Whole-genome duplication and host genotype affect rhizosphere microbial communities

Abstract

The composition of complex microbial communities found in association with plants is influenced in part by host phenotype. Yet, the salient genetic architecture is often unknown. Genome duplication events are common in the evolutionary history of plants, influence many important plant traits, and 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. Specifically, we performed 16S rRNA amplicon sequencing to characterize differences between microbiomes associated with specific host genotypes (Columbia vs. Landsberg) and ploidy levels (diploid vs. tetraploid). We modeled abundances of individual bacterial taxa by utilizing a hierarchical Bayesian framework, based on the Dirichlet and multinomial distributions. We found that host genotype and host ploidy level affected rhizosphere community composition, for instance, the microbiome of the tetraploid Columbia genotype differed from that of other host genotypes. We then tested to what extent microbiomes derived from a given host genotype or ploidy level affected plant performance by inoculating sterile seedlings of each genotype with microbial communities harvested from a prior generation. We found a negative effect of the tetraploid Columbia microbiome on growth of all four plant genotypes. The findings suggest that while both host genotype and ploidy affect microbial community assembly, bacterial communities found in association with only some host genotypes may affect growth of subsequent plant generations.ImportancePlants influence the composition of their associated microbial communities; yet the underlying host genetic factors are often unknown. Genome duplication events are common in the evolutionary history of plants and affect many plant traits, including the quality and quantity of compounds exuded into the root zone, which can affect root-bound microbes. In Arabidopsis thaliana, we characterized how whole-genome duplication affected the composition of rhizosphere bacterial communities, and how bacterial communities associated with two host plant genotypes and ploidy levels affected subsequent plant growth. We observed an interaction in which ploidy level within one host genotype 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 the coexistence of bacterial taxa and affects plant growth.

Induction of autotetraploidy and microbiome associations mediate differential responses to pathogens

“…Likewise, we did not find any significant differences in the relative abundance of any of the synthetic community members across the two ploidy levels, both of which were dominated by Pantoea, Pseudomonas, and Exiguobacterium. This is in line with work on wheat, where ploidy was found to play a weak and inconsistent role in shaping the below-ground microbiome (Wipf & Coleman-Derr 2021), but contrasts with previous work on Arabidopsis which did find a signature of ploidy in shaping microbial community composition across accessions (Ponsford et al 2020).…”

Evaluating domestication and ploidy effects on the assembly of the wheat bacterial microbiome

“…These results regarding ploidy effects on bacterial recruitment loosely corroborate past work in which a cordgrass allopolyploid (genus Spartina ) was found to harbor a more diverse rhizosphere bacterial community, as compared to diploid counterparts [ 64 ]. Another study using Arabidopsis reported that rhizosphere community composition—but not alpha diversity—shifted with whole genome duplication and differences in host genotype [ 65 ]. Indeed, degree of impact from host genetic factors, including ploidy level, on the plant microbiome seems to vary across species, as observed in our cotton outgroup compared to tested wheat species, as well as demonstrated in past work [ 66 – 68 ].…”

Heterosis of leaf and rhizosphere microbiomes in field‐grown maize

“…Or is it a contributing mechanism of hybrid vigor itself? These questions could be addressed using synthetic microbial communities, reinoculation or soil‐conditioning experiments (Panke‐Buisse et al ., 2015; Vorholt et al ., 2017; Ponsford et al ., 2019). These important next steps will help to clarify the role of plant‐associated microbes in hybrid vigor.…”