Abstract
Plant microbiomes and immune responses have coevolved through history, and this applies just as much to the phyllosphere microbiome and defense phytohormone signaling. When in homeostasis, the phyllosphere microbiome confers benefits to its host. However, the phyllosphere is also dynamic and subject to stochastic events that can modulate community assembly. Investigations into the impact of defense phytohormone signaling on the microbiome have so far been limited to culture-dependent studies; or focused on the rhizosphere. In this study, the impact of the foliar phytohormone salicylic acid (SA) on the structure and composition of the phyllosphere microbiome was investigated. 16S rRNA amplicons were sequenced from aerial tissues of two Arabidopsis mutants that exhibit elevated SA signaling through different mechanisms. SA signaling was shown to increase community diversity and to result in the colonization of rare, satellite taxa in the phyllosphere. However, a stable core community remained in high abundance. Therefore, we propose that SA signaling acts as a source of intermediate disturbance in the phyllosphere. Predictive metagenomics revealed that the SA-mediated microbiome was enriched for antibiotic biosynthesis and the degradation of a diverse range of xenobiotics. Core taxa were predicted to be more motile, biofilm-forming and were enriched for traits associated with microbe-microbe communication; offering potential mechanistic explanation of their success despite SA-mediated phyllospheric disturbance.
Highlights
Plants and animals have coevolved throughout history with functionally diverse colonizing microbes which modulate host fitness and environment-holobiont interactions (Limborg and Heeb, 2018)
In order to assess the impact of salicylic acid (SA) and its potential role in mediating disturbance on the phyllosphere microbiome, NGS metabarcoding was performed on amplicons of bacterial 16S rRNA sequences extracted from aerial tissue 35 days after sowing (DAS) on two A. thaliana mutants that exhibit elevated SA signaling, fhy3 far1 and lsd1
Comparisons between the microbiomes of three biological replicates of the fhy3 far1 and lsd1 mutant lines and their wild type (WT) background ecotypes (No-0 and Col-0, respectively) were performed using a phylotypebased approach due to the different 16S rRNA regions used for each pair
Summary
Plants and animals have coevolved throughout history with functionally diverse colonizing microbes which modulate host fitness and environment-holobiont interactions (Limborg and Heeb, 2018). The phyllosphere microbiome is dynamic and variable due to environmental exposure and the low nutrient availability in aerial plant matter when compared to the nutrient-rich soil environment in the rhizosphere (Maignien et al, 2014; Bringel and Couée, 2015; Singh et al, 2019). Phyllosphere microbiota are exposed to fluctuations in wind speed, temperature, light, SA and Phyllosphere Bacteria Disturbance humidity, UV radiation and rainfall which can temporally alter the microbiome composition (Carvalho and Castillo, 2018; Dastogeer et al, 2020; Sivakumar et al, 2020). These conditions make the phyllosphere prone to stochastic colonization processes such as dispersal and ecological drift (Maignien et al, 2014). Nutrient-poor environment in the phyllosphere, microbial community assembly is not considered to be an entirely random process; and is driven by other factors, including the host age, leaf physiology and genotype (Vorholt, 2012; Wagner et al, 2016; Singh et al, 2018; Chen T. et al, 2020; Shakir et al, 2020)
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