001	journal	December 2012
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
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature, Vol. 408, Issue 6814, p. 796-815 https://doi.org/10.1038/35048692	journal	December 2000
1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation Barnawal, Deepti; Bharti, Nidhi; Maji, Deepamala Plant Physiology and Biochemistry, Vol. 58 https://doi.org/10.1016/j.plaphy.2012.07.008	journal	September 2012
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species Coleman-Derr, Devin; Desgarennes, Damaris; Fonseca-Garcia, Citlali New Phytologist, Vol. 209, Issue 2 https://doi.org/10.1111/nph.13697	journal	October 2015
Aerenchyma Formation and Recovery from Hypoxia of the Flooded Root System of Nodulated Soybean Thomas, A. L.; Guerreiro, S. M. C.; Sodek, L. Annals of Botany, Vol. 96, Issue 7 https://doi.org/10.1093/aob/mci272	journal	September 2005
Understanding: the Drought Phenomenon: The Role of Definitions Wilhite, Donald A.; Glantz, Michael H. Water International, Vol. 10, Issue 3 https://doi.org/10.1080/02508068508686328	journal	January 1985
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
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
Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems Ramirez, Kelly S.; Lauber, Christian L.; Knight, Rob Ecology, Vol. 91, Issue 12 https://doi.org/10.1890/10-0426.1	journal	December 2010
Tackling Plant Phosphate Starvation by the Roots Crombez, Hanne; Motte, Hans; Beeckman, Tom Developmental Cell, Vol. 48, Issue 5 https://doi.org/10.1016/j.devcel.2019.01.002	journal	March 2019
Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales Smith, Sally E.; Smith, F. Andrew Annual Review of Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev-arplant-042110-103846	journal	June 2011
Metabolite profiling of pea roots in response to phosphate availability Laparre, Jérôme; Balzergue, Coline; Rochange, Soizic Plant Signaling & Behavior, Vol. 6, Issue 6 https://doi.org/10.4161/psb.6.6.15168	journal	June 2011
Metabolite Profiling of Shoot Extracts, root Extracts, and root Exudates of rice Plant Under Phosphorus Deficiency Tawaraya, Keitaro; Horie, Ryota; Saito, Akiko Journal of Plant Nutrition, Vol. 36, Issue 7 https://doi.org/10.1080/01904167.2013.780613	journal	January 2013
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Trends in Plant Science, Vol. 23, Issue 1 https://doi.org/10.1016/j.tplants.2017.09.003	journal	January 2018
Plant-Growth-Promoting Rhizobacteria Lugtenberg, Ben; Kamilova, Faina Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.162918	journal	October 2009
Phosphate solubilizing bacteria and their role in plant growth promotion Rodrı́guez, Hilda; Fraga, Reynaldo Biotechnology Advances, Vol. 17, Issue 4-5 https://doi.org/10.1016/S0734-9750(99)00014-2	journal	October 1999
Improved Cytoplasmic pH Regulation, Increased Lactate Efflux, and Reduced Cytoplasmic Lactate Levels Are Biochemical Traits Expressed in Root Tips of Whole Maize Seedlings Acclimated to a Low-Oxygen Environment Xia, J. H.; Roberts, Jkm. Plant Physiology, Vol. 105, Issue 2 https://doi.org/10.1104/pp.105.2.651	journal	June 1994
The Plant Microbiome at Work Schlaeppi, Klaus; Bulgarelli, Davide Molecular Plant-Microbe Interactions, Vol. 28, Issue 3 https://doi.org/10.1094/MPMI-10-14-0334-FI	journal	March 2015
Succession of bacterial community structure and diversity in a paddy soil oxygen gradient Noll, Matthias; Matthies, Diethart; Frenzel, Peter Environmental Microbiology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1462-2920.2005.00700.x	journal	March 2005
Drought-resistant fungi control soil organic matter decomposition and its response to temperature: FUNGAL DIVERSITY CONTROL OVER SOIL C BALANCE Yuste, J. C.; PeÑUelas, J.; Estiarte, M. Global Change Biology, Vol. 17, Issue 3 https://doi.org/10.1111/j.1365-2486.2010.02300.x	journal	September 2010
Phosphate sensing in higher plants Abel, Steffen; Ticconi, Carla A.; Delatorre, Carla A. Physiologia Plantarum, Vol. 115, Issue 1 https://doi.org/10.1034/j.1399-3054.2002.1150101.x	journal	May 2002
Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field-grown maize roots Yu, Peng; Wang, Chao; Baldauf, Jutta A. New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14893	journal	November 2017
Highly Parallel Genome-wide Expression Profiling of Individual Cells Using Nanoliter Droplets Macosko, Evan Z.; Basu, Anindita; Satija, Rahul Cell, Vol. 161, Issue 5 https://doi.org/10.1016/j.cell.2015.05.002	journal	May 2015
Factors Influencing Oxygen Consumption Rates in Flooded Soils1 Reddy, K. R.; Rao, P. S. C.; Patrick, W. H. Soil Science Society of America Journal, Vol. 44, Issue 4 https://doi.org/10.2136/sssaj1980.03615995004400040016x	journal	January 1980
How plants cope with complete submergence Voesenek, L. A. C. J.; Colmer, T. D.; Pierik, R. New Phytologist, Vol. 170, Issue 2 https://doi.org/10.1111/j.1469-8137.2006.01692.x	journal	April 2006
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
Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize Zhu, Shusheng; Vivanco, Jorge M.; Manter, Daniel K. Applied Soil Ecology, Vol. 107 https://doi.org/10.1016/j.apsoil.2016.07.009	journal	November 2016
The global nitrogen cycle in the twenty-first century Fowler, David; Coyle, Mhairi; Skiba, Ute Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621 https://doi.org/10.1098/rstb.2013.0164	journal	July 2013
The Root-Colonizing Endophyte Pirifomospora indica Confers Drought Tolerance in Arabidopsis by Stimulating the Expression of Drought Stress–Related Genes in Leaves Sherameti, Irena; Tripathi, Swati; Varma, Ajit Molecular Plant-Microbe Interactions, Vol. 21, Issue 6 https://doi.org/10.1094/MPMI-21-6-0799	journal	June 2008
The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events Balzergue, Coline; Puech-Pagès, Virginie; Bécard, Guillaume Journal of Experimental Botany, Vol. 62, Issue 3 https://doi.org/10.1093/jxb/erq335	journal	November 2010
Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale Lauber, C. L.; Hamady, M.; Knight, R. Applied and Environmental Microbiology, Vol. 75, Issue 15 https://doi.org/10.1128/AEM.00335-09	journal	June 2009
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots Colmer, T. D. Plant, Cell and Environment, Vol. 26, Issue 1 https://doi.org/10.1046/j.1365-3040.2003.00846.x	journal	January 2003
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
Microbial interactions and biocontrol in the rhizosphere Whipps, John M. Journal of Experimental Botany, Vol. 52, Issue suppl_1 https://doi.org/10.1093/jxb/52.suppl_1.487	journal	March 2001
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
Drought stress and reactive oxygen species: production, scavenging and signaling Cruz de Carvalho, Maria Helena Plant Signaling & Behavior, Vol. 3, Issue 3 https://doi.org/10.4161/psb.3.3.5536	journal	March 2008
Strigolactones Stimulate Arbuscular Mycorrhizal Fungi by Activating Mitochondria Besserer, Arnaud; Puech-Pagès, Virginie; Kiefer, Patrick PLoS Biology, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pbio.0040226	journal	June 2006
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
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105159	journal	June 2006
Climate change effects on beneficial plant-microorganism interactions: Climate change and beneficial plant-microorganism interactions Compant, Stéphane; Van Der Heijden, Marcel G. A.; Sessitsch, Angela FEMS Microbiology Ecology https://doi.org/10.1111/j.1574-6941.2010.00900.x	journal	May 2010
Effect of nitrogen and phosphorus fertilization on the composition of rhizobacterial communities of two Chilean Andisol pastures Jorquera, Milko A.; Martínez, Oscar A.; Marileo, Luis G. World Journal of Microbiology and Biotechnology, Vol. 30, Issue 1 https://doi.org/10.1007/s11274-013-1427-9	journal	July 2013
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
The Endophytic Bacterial Microbiota Associated with Sweet Sorghum ( Sorghum bicolor ) Is Modulated by the Application of Chemical N Fertilizer to the Field Mareque, Cintia; da Silva, Thais Freitas; Vollú, Renata Estebanez International Journal of Genomics, Vol. 2018 https://doi.org/10.1155/2018/7403670	journal	September 2018
