DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [1]; ORCiD logo [1];  [1];  [1];  [2]; ORCiD logo [2];  [2];  [2];  [1]; ORCiD logo [3];  [3];  [3];  [4];  [4];  [5];  [6];  [7];  [4]; ORCiD logo [2] more »;  [3];  [3];  [1] « less
  1. Univ. of California, Berkeley, CA (United States); US Dept. of Agriculture-Agricultural Research Service, Albany, CA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Kearney Agricultural Research & Extension Center, Parlier, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of California, Davis, Five Points, CA (United States)

Here, drought stress is a major obstacle to crop productivity, and the severity and frequency of drought are expected to increase in the coming century. Certain root-associated bacteria have been shown to mitigate the negative effects of drought stress on plant growth, and manipulation of the crop microbiome is an emerging strategy for overcoming drought stress in agricultural systems, yet the effect of drought on the development of the root microbiome is poorly understood. Through 16S rRNA amplicon and metatranscriptome sequencing, as well as root metabolomics, we demonstrate that drought delays the development of the early sorghum root microbiome and causes increased abundance and activity of monoderm bacteria, which lack an outer cell membrane and contain thick cell walls. Our data suggest that altered plant metabolism and increased activity of bacterial ATP-binding cassette (ABC) transporter genes are correlated with these shifts in community composition. Finally, inoculation experiments with monoderm isolates indicate that increased colonization of the root during drought can positively impact plant growth. Collectively, these results demonstrate the role that drought plays in restructuring the root microbiome and highlight the importance of temporal sampling when studying plant-associated microbiomes.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
DOA-0001207; CRIS-203021430-008-00D; AC05-76RL01830; AC02-05CH11231
OSTI ID:
1433401
Alternate ID(s):
OSTI ID: 1437150; OSTI ID: 1457007
Report Number(s):
PNNL-SA-131119
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, Issue 18; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English

References (69)

Changes through time: integrating microorganisms into the study of succession journal October 2010
Stable Coexistence in a Fluctuating Environment: an Experimental Demonstration journal October 2005
Control of Drought Stress in Wheat Using Plant-Growth-Promoting Bacteria journal June 2012
Teichuronic acid of the cell wall of Actinoplanes brasiliensis journal December 1994
Fundamentals of Microbial Community Resistance and Resilience journal January 2012
A crop water stress index and time threshold for automatic irrigation scheduling of grain sorghum journal May 2012
Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. journal October 2013
Structure, variation, and assembly of the root-associated microbiomes of rice journal January 2015
Differential expression analysis for sequence count data journal October 2010
Glycerol-3-phosphate transporter of Escherichia coli: Structure, function and regulation journal October 2004
Drought Stress Results in a Compartment-Specific Restructuring of the Rice Root-Associated Microbiomes journal July 2017
Global patterns of drought recovery journal August 2017
Origin of diderm (Gram-negative) bacteria: antibiotic selection pressure rather than endosymbiosis likely led to the evolution of bacterial cells with two membranes journal June 2011
The Influence of Land Use Intensity on the Plant-Associated Microbiome of Dactylis glomerata L. journal June 2017
Microbiome and Exudates of the Root and Rhizosphere of Brachypodium distachyon, a Model for Wheat journal October 2016
Comparison of canopy temperature-based water stress indices for maize journal July 2015
Bacterial-mediated drought tolerance: Current and future prospects journal September 2016
Conceptual Synthesis in Community Ecology journal June 2010
Host genotype and age shape the leaf and root microbiomes of a wild perennial plant text January 2016
Rhizosphere microbiome assemblage is affected by plant development journal November 2013
Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics journal February 2009
Polyene antibiotic biosynthesis gene clusters journal December 2002
Exploring interactions of plant microbiomes journal December 2014
Defining the core Arabidopsis thaliana root microbiome text January 2012
Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils journal July 2012
Application of Natural Blends of Phytochemicals Derived from the Root Exudates of Arabidopsis to the Soil Reveal That Phenolic-related Compounds Predominantly Modulate the Soil Microbiome journal January 2013
YSK2 Type Dehydrin (SbDhn1) from Sorghum bicolor Showed Improved Protection under High Temperature and Osmotic Stress Condition journal May 2017
Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms journal October 2011
A phylum level perspective on bacterial cell envelope architecture journal October 2010
Temporal Stability of the Human Skin Microbiome journal May 2016
Membrane-induced folding of the plant-stress protein Lti30. journal April 2016
Function of Dislocations in Cell Walls and Membranes journal November 1970
Host lifestyle affects human microbiota on daily timescales journal January 2014
General mechanisms of drought response and their application in drought resistance improvement in plants journal October 2014
Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland journal September 2013
Characterization and expression of dehydrins in water-stressed Sorghum bicolor journal January 1997
Bacterial Root Microbiome of Plants Growing in Oil Sands Reclamation Covers journal May 2017
Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species journal October 2015
The Root-Associated Microbial Community of the World’s Highest Growing Vascular Plants journal May 2016
Specificity of root microbiomes in native-grown Nicotiana attenuata and plant responses to UVB increase Deinococcus colonization journal March 2017
Drought and host selection influence bacterial community dynamics in the grass root microbiome journal July 2017
A decade of irrigation transforms the soil microbiome of a semi-arid pine forest journal January 2017
Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait: Root bacteria protect plants from drought journal March 2014
Sporulation, bacterial cell envelopes and the origin of life journal June 2016
Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis) journal March 2020
Assembly and ecological function of the root microbiome across angiosperm plant species journal January 2018
Deciphering composition and function of the root microbiome of a legume plant journal January 2017
The Impact of Beneficial Plant-Associated Microbes on Plant Phenotypic Plasticity journal July 2013
Root Exudation of Phytochemicals in Arabidopsis Follows Specific Patterns That Are Developmentally Programmed and Correlate with Soil Microbial Functions journal February 2013
Influence of extreme weather disasters on global crop production text January 2019
Defining the core Arabidopsis thaliana root microbiome journal August 2012
Stimulation of Plant Growth and Drought Tolerance by Native Microorganisms (AM Fungi and Bacteria) from Dry Environments: Mechanisms Related to Bacterial Effectiveness journal February 2009
Belowground Response to Drought in a Tropical Forest Soil. I. Changes in Microbial Functional Potential and Metabolism journal April 2016
Reactive Oxygen Species and the Cardiovascular System journal January 2013
Molecules to Ecosystems: Actinomycete Natural Products In situ journal January 2017
Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities journal November 2016
Characterization and expression of dehydrins in water-stressed Sorghum bicolor journal January 1997
Bacterial reference genes for gene expression studies by RT-qPCR: survey and analysis journal July 2015
Drought Stress and Root-Associated Bacterial Communities journal January 2018
Differential expression analysis for sequence count data journal April 2010
Climate variability has a stabilizing effect on the coexistence of prairie grasses journal August 2006
Increased plant productivity and decreased microbial respiratory C loss by plant growth-promoting rhizobacteria under elevated CO2 journal March 2015
Water deficiency at different developmental stages of Glycine max can improve drought tolerance journal January 2008
Biogeographic Patterns of Arbuscular Mycorrhizal Fungal Communities Along a Land-Use Intensification Gradient in the Subtropical Atlantic Forest Biome journal March 2021
Analysis of Temporal Gene Expression during Bacillus subtilis Spore Germination and Outgrowth journal February 2007
Influence of extreme weather disasters on global crop production journal January 2016
Uncovering the Horseshoe Effect in Microbial Analyses journal February 2017
Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient journal August 2012
Model plant systems in salinity and drought stress proteomics studies: a perspective on Arabidopsis and Sorghum journal September 2014

