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1. The Floral Microbiome: Plant, Pollinator, and Microbial Perspectives

   https://doi.org/10.1146/annurev-ecolsys-011720-013401  

   Vannette, Rachel L. (November 2020, Annual Review of Ecology, Evolution, and Systematics)

   null (Ed.)

   Flowers at times host abundant and specialized communities of bacteria and fungi that influence floral phenotypes and interactions with pollinators. Ecological processes drive variation in microbial abundance and composition at multiple scales, including among plant species, among flower tissues, and among flowers on the same plant. Variation in microbial effects on floral phenotype suggests that microbial metabolites could cue the presence or quality of rewards for pollinators, but most plants are unlikely to rely on microbes for pollinator attraction or reproduction. From a microbial perspective, flowers offer opportunities to disperse between habitats, but microbial species differ in requirements for and benefits received from such dispersal. The extent to which floral microbes shape the evolution of floral traits, influence fitness of floral visitors, and respond to anthropogenic change is unclear. A deeper understanding of these phenomena could illuminate the ecological and evolutionary importance of floral microbiomes and their role in the conservation of plant–pollinator interactions. 

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2. Whole-Genome Duplication and Host Genotype Affect Rhizosphere Microbial Communities

   https://doi.org/10.1128/msystems.00973-21  

   Ponsford, Julian C.; Hubbard, Charley J.; Harrison, Joshua G.; Maignien, Lois; Buerkle, C. Alex; Weinig, Cynthia (February 2022, mSystems)

   Bulgarelli, Davide (Ed.)

   ABSTRACT The composition of microbial communities found in association with plants is influenced by host phenotype and genotype. However, the ways in which specific genetic architectures of host plants shape microbiomes are unknown. Genome duplication events are common in the evolutionary history of plants and influence many important plant traits, and thus, they may affect associated microbial communities. Using experimentally induced whole-genome duplication (WGD), we tested the effect of WGD on rhizosphere bacterial communities in Arabidopsis thaliana . We performed 16S rRNA amplicon sequencing to characterize differences between microbiomes associated with specific host genetic backgrounds (Columbia versus Landsberg) and ploidy levels (diploid versus tetraploid). We modeled relative abundances of bacterial taxa using a hierarchical Bayesian approach. We found that host genetic background and ploidy level affected rhizosphere community composition. We then tested to what extent microbiomes derived from a specific genetic background or ploidy level affected plant performance by inoculating sterile seedlings with microbial communities harvested from a prior generation. We found a negative effect of the tetraploid Columbia microbiome on growth of all four plant genetic backgrounds. These findings suggest an interplay between host genetic background and ploidy level and bacterial community assembly with potential ramifications for host fitness. Given the prevalence of ploidy-level variation in both wild and managed plant populations, the effects on microbiomes of this aspect of host genetic architecture could be a widespread driver of differences in plant microbiomes. IMPORTANCE Plants influence the composition of their associated microbial communities, yet the underlying host-associated genetic determinants are typically unknown. Genome duplication events are common in the evolutionary history of plants and affect many plant traits. Using Arabidopsis thaliana , we characterized how whole-genome duplication affected the composition of rhizosphere bacterial communities and how bacterial communities associated with two host plant genetic backgrounds and ploidy levels affected subsequent plant growth. We observed an interaction between ploidy level and genetic background that affected both bacterial community composition and function. This research reveals how genome duplication, a widespread genetic feature of both wild and crop plant species, influences bacterial assemblages and affects plant growth. 

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3. Rhizosphere microbial community composition shifts diurnally and in response to natural variation in host clock phenotype

   https://doi.org/10.1128/msystems.01487-21  

   Hubbard, Charley J.; Harrison, Joshua G.; McMinn, Robby; Bennett Ponsford, Julian C.; Maignien, Lois; Ewers, Brent; Weinig, Cynthia (June 2023, mSystems)

   Heck, Michelle (Ed.)