Signaling in the Arbuscular Mycorrhizal Symbiosis Harrison, Maria J. Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.58.030603.123749	journal	October 2005
Regulation and function of root exudates Badri, Dayakar V.; Vivanco, Jorge M. Plant, Cell & Environment, Vol. 32, Issue 6 https://doi.org/10.1111/j.1365-3040.2009.01926.x	journal	June 2009
Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Haase, Susan; Neumann, Günter; Kania, Angelika Soil Biology and Biochemistry, Vol. 39, Issue 9 https://doi.org/10.1016/j.soilbio.2007.03.014	journal	September 2007
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa Lebeis, S. L.; Paredes, S. H.; Lundberg, D. S. Science, Vol. 349, Issue 6250 https://doi.org/10.1126/science.aaa8764	journal	July 2015
The influence of soil properties on the structure of bacterial and fungal communities across land-use types Lauber, Christian L.; Strickland, Michael S.; Bradford, Mark A. Soil Biology and Biochemistry, Vol. 40, Issue 9 https://doi.org/10.1016/j.soilbio.2008.05.021	journal	September 2008
Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research Hartmann, Anton; Rothballer, Michael; Schmid, Michael Plant and Soil, Vol. 312, Issue 1-2 https://doi.org/10.1007/s11104-007-9514-z	journal	December 2007
Soil Nitrogen Availability and Plant Genotype Modify the Nutrition Strategies of M. truncatula and the Associated Rhizosphere Microbial Communities Zancarini, Anouk; Mougel, Christophe; Voisin, Anne-Sophie PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0047096	journal	October 2012
Structure and Function of the Bacterial Root Microbiota in Wild and Domesticated Barley Bulgarelli, Davide; Garrido-Oter, Ruben; Münch, Philipp C. Cell Host & Microbe, Vol. 17, Issue 3 https://doi.org/10.1016/j.chom.2015.01.011	journal	March 2015
The Rules of Engagement in the Legume-Rhizobial Symbiosis Oldroyd, Giles E. D.; Murray, Jeremy D.; Poole, Philip S. Annual Review of Genetics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-genet-110410-132549	journal	December 2011
Role of Arbuscular Mycorrhizal Fungi in Uptake of Phosphorus and Nitrogen From Soil George, Eckhard; Marschner, Horst; Jakobsen, Iver Critical Reviews in Biotechnology, Vol. 15, Issue 3-4 https://doi.org/10.3109/07388559509147412	journal	January 1995
The plant microbiome Turner, Thomas R.; James, Euan K.; Poole, Philip S. Genome Biology, Vol. 14, Issue 6 https://doi.org/10.1186/gb-2013-14-6-209	journal	June 2013
Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource Vance, Carroll P.; Uhde-Stone, Claudia; Allan, Deborah L. New Phytologist, Vol. 157, Issue 3 https://doi.org/10.1046/j.1469-8137.2003.00695.x	journal	March 2003
Peak Phosphorus: Clarifying the Key Issues of a Vigorous Debate about Long-Term Phosphorus Security Cordell, Dana; White, Stuart Sustainability, Vol. 3, Issue 10 https://doi.org/10.3390/su3102027	journal	October 2011
Drought-Induced Accumulation of Root Exudates Supports Post-drought Recovery of Microbes in Mountain Grassland Karlowsky, Stefan; Augusti, Angela; Ingrisch, Johannes Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01593	journal	November 2018
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
Transcriptome Profiling of the Endophyte Burkholderia phytofirmans PsJN Indicates Sensing of the Plant Environment and Drought Stress Sheibani-Tezerji, Raheleh; Rattei, Thomas; Sessitsch, Angela mBio, Vol. 6, Issue 5 https://doi.org/10.1128/mBio.00621-15	journal	September 2015
Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus‐acquisition strategies of 16 crop species Wen, Zhihui; Li, Hongbo; Shen, Qi New Phytologist, Vol. 223, Issue 2 https://doi.org/10.1111/nph.15833	journal	April 2019
How does phosphate status influence the development of the arbuscular mycorrhizal symbiosis? Gu, Mian; Chen, Aiqun; Dai, Xiaoli Plant Signaling & Behavior, Vol. 6, Issue 9 https://doi.org/10.4161/psb.6.9.16365	journal	September 2011
Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils Mander, Carolyn; Wakelin, Steve; Young, Sandra Soil Biology and Biochemistry, Vol. 44, Issue 1 https://doi.org/10.1016/j.soilbio.2011.09.009	journal	January 2012
Strigolactones: Chemical Signals for Fungal Symbionts and Parasitic Weeds in Plant Roots Akiyama, Kohki; Hayashi, Hideo Annals of Botany, Vol. 97, Issue 6 https://doi.org/10.1093/aob/mcl063	journal	March 2006
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed LeBauer, David S.; Treseder, Kathleen K. Ecology, Vol. 89, Issue 2 https://doi.org/10.1890/06-2057.1	journal	February 2008
Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17 Naveed, Muhammad; Mitter, Birgit; Reichenauer, Thomas G. Environmental and Experimental Botany, Vol. 97 https://doi.org/10.1016/j.envexpbot.2013.09.014	journal	January 2014
Rice roots and CH4 oxidation: the activity of bacteria, their distribution and the microenvironment Gilbert, Bettina; Frenzel, Peter Soil Biology and Biochemistry, Vol. 30, Issue 14 https://doi.org/10.1016/S0038-0717(98)00061-3	journal	December 1998
Toward an Ecological Classification of soil Bacteria Fierer, Noah; Bradford, Mark A.; Jackson, Robert B. Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/05-1839	journal	June 2007
The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots York, Larry M.; Carminati, Andrea; Mooney, Sacha J. Journal of Experimental Botany, Vol. 67, Issue 12 https://doi.org/10.1093/jxb/erw108	journal	March 2016
Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling Hodge, A.; Fitter, A. H. Proceedings of the National Academy of Sciences, Vol. 107, Issue 31 https://doi.org/10.1073/pnas.1005874107	journal	July 2010
Changes in root-associated microbial communities are determined by species-specific plant growth responses to stress and disturbance Bouasria, Abderrahim; Mustafa, Tarfa; De Bello, Francesco European Journal of Soil Biology, Vol. 52 https://doi.org/10.1016/j.ejsobi.2012.06.003	journal	September 2012
Giving back to the community: microbial mechanisms of plant-soil interactions Herrera Paredes, Sur; Lebeis, Sarah L. Functional Ecology, Vol. 30, Issue 7 https://doi.org/10.1111/1365-2435.12684	journal	June 2016
Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency Carvalhais, Lilia C.; Dennis, Paul G.; Fedoseyenko, Dmitri Journal of Plant Nutrition and Soil Science, Vol. 174, Issue 1 https://doi.org/10.1002/jpln.201000085	journal	December 2010
Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes Gage, D. J. Microbiology and Molecular Biology Reviews, Vol. 68, Issue 2 https://doi.org/10.1128/MMBR.68.2.280-300.2004	journal	June 2004
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
Root-Associated Bacterial and Fungal Community Profiles of Arabidopsis thaliana Are Robust Across Contrasting Soil P Levels Robbins, Chanz; Thiergart, Thorsten; Hacquard, Stéphane Phytobiomes Journal, Vol. 2, Issue 1 https://doi.org/10.1094/pbiomes-09-17-0042-r	journal	January 2018
Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis Augé, Robert M. Mycorrhiza, Vol. 11, Issue 1 https://doi.org/10.1007/s005720100097	journal	May 2001
The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application: N fertilizer and sugarcane root microbiota Yeoh, Yun Kit; Paungfoo-Lonhienne, Chanyarat; Dennis, Paul G. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.12925	journal	July 2015
Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat Kawasaki, Akitomo; Donn, Suzanne; Ryan, Peter R. PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0164533	journal	October 2016
Plant species and nitrogen effects on soil biological properties of temperate upland grasslands Bardgett, R. D.; Mawdsley, J. L.; Edwards, S. Functional Ecology, Vol. 13, Issue 5 https://doi.org/10.1046/j.1365-2435.1999.00362.x	journal	October 1999
Secondary Succession and the Pattern of Plant Dominance Along Experimental Nitrogen Gradients Tilman, David Ecological Monographs, Vol. 57, Issue 3 https://doi.org/10.2307/2937080	journal	February 1987
