Drought is a major abiotic stress limiting agricultural productivity. Previous field-level experiments have demonstrated that drought decreases microbiome diversity in the root and rhizosphere. How these changes ultimately affect plant health remains elusive. Toward this end, we combined reductionist, transitional and ecological approaches, applied to the staple cereal crop sorghum to identify key root-associated microbes that robustly affect drought-stressed plant phenotypes. Fifty-three Arabidopsis-associated bacteria were applied to sorghum seeds and their effect on root growth was monitored. Two Arthrobacter strains caused root growth inhibition (RGI) in Arabidopsis and sorghum. In the context of synthetic communities, Variovorax strains were able to protect plants from Arthrobacter-caused RGI. As a transitional system, high-throughput phenotyping was used to test the synthetic communities. During drought stress, plants colonized by Arthrobacter had reduced growth and leaf water content. Plants colonized by both Arthrobacter and Variovorax performed as well or better than control plants. In parallel, we performed a field trial wherein sorghum was evaluated across drought conditions. By incorporating data on soil properties into the microbiome analysis, we accounted for experimental noise with a novel method and were able to observe the negative correlation between the abundance of Arthrobacter and plant growth. Having validated this approach, we cross-referenced datasets from the high-throughput phenotyping and field experiments and report a list of bacteria with high confidence that positively associated with plant growth under drought stress. In conclusion, a three-tiered experimental system successfully spanned the lab-to-field gap and identified beneficial and deleterious bacterial strains for sorghum under drought.
Root Microbiome Modulates Plant Growth Promotion Induced by Low Doses of Glyphosate
ABSTRACT Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis . We found that a dose of 3.6 × 10 −6 g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ∼14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by ∼17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restored growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains. IMPORTANCE Since the introduction of glyphosate-resistant crops, glyphosate has become the most common and widely used herbicide around the world. Due to its intensive use and ability to bind to soil particles, it can be found at low concentrations in the environment. The effect of these remnants of glyphosate in plants has not been broadly studied; however, glyphosate 1,000 to 100,000 times less concentrated than the recommended field dose promoted growth in several species in laboratory and greenhouse experiments. However, this effect is rarely observed in agricultural fields, where complex communities of microbes have a central role in the way plants respond to external cues. Our study reveals how root-associated bacteria modulate the responses of Arabidopsis to low doses of glyphosate, shifting between growth promotion and growth inhibition.
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- Award ID(s):
- 1917270
- NSF-PAR ID:
- 10233746
- Editor(s):
- Fischer, Reinhard
- Date Published:
- Journal Name:
- mSphere
- Volume:
- 5
- Issue:
- 4
- ISSN:
- 2379-5042
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
null (Ed.)Strategies to reduce crop losses due to drought are needed as climate variability affects agricultural productivity. Wheat (Triticum aestivum var. Juniper) growth in a nutrient-sufficient, solid growth matrix containing varied doses of CuO, ZnO, and SiO2 nanoparticles (NPs) was used to evaluate NP mitigation of drought stress. NP amendments were at fertilizer levels, with maxima of 30 Cu, 20 Zn, and 200 Si (mg metal/kg matrix). Seeds of this drought-tolerant cultivar were inoculated with Pseudomonas chlororaphis O6 (PcO6) to provide a protective root microbiome. An 8 day drought imposed on 14 day-old wheat seedlings decreased shoot and root mass, shoot water content, and the quantum yield of photosystem II when compared to watered plants. PcO6 root colonization was not impaired by drought or NPs. A dose-dependent increase in the Cu, Zn, and Si from the NPs was observed from analysis of the rhizosphere solution, and this process was not affected by drought. Consequently, fertilizer concentrations of the NPs did not further improve drought tolerance in wheat seedlings under the growth conditions of adequate mineral nutrition and the presence of a beneficial microbiome. These findings suggest that potential NP benefits in promoting plant drought tolerance occur only under certain environmental conditions.more » « less
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Plant growth-promoting bacteria (PGPB) can enhance plant health by facilitating nutrient uptake, nitrogen fixation, protection from pathogens, stress tolerance and/or boosting plant productivity. The genetic determinants that drive the plant–bacteria association remain understudied. To identify genetic loci highly correlated with traits responsive to PGPB, we performed a genome-wide association study (GWAS) using an Arabidopsis thaliana population treated with Azoarcus olearius DQS-4T. Phenotypically, the 305 Arabidopsis accessions tested responded differently to bacterial treatment by improving, inhibiting, or not affecting root system or shoot traits. GWA mapping analysis identified several predicted loci associated with primary root length or root fresh weight. Two statistical analyses were performed to narrow down potential gene candidates followed by haplotype block analysis, resulting in the identification of 11 loci associated with the responsiveness of Arabidopsis root fresh weight to bacterial inoculation. Our results showed considerable variation in the ability of plants to respond to inoculation by A. olearius DQS-4T while revealing considerable complexity regarding statistically associated loci with the growth traits measured. This investigation is a promising starting point for sustainable breeding strategies for future cropping practices that may employ beneficial microbes and/or modifications of the root microbiome.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mSphere.00484-20
