Plant‐driven changes in soil microbial communities influence seed germination through negative feedbacks

Abstract

Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination. We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs. We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host‐specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host‐specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs. Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host‐specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe‐mediated interactions between plants at different life stages that next‐generation sequencing can begin to unravel.

Community context for mechanisms of disease dilution: insights from linking epidemiology and plant–soil feedback theory

“…Microbial interactions are well known to drive disease suppression in agricultural systems 97 and are, therefore, expected to be important in modifying feedback in natural systems. Using metagenomic tools, microbial taxa are increasingly identified in studies of PSFs 76,77,98 . Still, it remains challenging to implicate particular taxa as drivers of the negative feedback, much less examine the antagonistic relationship between two pathogens or two microbes more generally.…”

Effects of the soil microbiome on the demography of two annual prairie plants

“…(2017) and Dudenhöffer, Ebeling, Klein, and Wagg (2018), who have focused on entire plant life cycles, including effects of soil microbes on plant reproduction. Miller, Perron, and Collins (2019) have studied feedback at the seed stage.…”

Differential analysis of prokaryotic communities from pristine mangrove tidal zone sediments reveal distinct structures and functional profiles

“…While we attempted to avoid the inclusion of plant material in our collection of sediments, the presence of mangrove trees and other vegetation is an unavoidable feature of the tidal zones. Similarly, the higher density of vegetation observed in the sublittoral area may, in part, explain the higher diversity of the prokaryotic populations we identified there (Bennett and Klironomos 2019;Miller, Perron and Collins 2019). Additionally, the microbiome of the mangrove can be heavily influenced by eukaryotic communities (Alzubaidy et al 2015), which would be invisible to our 16S rRNA amplicon sequencing method.…”