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z. Ecological Applications, Vol. 20, Issue 1 https://doi.org/10.1890/08-0127.1	journal	January 2010
Microbial Stress-Response Physiology and its Implications for Ecosystem Function Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/06-0219	journal	June 2007
Ethylene - and oxygen signalling - drive plant survival during flooding Voesenek, L. A. C. J.; Sasidharan, R. Plant Biology, Vol. 15, Issue 3 https://doi.org/10.1111/plb.12014	journal	April 2013
Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization Compant, Stéphane; Clément, Christophe; Sessitsch, Angela Soil Biology and Biochemistry, Vol. 42, Issue 5 https://doi.org/10.1016/j.soilbio.2009.11.024	journal	May 2010
Nitrogen Cycles: Past, Present, and Future Galloway, J. N.; Dentener, F. J.; Capone, D. G. Biogeochemistry, Vol. 70, Issue 2 https://doi.org/10.1007/s10533-004-0370-0	journal	September 2004
Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere Paungfoo-Lonhienne, Chanyarat; Yeoh, Yun Kit; Kasinadhuni, Naga Rup Pinaki Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08678	journal	March 2015
The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms Raaijmakers, Jos M.; Paulitz, Timothy C.; Steinberg, Christian Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-008-9568-6	journal	February 2008
Role of root microbiota in plant productivity Tkacz, A.; Poole, P. Journal of Experimental Botany, Vol. 66, Issue 8 https://doi.org/10.1093/jxb/erv157	journal	April 2015
Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition Wang, Chao; Liu, Dongwei; Bai, Edith Soil Biology and Biochemistry, Vol. 120 https://doi.org/10.1016/j.soilbio.2018.02.003	journal	May 2018
A plant perspective on nitrogen cycling in the rhizosphere Moreau, Delphine; Bardgett, Richard D.; Finlay, Roger D. Functional Ecology, Vol. 33, Issue 4 https://doi.org/10.1111/1365-2435.13303	journal	March 2019
Nitrogen- and phosphorus-starved Triticum aestivum show distinct belowground microbiome profiles Pagé, Antoine P.; Tremblay, Julien; Masson, Luke PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0210538	journal	February 2019
Cultivar and phosphorus effects on switchgrass yield and rhizosphere microbial diversity Sawyer, Anne; Staley, Christopher; Lamb, John Applied Microbiology and Biotechnology, Vol. 103, Issue 4 https://doi.org/10.1007/s00253-018-9535-y	journal	December 2018
Long-Term Rock Phosphate Fertilization Impacts the Microbial Communities of Maize Rhizosphere Silva, Ubiana C.; Medeiros, Julliane D.; Leite, Laura R. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01266	journal	July 2017
The Plant Microbiota: Systems-Level Insights and Perspectives Müller, Daniel B.; Vogel, Christine; Bai, Yang Annual Review of Genetics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-genet-120215-034952	journal	November 2016
Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase Glick, Bernard R. FEMS Microbiology Letters, Vol. 251, Issue 1 https://doi.org/10.1016/j.femsle.2005.07.030	journal	October 2005
Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria Xu, Ling; Naylor, Dan; Dong, Zhaobin Proceedings of the National Academy of Sciences, Vol. 115, Issue 18 https://doi.org/10.1073/pnas.1717308115	journal	April 2018
Carbon flow in the rhizosphere: carbon trading at the soil–root interface Jones, D. L.; Nguyen, C.; Finlay, R. D. Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-009-9925-0	journal	February 2009
Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems Hodge, Angela; Storer, Kate Plant and Soil, Vol. 386, Issue 1-2 https://doi.org/10.1007/s11104-014-2162-1	journal	June 2014
Nutrient Imbalances in Agricultural Development Vitousek, P. M.; Naylor, R.; Crews, T. Science, Vol. 324, Issue 5934 https://doi.org/10.1126/science.1170261	journal	June 2009
Aerenchyma formation in crop species: A review Yamauchi, Takaki; Shimamura, Satoshi; Nakazono, Mikio Field Crops Research, Vol. 152 https://doi.org/10.1016/j.fcr.2012.12.008	journal	October 2013
Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli Canarini, Alberto; Kaiser, Christina; Merchant, Andrew Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00157	journal	February 2019
