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Elucidating the impacts of environment and host on the assembly of plant-associated microbial communities

Abstract

The microbial world is integrally involved with major ecological processes and affects all domains of life. With the numerous societal challenges we face today, efforts are being directed towards better utilizing microbial communities to support host health and resilience. In regards to agriculture, this includes the fortification of crop production through microbial amendments and microbiome manipulation. To better engineer microbiomes capable of promoting plant growth and ameliorating stress, additional research is needed to untangle the relative contributions of environmental and host factors in recruiting and maintaining beneficial microbes, while repelling potential pathogens. The work presented here seeks to identify and explore the importance of a set of these environmental and host forces in shaping the root and rhizosphere microbiomes of crop species. Specifically, the impacts of disturbance on plant-microbe interactions are characterized in relation to the farming practices of tillage and cover-cropping, heat and drought stress, and host evolution.

This research first explores how a set of widely employed agricultural soil management practices influence the belowground interactions between sorghum, bacteria, and fungi. Currently, it is not well characterized how cultivation systems influence microbiome assembly and activity. Utilizing next generation sequencing methods, we characterized a field system managed for close to two decades with standard tillage or no till practices in combination with either cover-cropping or letting the field lay fallow. We observed a promotion of microbial diversity by standard till and determined that fungal communities responded to a greater degree - in both composition and activity - to management practice than bacteria. Interestingly, despite distinct communities under each regime, similar plant growth outcomes were observed. This work informs understandings of how intermittent soil disturbance impacts agroecosystems and highlights the importance of cross-kingdom analyses.

This work then investigates the combined and isolated impacts of heat and drought stress on sorghum microbiome assembly. Recent studies of drought and the plant microbiome have shown a high degree of variability in bacterial enrichment under drought, particularly for the phylum Actinobacteria. As heat often co-occurs with drought in the field, we sought to determine the relative contributions of temperature to this enrichment. Using a set of controlled growth chamber experiments, we observed that high temperatures do indeed correlate to a restructuring of sorghum-associated bacterial communities. This community differed from what was observed under drought alone, and the majority of indicator taxa within Actinobacteria were not shared between stresses. These results further our knowledge on how different abiotic stresses help modulate community interactions and lay the foundation for additional work characterizing the mechanisms involved in differential microbial enrichment.

In the final chapter of this work, the influence of host evolution on the associations between plants and their belowground microbiome is explored. Past research has shown that plant domestication and polyploidy can broadly influence plant biotic and abiotic interactions. We utilized three approaches - two field studies and one greenhouse-based experiment - to determine whether patterns in bacterial community assembly in wheat roots and rhizospheres could be partially attributable to these host factors. Collectively, we found little evidence of ploidy level and domestication status correlating with shifts in wheat bacterial communities. However, the greatest influence of the host on the microbiome appeared to occur in the rhizosphere compartment, and we suggest future work focuses on this environment to further characterize how host genomic and phenotypic changes influence plant-microbe communications. This research informs perspectives on what key driving forces may underlie microbiome structuring, as well as where future efforts may be best directed towards fortifying plant growth by microbial means.

Taken together, this work addresses fundamental gaps in our knowledge of the plant microbiome and the factors that help govern its structure and function. It demonstrates the ecological importance of agricultural soil management practices on plant-microbial interactions, uncovers the distinct roles of heat and drought stress in plant microbiome assembly, and indicates that domestication and polyploidy are minor contributors in shaping the wheat bacterial microbiome.

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