Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution.

Pierre-Marc Delaux,J Chris Pires,Jean-Michel Ané,Kranthi Varala,Gloria M Coruzzi,Patrick P Edger,John M Mcdowell

doi:10.1371/journal.pgen.1004487

Abstract

Mutualistic symbioses between eukaryotes and beneficial microorganisms of their microbiome play an essential role in nutrition, protection against disease, and development of the host. However, the impact of beneficial symbionts on the evolution of host genomes remains poorly characterized. Here we used the independent loss of the most widespread plant–microbe symbiosis, arbuscular mycorrhization (AM), as a model to address this question. Using a large phenotypic approach and phylogenetic analyses, we present evidence that loss of AM symbiosis correlates with the loss of many symbiotic genes in the Arabidopsis lineage (Brassicales). Then, by analyzing the genome and/or transcriptomes of nine other phylogenetically divergent non-host plants, we show that this correlation occurred in a convergent manner in four additional plant lineages, demonstrating the existence of an evolutionary pattern specific to symbiotic genes. Finally, we use a global comparative phylogenomic approach to track this evolutionary pattern among land plants. Based on this approach, we identify a set of 174 highly conserved genes and demonstrate enrichment in symbiosis-related genes. Our findings are consistent with the hypothesis that beneficial symbionts maintain purifying selection on host gene networks during the evolution of entire lineages.

Highlights

Eukaryotes interact with microbes in a dynamic network of symbiotic associations
In order to determine when the ‘symbiosis-specific’ genes have been lost in Brassicales and test if this loss correlates with the loss of the symbiotic ability, we assessed the presence of these genes in five sequenced Brassicaceae genomes, in the transcriptomes of four other Brassicaceae, including Aethionema arabicum, and in thirteen other taxa belonging to more basal Brassicales families
We reconstructed the evolutionary history of 33 fully sequenced plant genomes using BigPlant, a phylogenomic pipeline originally developed to analyze genomes and transcriptomes of seed plants [40]. Using this phylogenomic framework to analyze the genomes of 33 fully sequenced species, we identified a set of 395 ortholog groups, corresponding to 305 and 409 genes in Medicago and rice (Oryza sativa), respectively (Table 1, Tables S6 and Figure S4), that are highly conserved across land plants, but missing in the genomes of the five Brassicaceae sequenced to date (Table S6)

Summary

Introduction

Eukaryotes interact with microbes in a dynamic network of symbiotic associations. These associations represent a continuum from parasitic, where one partner takes advantage of the other one, to mutualistic, where both partners benefit from the interaction. Mutualistic symbioses between eukaryotes and a subset of their microbiome are essential to their nutrition, protection against diseases and development, as exemplified by the gut microbiome in humans or the arbuscular mycorrhizal (AM) symbiosis in plants [1,2]. During the lifetime of a single individual or at the scale of an entire population, hosts are known to select and shape their associated microbiome [3,4]. Recent studies shed light on the effect of the microbiome on plant and animal development by modifying gene expression [5,6,7]. The impact of associated microorganisms on the evolution of host organisms remains poorly characterized

Methods

Results

Conclusion