Search bioRxiv⌕ Search

Biology subjects

Masson-Boivin, C.

Publications and source records attributed to Masson-Boivin, C..

4 recordsLinked to original sources

Comparative phylotranscriptomics reveals a 110 million years-old symbiotic program

Symbiotic interactions have structured past and present ecosystems and shaped the evolution of life. As any trait, the symbiotic state observed in extant species builds on ancestral and conserved features, and lineage-specific innovations. From these mixed origins, defining the ancestral state of symbiotic associations is challenging although it is instrumental for understanding how symbiotic abilities emerge from non-symbiotic states. Here we aimed at reconstructing the intermediate steps leading to the root-nodule nitrogen-fixing symbiosis (RNS) observed in some extant flowering plants. For this, we compared the transcriptomic responses of nine host plants in response to symbiotic bacteria. We included the mimosoid legume Mimosa pudica for which we assembled a chromosome-level genome and generated the transcriptomic response to experimentally evolved bacterial symbionts. With this dataset, we reconstructed the ancestral RNS transcriptome, composed of most already described symbiotic genes together with hundreds of novel candidates. We found that the response to the chemical signals produced by the symbiont, nodule organogenesis and nitrogen-fixation are predominantly linked to ancestral responses, although these traits have diversified in the different nitrogen-fixing lineages. We detected a clear signature of recent and convergent evolution for the ability to release intracellular symbiosomes in two legume lineages, exemplified by the expression of different classes of small proteins in each group, potentially leading to the convergent gain of symbiotic evolutionary stability. Our findings demonstrate that most of the novelties for RNS were mostly in place in the most recent common ancestor of the RNS-forming species that lived on Earth 110 million years ago. Graphical abstractA little graphical/nice phylogeny with nodes of interest HighlightsO_LIWe sequenced a high-quality genome of the Mimosoideae Mimosa pudica C_LIO_LIThe nitrogen-fixing root-nodule symbiosis relies on an ancestral transcriptomic response C_LIO_LIAll symbiotic traits involve genes of the ancestral symbiotic program C_LIO_LISymbiont perception, nodule organogenesis and nitrogen-fixation are essentially ancestral processes C_LIO_LIConvergent evolution of intracellular accommodation of symbionts additionally involves lineage-specific genes C_LI

plant biology↗

A selective bottleneck during host entry drives the evolution of new legume symbionts

During the emergence of new host-microbe symbioses, multiple selective pressures-acting at the different steps of the microbial life cycle-shape the phenotypic traits that jointly determine microbial fitness. However, the relative contribution of these different selective pressures to the adaptive trajectories of microbial symbionts are still poorly known. Here we characterized the dynamics of phenotypic adaptation and its underlying genetic bases during the experimental evolution of a plant pathogenic bacterium into a legume symbiont. We observed that fast adaptation was predominantly driven by selection acting on competitiveness for host entry, which outweighed selection acting on within-host proliferation. Whole-population sequencing of evolved bacteria revealed that phenotypic adaptation was supported by the continuous accumulation of new mutations and the sequential sweeps of cohorts of mutations with similar temporal trajectories. The identification of adaptive mutations within the fixed mutational cohorts showed that all of them improved competitiveness for host entry, while only a subset of those also improved within host proliferation. Computer simulations predict that this effect emerges from the presence of a strong selective bottleneck at host entry. Together, these results show how selective bottlenecks can alter the relative influence of selective pressures acting during bacterial adaptation to multistep infection processes.

evolutionary biology↗

Rhizobium leguminosarum symbiovar viciae strains are natural wheat endophytes and can stimulate root development and colonization by arbuscular mycorrhizal fungi

O_LIAlthough rhizobia establishing a nitrogen-fixing symbiosis with legumes are also known to promote growth in non-legumes, studies on rhizobia association with wheat roots are scarce. C_LIO_LIWe searched for Rhizobium leguminosarum symbiovar viciae (Rlv) strains naturally competent for wheat roots colonization. We isolated 20 strains and tested the ability of a subset for wheat roots colonization when co-inoculated with other Rlv. We also measured the effect of these strains on wheat root architecture and Arbuscular Mycorrhizal Fungal (AMF) colonization. C_LIO_LIWe found a low diversity of Rlv in wheat roots compared to that observed in the Rlv species complex. Only a few strains, including those isolated from wheat roots, and one strain isolated from pea nodules, were efficient to colonize wheat roots in co-inoculation conditions. These strains had a high ability for endophytic colonization of wheat root and were able to stimulate root development and AMF colonization in single strain inoculation conditions. C_LIO_LIThese results suggest that wheat is an alternative host for some Rlv; nevertheless, there is a strong competition between Rlv strains for wheat root colonization. Furthermore, our study suggests that the level of endophytic colonization is critical for Rlv ability to promote wheat growth. C_LI

microbiology↗

Parallels between experimental and natural evolution of legume symbionts

The emergence of symbiotic interactions has been studied using population genomics in nature and experimental evolution in the laboratory, but the parallels between these processes remain unknown. We compared the emergence of rhizobia after the horizontal transfer of a symbiotic plasmid in natural populations of Cupriavidus taiwanensis, over 10 MY ago, with the experimental evolution of symbiotic Ralstonia solanacearum for a few hundred generations. In spite of major differences in terms of time-span, environment, genetic background and phenotypic achievement, both processes resulted in rapid diversification dominated by purifying selection concomitant with acquisition of positively selected mutations. The latter were lacking in the plasmid carrying the genes responsible for the ecological transition. Instead, adaptation targeted the same set of genes leading to the cooption of the same quorum-sensing system. Our results provide evidence for similarities in experimental and natural evolutionary transitions and highlight the potential of comparisons between both processes to understand symbiogenesis.

evolutionary biology↗