Successive plant growth amplifies genotype-specific assembly of the tomato rhizosphere microbiome

Viviane Cordovez,Cristina Rotoni,Francisco Dini-Andreote,Ben Oyserman,Víctor J Carrión,Jos M Raaijmakers

doi:10.1016/j.scitotenv.2020.144825

Abstract

Plant microbiome assembly is a spatial and dynamic process driven by root exudates and influenced by soil type, plant developmental stage and genotype. Genotype-dependent microbiome assembly has been reported for different crop plant species. Despite the effect of plant genetics on microbiome assembly, the magnitude of host control over its root microbiome is relatively small or, for many plant species, still largely unknown. Here we cultivated modern and wild tomato genotypes for four successive cycles and showed that divergence in microbiome assembly between the two genotypes was significantly amplified over time. Also, we show that the composition of the rhizosphere microbiome of modern and wild plants became more dissimilar from the initial bulk soil and from each other. Co-occurrence analyses further identified amplicon sequence variants (ASVs) associated with early and late successions of the tomato rhizosphere microbiome. Among the members of the Late Successional Rhizosphere microbiome, we observed an enrichment of ASVs belonging to the genera Acidovorax, Massilia and Rhizobium in the wild tomato rhizosphere, whereas the modern tomato rhizosphere was enriched for an ASV belonging to the genus Pseudomonas. Collectively, our approach allowed us to study the dynamics of rhizosphere microbiome over successional cultivation as well as to categorize rhizobacterial taxa for their ability to form transient or long-term associations with their host plants.

Highlights

Plant microbiome assembly is a spatial and dynamic process driven by root exudates and influenced by soil type, plant developmental stage and genotype
Among the members of the Late Successional Rhizosphere microbiome, we observed an enrichment of amplicon sequence variants (ASVs) belonging to the genera Acidovorax, Massilia and Rhizobium in the wild tomato rhizosphere, whereas the modern tomato rhizosphere was enriched for an ASV belonging to the genus Pseudomonas
Investigations into rhizosphere microbiome assembly are generally conducted for a single life cycle of the host plant and a single time point or developmental stage, and little is known about microbial community dynamics in the rhizosphere during plant succession (Chang and Turner, 2019)

Summary

Introduction

Plant microbiome assembly is a spatial and dynamic process driven by root exudates and influenced by soil type, plant developmental stage and genotype. Many studies have shown that the influence of host genetics on rhizosphere microbiome assembly, significant, is relatively small compared to the impact of other environmental factors, in particular of soil type and pH These findings have been consistently described for several plant species, including model plant species such as Arabidopsis thaliana and Lotus japonicus (Lundberg et al, 2012; Micallef et al, 2009b; Thiergart et al, 2019) as well as different crop species (Bulgarelli et al, 2015; Perez-Jaramillo et al, 2017). We highlighted the associations of these changes with plant phenotypic traits, in particular, seedling emergence

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