Cited By (38)

Interactions between plants and soil shaping the root microbiome under abiotic stress journal October 2019
Identification of beneficial and detrimental bacteria that impact sorghum responses to drought using multi-scale and multi-system microbiome comparisons dataset January 2021
Additional file 4 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) image January 2021
Additional file 3 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) image January 2021
A critical assessment of the feature selection methods used for biomarker discovery in current metaproteomics studies journal June 2019
Additional file 6 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) image January 2021
Plant Stage, Not Drought Stress, Determines the Effect of Cultivars on Bacterial Community Diversity in the Rhizosphere of Broomcorn Millet (Panicum miliaceum L.) journal April 2019
Additional file 5 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) image January 2021
Additional file 15 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Additional file 9 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Plant growth rate and nitrogen uptake shape rhizosphere bacterial community composition and activity in an agricultural field journal October 2019
Additional file 10 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Additional file 12 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Strong succession in arbuscular mycorrhizal fungal communities journal August 2018
Host-mediated microbiome engineering (HMME) of drought tolerance in the wheat rhizosphere journal December 2019
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response journal November 2019
Additional file 11 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Plant Host-Associated Mechanisms for Microbial Selection journal July 2019
A foliar Epichloë endophyte and soil moisture modified belowground arbuscular mycorrhizal fungal biodiversity associated with Achnatherum inebrians journal November 2019
Impact of abiotic stressors on native rhizospheric bacterial community of Cajanus cajan journal November 2019
Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses journal December 2019
Testing sustained soil-to-soil contact as an approach for limiting the abiotic influence of source soils during experimental microbiome transfer journal October 2019
Additional file 8 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics journal January 2020
Additional file 7 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk journal January 2019
Root microbiota assembly and adaptive differentiation among European Arabidopsis populations journal December 2019
Additional file 13 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021
Additional file 2 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) image January 2021
Duckweed hosts a taxonomically similar bacterial assemblage as the terrestrial leaf microbiome journal February 2020
Endophytic bacterial communities in peels and pulp of five root vegetables journal January 2019
Why Evolve Reliance on the Microbiome for Timing of Ontogeny? journal October 2019
The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response text January 2019
Additional file 1 of Host genotype-specific rhizosphere fungus enhances drought resistance in wheat dataset January 2024
Experimental warming alters the community composition, diversity, and N 2 fixation activity of peat moss ( Sphagnum fallax ) microbiomes journal May 2019
Plasticity of a holobiont: desiccation induces fasting-like metabolism within the lichen microbiota journal October 2018
Belowground microbial communities respond to water deficit and are shaped by decades of maize hybrid breeding journal June 2019
Additional file 14 of Strategies and Structure Feature of the Aboveground and Belowground Microbial Community Respond to Drought in Wild Rice (Oryza longistaminata) dataset January 2021