Anaerobic stimulation of root exudates and disease of peas Smucker, A. J. M.; Erickson, A. E. Plant and Soil, Vol. 99, Issue 2-3 https://doi.org/10.1007/BF02370887	journal	June 1987
Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes Schimel, Joshua P. Annual Review of Ecology, Evolution, and Systematics, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062614	journal	November 2018
Bacterial Modulation of Plant Ethylene Levels Gamalero, Elisa; Glick, Bernard R. Plant Physiology, Vol. 169, Issue 1 https://doi.org/10.1104/pp.15.00284	journal	April 2015
Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes Ramirez, Kelly S.; Craine, Joseph M.; Fierer, Noah Global Change Biology, Vol. 18, Issue 6 https://doi.org/10.1111/j.1365-2486.2012.02639.x	journal	February 2012
Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S. Molecular Ecology, Vol. 23, Issue 13 https://doi.org/10.1111/mec.12821	journal	June 2014
Thirsty tree roots exude more carbon Preece, Catherine; Farré-Armengol, Gerard; Llusià, Joan Tree Physiology, Vol. 38, Issue 5 https://doi.org/10.1093/treephys/tpx163	journal	January 2018
Unraveling the role of fungal symbionts in plant abiotic stress tolerance Singh, Lamabam Peter; Gill, Sarvajeet Singh; Tuteja, Narendra Plant Signaling & Behavior, Vol. 6, Issue 2 https://doi.org/10.4161/psb.6.2.14146	journal	February 2011
Phosphate Acquisition Raghothama, K. G. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.665	journal	June 1999
Rhizosphere Oxidation in Rice and other Species: A Mathematical Model Based on the Oxygen Flux Component Armstrong, W. Physiologia Plantarum, Vol. 23, Issue 3 https://doi.org/10.1111/j.1399-3054.1970.tb06455.x	journal	June 1970
Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants Koyama, Akihiro; Steinweg, J. Megan; Haddix, Michelle L. FEMS Microbiology Ecology, Vol. 94, Issue 1 https://doi.org/10.1093/femsec/fix156	journal	November 2017
Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event Fuchslueger, Lucia; Bahn, Michael; Hasibeder, Roland Journal of Ecology, Vol. 104, Issue 5 https://doi.org/10.1111/1365-2745.12593	journal	May 2016
Changes in precipitation with climate change Trenberth, Ke Climate Research, Vol. 47, Issue 1 https://doi.org/10.3354/cr00953	journal	March 2011
Biological costs and benefits to plant–microbe interactions in the rhizosphere Morgan, J. A. W.; Bending, G. D.; White, P. J. Journal of Experimental Botany, Vol. 56, Issue 417 https://doi.org/10.1093/jxb/eri205	journal	May 2005
Sampling root exudates – Mission impossible? Oburger, Eva; Jones, David L. Rhizosphere, Vol. 6 https://doi.org/10.1016/j.rhisph.2018.06.004	journal	June 2018
Mycorrhizal ecology and evolution: the past, the present, and the future van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13288	journal	February 2015
Agricultural sustainability and intensive production practices Tilman, David; Cassman, Kenneth G.; Matson, Pamela A. Nature, Vol. 418, Issue 6898 https://doi.org/10.1038/nature01014	journal	August 2002
Responses of soil total microbial biomass and community compositions to rainfall reductions Ren, Chengjie; Chen, Ji; Lu, Xingjie Soil Biology and Biochemistry, Vol. 116 https://doi.org/10.1016/j.soilbio.2017.09.028	journal	January 2018
Plant Responses to Flooding of Soil Kozlowski, T. T. BioScience, Vol. 34, Issue 3 https://doi.org/10.2307/1309751	journal	March 1984
Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency Kant, S.; Bi, Y. -M.; Rothstein, S. J. Journal of Experimental Botany, Vol. 62, Issue 4 https://doi.org/10.1093/jxb/erq297	journal	October 2010
Nicotiana Roots Recruit Rare Rhizosphere Taxa as Major Root-Inhabiting Microbes Saleem, Muhammad; Law, Audrey D.; Moe, Luke A. Microbial Ecology, Vol. 71, Issue 2 https://doi.org/10.1007/s00248-015-0672-x	journal	September 2015
Differences in Root Exudation Among Phosphorus‐Starved Genotypes of Maize and Green Gram and Its Relationship with Phosphorus Uptake Singh, Bhupinder; Pandey, Renu Journal of Plant Nutrition, Vol. 26, Issue 12 https://doi.org/10.1081/PLN-120025467	journal	November 2003
