Identification of beneficial and detrimental bacteria that impact sorghum responses to drought using multi-scale and multi-system microbiome comparisons
Authors: Qi Mingsheng , Berry Jeffrey C. , Veley Kira , O’Connor Lily , Finkel Omri M. , Salas-González Isai , Kuhs Molly , Jupe Julietta , Holcomb Emily , del Rio Tijana Glavina , Creech Cody , Liu Peng , Tringe Susannah , Dangl Jeffery L. , Schachtman Daniel , Bart Rebecca S. 
Published: April 2021

Background

Drought is a major abiotic stress that limits agricultural productivity. Previous field-level experiments have demonstrated that drought decreases microbiome diversity in the root and rhizosphere and may lead to enrichment of specific groups of microbes, such asActinobacteria. How these changes ultimately affect plant health is not well understood. In parallel, model systems have been used to tease apart the specific interactions between plants and single, or small groups of microbes. However, translating this work into crop species and achieving increased crop yields within noisy field settings remains a challenge. Thus, the next scientific leap forward in microbiome research must cross the great lab-to-field divide. Toward this end, we combined reductionist, transitional and ecological approaches, applied to the staple cereal crop sorghum to identify key beneficial and detrimental, root associated microbes that robustly affect drought stressed plant phenotypes.

Results

Fifty-three bacterial strains, originally characterized for association withArabidopsis, were applied to sorghum seeds and their effect on root growth was monitored for seven days. TwoArthrobacterstrains, members of theActinobacteriaphylum, caused root growth inhibition (RGI) inArabidopsisand sorghum. In the context of synthetic communities, strains ofVariovoraxwere able to protect bothArabidopsisand sorghum from the RGI caused byArthrobacter. As a transitional system, we tested the synthetic communities through a 24-day high-throughput sorghum phenotyping assay and found that during drought stress, plants colonized byArthrobacterwere significantly smaller and had reduced leaf water content as compared to control plants. However, plants colonized by bothArthrobacterandVariovoraxperformed as well or better than control plants. In parallel, we performed a field trial wherein sorghum was evaluated across well-watered and drought conditions. Drought responsive microbes were identified, including an enrichment inActinobacteria, consistent with previous findings. By incorporating data on soil properties into the microbiome analysis, we accounted for experimental noise with a newly developed method and were then able to observe that the abundance ofArthrobacterstrains negatively correlated with plant growth. Having validated this approach, we cross-referenced datasets from the high-throughput phenotyping and field experiments and report a list of high confidence bacterial taxa that positively associated with plant growth under drought stress.

Conclusions

A three-tiered experimental system connected reductionist and ecological approaches and identified beneficial and deleterious bacterial strains for sorghum under drought stress.