   ABSTRACT Plant-associated microbial assemblages are known to shift at time scales aligned with plant phenology, as influenced by the changes in plant-derived nutrient concentrations and abiotic conditions observed over a growing season. But these same factors can change dramatically in a sub-24-hour period, and it is poorly understood how such diel cycling may influence plant-associated microbiomes. Plants respond to the change from day to night via mechanisms collectively referred to as the internal “clock,” and clock phenotypes are associated with shifts in rhizosphere exudates and other changes that we hypothesize could affect rhizosphere microbes. The mustardBoechera strictahas wild populations that contain multiple clock phenotypes of either a 21- or a 24-hour cycle. We grew plants of both phenotypes (two genotypes per phenotype) in incubators that simulated natural diel cycling or that maintained constant light and temperature. Under both cycling and constant conditions, the extracted DNA concentration and the composition of rhizosphere microbial assemblages differed between time points, with daytime DNA concentrations often triple what were observed at night and microbial community composition differing by, for instance, up to 17%. While we found that plants of different genotypes were associated with variation in rhizosphere assemblages, we did not see an effect on soil conditioned by a particular host plant circadian phenotype on subsequent generations of plants. Our results suggest that rhizosphere microbiomes are dynamic at sub-24-hour periods, and those dynamics are shaped by diel cycling in host plant phenotype. IMPORTANCEWe find that the rhizosphere microbiome shifts in composition and extractable DNA concentration in sub-24-hour periods as influenced by the plant host’s internal clock. These results suggest that host plant clock phenotypes could be an important determinant of variation in rhizosphere microbiomes. 

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4. Soil moisture incidentally selects for microbes that facilitate locally adaptive plant response

   https://doi.org/10.1098/rspb.2023.0469  

   Ricks, Kevin D.; Yannarell, Anthony C. (June 2023, Proceedings of the Royal Society B: Biological Sciences)

   While a plant's microbiome can facilitate adaptive phenotypes, the plant's role in selecting for these microbes is unclear. Do plants actively recruit microbes beneficial to their current environment, or are beneficial microbes only an incidental by-product of microbial adaptation? We addressed these questions through a multigeneration greenhouse experiment, selecting for either dry- or wet-adapted soil microbial communities, either with or without plants. After three plant generations, we conducted a full reciprocal transplant of each soil community onto wet- and dry-treated plants. We found that plants generally benefited from soil microbes, and this benefit was greater whenever their current watering conditions matched the microbes' historical watering conditions. Principally, the plant's presence was not necessary in the historical treatments for this environmental matching benefit to emerge. Moreover, we found microbes from droughted soils could better tolerate drought stress. Taken together, these results suggest that the moisture environment selects for microbes that benefit plants under those specific moisture conditions, and that these beneficial properties arise as a by-product of microbial adaptation to the watering environment and not as a co-adapting plant–microbe system. This work highlights that understanding the selective agents on these plant-associated microbes will lead to a better understanding of plant adaptation. 

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5. Environment and Host Genetics Influence the Biogeography of Plant Microbiome Structure

   https://doi.org/10.1007/s00248-023-02288-6  

   Wei, Na; Tan, Jiaqi (August 2023, Microbial Ecology)

   To understand how microbiota influence plant populations in nature, it is important to examine the biogeographic distribution of plant-associated microbiomes and the underlying mechanisms. However, we currently lack a fundamental understanding of the biogeography of plant microbiomes across populations and the environmental and host genetic factors that shape their distribution. Leveraging the broad distribution and extensive genetic variation in duckweeds (the Lemna species complex), we identified key factors that governed plant microbiome diversity and compositional variation geographically. In line with the microbial biogeography of free-living microbiomes, we observed higher bacterial richness in temperate regions relative to lower latitudes in duckweed microbiomes (with 10% higher in temperate populations). Our analyses revealed that higher temperature and sodium concentration in aquatic environments showed a negative impact on duckweed bacterial richness, whereas temperature, precipitation, pH, and concentrations of phosphorus and calcium, along with duckweed genetic variation, influenced the biogeographic variation of duckweed bacterial community composition. Analyses of plant microbiome assembly processes further revealed that niche-based selection played an important role (26%) in driving the biogeographic variation of duckweed bacterial communities, alongside the contributions of dispersal limitation (33%) and drift (39%). These findings add significantly to our understanding of host-associated microbial biogeography and provide important insights for predicting plant microbiome vulnerability and resilience under changing climates and intensifying anthropogenic activities. 

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