The under-recognized dominance of Verrucomicrobia in soil bacterial communities Bergmann, Gaddy T.; Bates, Scott T.; Eilers, Kathryn G. Soil Biology and Biochemistry, Vol. 43, Issue 7 https://doi.org/10.1016/j.soilbio.2011.03.012	journal	July 2011
The story of phosphorus: Global food security and food for thought Cordell, Dana; Drangert, Jan-Olof; White, Stuart Global Environmental Change, Vol. 19, Issue 2 https://doi.org/10.1016/j.gloenvcha.2008.10.009	journal	May 2009
Targeted genome modification of crop plants using a CRISPR-Cas system Shan, Qiwei; Wang, Yanpeng; Li, Jun Nature Biotechnology, Vol. 31, Issue 8 https://doi.org/10.1038/nbt.2650	journal	August 2013
The Mineral Nutrition of Wild Plants Chapin, F. S. Annual Review of Ecology and Systematics, Vol. 11, Issue 1 https://doi.org/10.1146/annurev.es.11.110180.001313	journal	November 1980
Molecular and Cellular Aspects of the Arbuscular Mycorrhizal Symbiosis Harrison, Maria J. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.361	journal	June 1999
Plant-driven selection of microbes Hartmann, Anton; Schmid, Michael; Tuinen, Diederik van Plant and Soil, Vol. 321, Issue 1-2 https://doi.org/10.1007/s11104-008-9814-y	journal	November 2008
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees Shakya, Migun; Gottel, Neil; Castro, Hector PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076382	journal	October 2013
Root Endophyte Colletotrichum tofieldiae Confers Plant Fitness Benefits that Are Phosphate Status Dependent Hiruma, Kei; Gerlach, Nina; Sacristán, Soledad Cell, Vol. 165, Issue 2 https://doi.org/10.1016/j.cell.2016.02.028	journal	April 2016
Agricultural Intensification and Ecosystem Properties Matson, P. A. Science, Vol. 277, Issue 5325 https://doi.org/10.1126/science.277.5325.504	journal	July 1997
Soil bacterial and fungal communities across a pH gradient in an arable soil Rousk, Johannes; Bååth, Erland; Brookes, Philip C. The ISME Journal, Vol. 4, Issue 10 https://doi.org/10.1038/ismej.2010.58	journal	May 2010
Nitrogen Fixation in Cereals Rosenblueth, Mónica; Ormeño-Orrillo, Ernesto; López-López, Aline Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01794	journal	August 2018
Root-Associated Microbiome of Maize Genotypes with Contrasting Phosphorus Use Efficiency Gomes, Eliane A.; Lana, Ubiraci G. P.; Quensen, John F. Phytobiomes Journal, Vol. 2, Issue 3 https://doi.org/10.1094/PBIOMES-03-18-0012-R	journal	January 2018
Dark Septate Endophytic Fungi Help Tomato to Acquire Nutrients from Ground Plant Material Vergara, Carlos; Araujo, Karla E. C.; Urquiaga, Segundo Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02437	journal	December 2017
Resistance and resilience of root fungal communities to water limitation in a temperate agroecosystem Furze, Jessie R.; Martin, Adam R.; Nasielski, Joshua Ecology and Evolution, Vol. 7, Issue 10 https://doi.org/10.1002/ece3.2900	journal	April 2017
Increasing aridity reduces soil microbial diversity and abundance in global drylands Maestre, Fernando T.; Delgado-Baquerizo, Manuel; Jeffries, Thomas C. Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1516684112	journal	December 2015
Long-term effects of mineral fertilizers on soil microorganisms – A review Geisseler, Daniel; Scow, Kate M. Soil Biology and Biochemistry, Vol. 75 https://doi.org/10.1016/j.soilbio.2014.03.023	journal	August 2014
Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type Marschner, Petra; Crowley, David; Yang, Ching Hong Plant and Soil, Vol. 261, Issue 1/2 https://doi.org/10.1023/B:PLSO.0000035569.80747.c5	journal	April 2004
Nutrient status effects on loss of amides and amino acids from pine roots Bowen, G. D. Plant and Soil, Vol. 30, Issue 1 https://doi.org/10.1007/BF01885274	journal	February 1969
Oxidative stress, antioxidants and stress tolerance Mittler, Ron Trends in Plant Science, Vol. 7, Issue 9 https://doi.org/10.1016/S1360-1385(02)02312-9	journal	September 2002
