A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota

Abstract

The identity of plant host genetic factors controlling the composition of the plant microbiota and the extent to which plant genes affect associated microbial populations is currently unknown. Here, we use a candidate gene approach to investigate host effects on the phyllosphere community composition and abundance. To reduce the environmental factors that might mask genetic factors, the model plant Arabidopsis thaliana was used in a gnotobiotic system and inoculated with a reduced complexity synthetic bacterial community composed of seven strains representing the most abundant phyla in the phyllosphere. From a panel of 55 plant mutants with alterations in the surface structure, cell wall, defense signaling, secondary metabolism, and pathogen recognition, a small number of single host mutations displayed an altered microbiota composition and/or abundance. Host alleles that resulted in the strongest perturbation of the microbiota relative to the wild-type were lacs2 and pec1. These mutants affect cuticle formation and led to changes in community composition and an increased bacterial abundance relative to the wild-type plants, suggesting that different bacteria can benefit from a modified cuticle to different extents. Moreover, we identified ein2, which is involved in ethylene signaling, as a host factor modulating the community's composition. Finally, we found that different Arabidopsis accessions exhibited different communities, indicating that plant host genetic factors shape the associated microbiota, thus harboring significant potential for the identification of novel plant factors affecting the microbiota of the communities.

The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen

“…Overall, a relative consistency was observed among the genera on the different plants (Figs 3, 4, S3). Burkholderia, Pseudomonas and Methylophilus are among the major genera reported in the phylloplane of A. thaliana and other plants (Vorholt, 2012;Reisberg et al, 2013;Bodenhausen et al, 2014). Obviously, the physical and biochemical properties of the plant leaf surface, as well as environmental factors determine the composition of the microbes it harbours (Vorholt, 2012;Copeland et al, 2015).…”

“…The phylloplane of A. thaliana plants grown under similar sterile conditions and inoculated initially with a same representative mixture of the most abundant phylloplane bacteria was analysed in a collection of mutants with phenotypes ranging from altered cell walls to impaired defences and secondary metabolism. Interestingly, the strongest difference in bacterial composition and abundance compared to the wild-type plants was observed in lacs2.3, lacs2.4 and pec1 mutants affected in the biosynthesis of the cuticle (Bodenhausen et al, 2014). Mutants affected in the structure of the cuticle are characterized by enhanced cuticular permeability and display enhanced resistance to the agriculturally relevant fungal pathogen Botrytis cinerea.…”

Engineering Microbiomes to Improve Plant and Animal Health

“…Advantages: Synthetic microbiomes allow increased control over microbiome composition, potentially testing antagonistic versus synergistic effects among strains on host performance [90], uncovering host loci that mediate microbiome taxonomic makeup [91], or to reverse effects of dysbiosis, for instance in cases of Clostridium infections in humans [26]. Disadvantages: Only culturable or easily transferable microbes can be used to construct synthetic microbiomes.…”

Biological control in the microbiome era: Challenges and opportunities

“…The genotype is also particularly important. For example, a single mutation in a plant gene, like lacs2 and pec1 in Arabidopsis thaliana, can modify the microbiome (Bodenhausen et al, 2014). Moreover, environmental factors, such as, UV exposure and air humidity, and geographical location, also influence microbiome composition (Rastogi et al, 2013;Vorholt, 2012).…”