Abstract
BackgroundPlants have developed defense strategies for phytopathogen and herbivore protection via coordinated metabolic mechanisms. Low-molecular weight metabolites produced within plant tissues, such as salicylic acid, represent one such mechanism which likely mediates plant – microbe interactions above and below ground. Salicylic acid is a ubiquitous phytohormone at low levels in most plants, yet are concentrated defense compounds in Populus, likely acting as a selective filter for rhizosphere microbiomes. We propagated twelve Populus trichocarpa genotypes which varied an order of magnitude in salicylic acid (SA)-related secondary metabolites, in contrasting soils from two different origins. After four months of growth, plant properties (leaf growth, chlorophyll content, and net photosynthetic rate) and plant root metabolomics specifically targeting SA metabolites were measured via GC-MS. In addition, rhizosphere microbiome composition was measured via Illumina MiSeq sequencing of 16S and ITS2 rRNA-genes.ResultsSoil origin was the primary filter causing divergence in bacterial/archaeal and fungal communities with plant genotype secondarily influential. Both bacterial/archaeal and fungal evenness varied between soil origins and bacterial/archaeal diversity and evenness correlated with at least one SA metabolite (diversity: populin; evenness: total phenolics). The production of individual salicylic acid derivatives that varied by host genotype resulted in compositional differences for bacteria /archaea (tremuloidin) and fungi (salicylic acid) within one soil origin (Clatskanie) whereas soils from Corvallis did not illicit microbial compositional changes due to salicylic acid derivatives. Several dominant bacterial (e.g., Betaproteobacteria, Acidobacteria, Verrucomicrobia, Chloroflexi, Gemmatimonadete, Firmicutes) and one fungal phyla (Mortierellomycota) also correlated with specific SA secondary metabolites; bacterial phyla exhibited more negative interactions (declining abundance with increasing metabolite concentration) than positive interactions.ConclusionsThese results indicate microbial communities diverge most among soil origin. However, within a soil origin, bacterial/archaeal communities are responsive to plant SA production within greenhouse-based rhizosphere microbiomes. Fungal microbiomes are impacted by root SA-metabolites, but overall to a lesser degree within this experimental context. These results suggest plant defense strategies, such as SA and its secondary metabolites, may partially drive patterns of both bacterial/archaeal and fungal taxa-specific colonization and assembly.
Highlights
Plants have developed defense strategies for phytopathogen and herbivore protection via coordinated metabolic mechanisms
Leaf chlorophyll content was lower for BESC-838 compared to GW-9830 and KTMC-12-5 (Tukey’s HSD: p < 0.02) whereas BESC-838 had greater leaf growth compared to these two genotypes (Tukey’s HSD: p < 0.02)
Photosynthetic rate (p ≤ 0.05) and chlorophyll content (p ≤ 0.02) correlated with either catechin, tremuloidin, or salicylic acid, but this relationship depended on soil origin (Additional file 1: Table S4); leaf growth did not correlate with any metabolite regardless of soil origin (p ≥ 0.06)
Summary
Plants have developed defense strategies for phytopathogen and herbivore protection via coordinated metabolic mechanisms. Low-molecular weight metabolites produced within plant tissues, such as salicylic acid, represent one such mechanism which likely mediates plant – microbe interactions above and below ground. Environmental variation spanning large spatial extents, such as edaphic or climatic conditions [5, 6] to smaller-scale interactions via plant-microbe cellular processes, such as plant-mediated chemical signaling [7], may concurrently impact below ground microbiome development and maintenance. Wagner et al, (2013) [8] indicated plant hosts, Boechera stricta, exhibited greater genetic control in aboveground bacterial communities relative to belowground suggesting the importance of environmental heterogeneity in shaping assembly dynamics, for belowground tissues. The relative importance of edaphic conditions versus host selection processes in determining plant microbiome composition, in tree species, has been largely unexplored [9] and may be dependent on the wide range of physiological or genetic differences among or within plant species
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