Fertilization of Phaseolus vulgaris with the Tunisian rock phosphate affects richness and structure of rhizosphere bacterial communities Trabelsi, Darine; Cherni, Alaeddine; Zineb, Ameni Ben Applied Soil Ecology, Vol. 114 https://doi.org/10.1016/j.apsoil.2016.11.014	journal	June 2017
The diversity and biogeography of soil bacterial communities Fierer, N.; Jackson, R. B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0507535103	journal	January 2006
Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient Gosling, Paul; Mead, Andrew; Proctor, Maude New Phytologist, Vol. 198, Issue 2 https://doi.org/10.1111/nph.12169	journal	February 2013
Root microbiota drive direct integration of phosphate stress and immunity Castrillo, Gabriel; Teixeira, Paulo José Pereira Lima; Paredes, Sur Herrera Nature, Vol. 543, Issue 7646 https://doi.org/10.1038/nature21417	journal	March 2017
Translocation and turnover of rhizodeposit carbon within soil microbial communities of an extensive grassland ecosystem Balasooriya, Wajira K.; Denef, Karolien; Huygens, Dries Plant and Soil, Vol. 376, Issue 1-2 https://doi.org/10.1007/s11104-012-1343-z	journal	July 2012
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
Piriformospora indica , a Cultivable Plant-Growth-Promoting Root Endophyte Varma, Ajit; Verma, Savita Applied and Environmental Microbiology, Vol. 65, Issue 6, p. 2741-2744 https://doi.org/10.1128/AEM.65.6.2741-2744.1999	journal	June 1999
Rhizobium-Legume Symbiosis and Nitrogen Fixation under Severe Conditions and in an Arid Climate Zahran, Hamdi Hussein Microbiology and Molecular Biology Reviews, Vol. 63, Issue 4 https://doi.org/10.1128/MMBR.63.4.968-989.1999	journal	December 1999
Regulation and function of root exudates Badri, Dayakar V.; Vivanco, Jorge M. Plant, Cell & Environment https://doi.org/10.1111/j.1365-3040.2008.01926.x	journal	December 2008
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
Petunia- and Arabidopsis-Specific Root Microbiota Responses to Phosphate Supplementation Bodenhausen, Natacha; Somerville, Vincent; Desiro, Alessandro ETH Zurich https://doi.org/10.3929/ethz-b-000416436	text	January 2019
Correction to: Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming Hartman, Kyle; Van Der Heijden, Marcel G. A.; Wittwer, Raphaël A. ETH Zurich https://doi.org/10.3929/ethz-b-000419340	text	January 2020
Correction to: Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming Hartman, Kyle; van der Heijden, Marcel G. A.; Wittwer, Raphaël A. Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00855-4	journal	May 2020
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
Feed Your Friends: Do Plant Exudates Shape the Root Microbiome? Sasse, Joelle; Martinoia, Enrico; Northen, Trent Elsevier https://doi.org/10.5167/uzh-148899	text	January 2018
Design of synthetic bacterial communities for predictable plant phenotypes G., Castrillo,; C. D., Jones,; V., Jojic, Public Library of Science https://doi.org/10.17615/pxry-gy47	text	January 2018
Petunia- and Arabidopsis-Specific Root Microbiota Responses to Phosphate Supplementation Bodenhausen, Natacha; Somerville, Vincent; Desirò, Alessandro The American Phytopathological Society https://doi.org/10.7892/boris.132913	text	January 2019
Accounting for the combined impacts of natural resources rent, income level, and energy consumption on environmental quality of G7 economies: a panel quantile regression approach Gyamfi, Bright Akwasi; Onifade, Stephen Taiwo; Nwani, Chinazaekpere Environmental Science and Pollution Research, Vol. 29, Issue 2 https://doi.org/10.1007/s11356-021-15756-8	journal	August 2021
Bacterial cycling of minerals that affect plant growth in waterlogged soils: a review Laanbroek, H. J. Aquatic Botany, Vol. 38, Issue 1 https://doi.org/10.1016/0304-3770(90)90101-p	journal	October 1990
Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming (vol 6, 14, 2018) Kyle, Hartman,; G. A., van der Heijden, Marcel; A., Wittwer, Raphaël ETH Zurich https://doi.org/10.3929/ethz-b-000262471	text	January 2018

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