Identification of beneficial and detrimental bacteria that impact sorghum responses to drought using multi-scale and multi-system microbiome comparisons

Abstract

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 as Actinobacteria. 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 with Arabidopsis, were applied to sorghum seeds and their effect on root growth was monitored for seven days. Two Arthrobacter strains, members of the Actinobacteria phylum, caused root growth inhibition (RGI) in Arabidopsis and sorghum. In the context of synthetic communities, strains of Variovorax were able to protect both Arabidopsis and sorghum from the RGI caused by Arthrobacter. 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 by Arthrobacter were significantly smaller and had reduced leaf water content as compared to control plants. However, 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 well-watered and drought conditions. Drought responsive microbes were identified, including an enrichment in Actinobacteria, 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 of Arthrobacter strains 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.

Poisson hurdle model-based method for clustering microbiome features

“…A microbiome study was carried out in Nebraska where sorghum plants of the genotype Grassl were grown with two varying nitrogen levels (Low/High). Rhizosphere microbiome samples were collected on four different dates throughout the growing season between June and September of 2017 and analyzed by 16S rRNA amplicon sequencing (Qi et al, 2021). Applying the persistence method (Shade and Handelsman, 2012) to identify core ASVs among the eight treatments, we obtained a subset of 449 ASVs with average read count of 44.21, and 38% of counts in this subset are zero.…”

Sorghum rhizosphere bacteriome studies to pinpoint, isolate and assess plant beneficial bacteria

“…Unlike the other major crops, sorghum is adapted to a wide range of climates being a resilient crop in hot and arid environments [26]. Several recent studies have been performed on the rhizosphere microbiome of sorghum evidencing that it is in uenced by a set of factors including plant genotype, pathogens, plant developmental stage, soil properties, salt and drought stress as well as agricultural soil practices [27][28][29][30][31][32][33].…”

Cross‐inoculation of rhizobiome from a congeneric ruderal plant imparts drought tolerance in maize (Zea mays) through changes in root morphology and proteome

“…There is now increasing recognition that plantassociated microbial communities can significantly stimulate plant growth and enhance plant resistance to abiotic stresses (Mapelli et al, 2013;Qi et al, 2021;Vejan et al, 2016). Sustained by root exudates (Chai & Schachtman, 2022;Sasse et al, 2018;Huang et al 2019), and root chemistry (Wang et al, 2015), a plethora of microorganisms inhabit rhizosphere forming a complex ecological community that influences plant growth and productivity (Lugtenberg & Kamilova, 2009;Zhalnina et al, 2018).…”

“…Such efforts include screening for drought‐tolerant varieties using conventional breeding or biotechnological approaches, shifting the crop calendars, and improving resource management practices (Venkateswarlu & Shanker, 2009; Vurukonda et al., 2016). Along with the above approaches, the precise modulation of soil microbial communities inhabiting the rhizosphere (rhizobiome) is a promising avenue for improving the performance of crops under environmental stress (Qi et al., 2021).…”

“…There is now increasing recognition that plant‐associated microbial communities can significantly stimulate plant growth and enhance plant resistance to abiotic stresses (Mapelli et al., 2013; Qi et al., 2021; Vejan et al., 2016). Sustained by root exudates (Chai & Schachtman, 2022; Sasse et al., 2018; Huang et al.…”