Search bioRxiv⌕ Search

Biology subjects

Frachon, L.

Publications and source records attributed to Frachon, L..

9 recordsLinked to original sources

Metabolism and chemical diversity evolve in response to pollinator availability

Phytochemistry is a core player in shaping plant-pollinator networks and pollination services. Yet, little is known about the dynamic evolution of phytochemical traits in response to limited pollinator access, especially concerning chemical diversity. We combined an evolutionary experiment manipulating pollinator access with predictive metabolomics to uncover evolutionary changes in phytochemical traits of Brassica rapa. Our results unveiled chemical changes in both leaf and flower chemistry. Moreover, plants under selection by limited pollinator access showed a decreased chemical richness and diversity and a modulated primary and specialised metabolism, which could be used to predict pollinator access with 88% accuracy. Chemical indices and metabolites responding to pollinator access were associated with variation in flowering time and performance of outcrossing flowers. Our findings provide key insights into the influence of pollinator access on plant chemistry and indicate a risk of pollinator decline and losses of chemical diversity for plant-pollinator network structure and ecosystem dynamics.

ecology↗

Phenotypic evolutionary response to temporally limited pollinator access in Brassica rapa

Plant-pollinator interactions are essential for plant reproductive success and pollinator food supply. However, the ongoing pollinator decline threatens many wild and cultivated flowering plants, urgently requiring studies on its impact on plant populations and their potential evolutionary responses. We combined an experimental evolution with a resurrection approach to test phenotypic evolutive changes in response to artificially limited access of plants to natural pollinators in a common garden setting using Brassica rapa. After six generations, we detected putative adaptive responses to the pollination treatments, including changes in phenology, floral morphology and flower volatile organic compounds, associated with changes in overall attractiveness to hoverflies. Although the generalist plant B. rapa shows ability to rapidly respond to strong limitations to its natural pollinator community, the observed decrease of fitness could threaten the population.

evolutionary biology↗

Biotic interactions promote local adaptation to soil in plants

Although different ecological factors shape adaptative evolution in natural habitats, we know little about how their interactions impact local adaptation. Here we used eight generations of experimental evolution with outcrossing Brassica rapa plants as a model system, in eight treatment groups that varied in soil type, herbivory (with/without aphids), and pollination mode (hand- or bumblebee-pollination), to study how biotic interactions affect local adaptation to soil. First, we show that several plant traits evolved in response to biotic interactions in a soil-specific way. Second, using a reciprocal transplant experiment, we demonstrate that significant local adaptation to soil-type evolved in the "number of open flowers", a trait used as a fitness proxy, but only in plants that evolved with herbivory and bee pollination. Whole genome re-sequencing of experimental lines revealed that biotic interactions caused a 10-fold increase in the number of SNPs across the genome with significant allele frequency change, and that alleles with opposite allele frequency change in different soil types (antagonistic pleiotropy) were most common in plants with an evolutionary history of herbivory and bee pollination. Our results demonstrate that the interaction of mutualists and antagonists can facilitate local adaptation to soil type through antagonistic pleiotropy.

evolutionary biology↗

Plant genetic bases explaining microbiota diversity shed light into a novel holobiont generalist gene theory

Plants as animals are strictly associated with a cortege of microbial communities influencing their health, fitness and evolution. Therefore, scientists refer to all living organisms as holobionts; complex genetic units that coevolve simultaneously. This is what has been recently proposed as the hologenome theory of evolution. This exciting and attractive theory has important implications on animal and plant health; however, it still needs consistent proof to be validated. Indeed, holobionts are still poorly studied in their natural habitats where coevolution and natural selective processes occur. Compared to animals and crops, wild plant populations are an excellent and unique model to explore the hologenome theory. These sessile holobionts have strictly coevolved with their microbiota for decades and natural selection and adaptive processes acting on wild plants are likely to regulate the plant-microbe interactions. Here we conducted for the first time a microbiota survey, plant genome sequencing and Genome-Environmental Analysis (GEA) of 26 natural populations of the non-model plant species Brassica rapa. We collected plants over two seasons in Italy and France, and analyzed the microbiota on two plant compartments (root and rhizosphere). We identified that plant compartment and season modulate B. rapa microbiota. More importantly, when conducting GEA we evidenced neat peaks of association correlating with both fungal and bacterial microbiota. Surprisingly, we found 13 common genes between fungal and bacterial diversity descriptors that we referred under the name of Holobiont Generalist Genes (HGG). These genes might strongly regulate the diversity and composition of plant microbiota at the inter-kingdom level. Significance StatementThe novel hologenome concept claims that hosts and their associated microbes (considered as holobionts) are a unique evolutionary unit on which natural selection acts. Thus, the hologenome theory assumes that hosts and microbiomes simultaneously coevolve. This novel vision of universal evolutionary entities is promising for both animal and plant health purposes. However, it is still quietly controversial as it suffers from a lack of tangible evidence. How can we enrich the debate on holobionts? How can we translate this concept in discoveries that can change farming practices? Our study is filling the gaps of the hologenome theory by showing that certain genes under natural selection and regulating plant microbiota are generalist in response to fungal and bacterial communities.

evolutionary biology↗

Uncovering genes involved in pollinator-driven mating system shifts and selfing syndrome evolution in Brassica rapa

BackgroundShifts in pollinator occurrence and their pollen transport effectiveness drive the evolution of mating systems in flowering plants. A decline in pollinator numbers can lead to the phenotypic evolution of floral traits favoring self-pollination (selfing syndrome). Understanding the genomic basis involved in such shifts of the mating system is crucial for predicting a species persistence or extinction under changing biotic and abiotic stressors in natural populations. We investigated loci showing high genetic differentiation before and after selection in fast-cycling Brassica rapa that were associated with rapid phenotypic evolution toward the selfing syndrome (reduction in petal width, stamen and pistil length, and herkogamy). Combining a genotyping-by-sequencing (GBS) approach with a genome-wide association study (GWAS), we shed light onto the genetic basis associated with the mating system shift over nine generations of pollination by Episyphrus balteatus (hoverflies), an abundant pollinator of B. rapa. Moreover, we functionally validated the involvement of candidate genes associated with changes in floral morphology by studying corresponding mutants in the model plant Arabidopsis thaliana. ResultsWe found that the mating system of B. rapa shifted from predominantly outcrossing to mixed mating with high rates of autonomous selfing, accompanied by a rapid reduction of floral morphological traits and herkogamy involving many loci. We found 31 candidate genes associated with the affected traits that were involved in a wide range of functions from DNA/RNA binding to transport. Our functional validation in A. thaliana confirmed that four of the identified genes are indeed involved in regulating the size of floral organs. Interestingly, two genes, both coding for the same protein complex responsible for active DNA methylation were successfully validated and closely linked to two correlated phenotypic traits, namely pistil and stamen length. ConclusionsAltogether, our study shows that hoverfly pollination leads to rapid evolutionary changes of the mating system through polygenic changes, highlighting the importance of using genomic approaches to understand pollinator-driven plant adaptation.

plant biology↗

The genetic architecture of adaptation to leaf and root bacterial microbiota in Arabidopsis thaliana

Understanding the role of host genome in modulating microbiota variation is a need to shed light into the holobiont theory and overcome the current limits on the description of host-microbiota interactions at the genomic and molecular levels. However, the host genetic architecture structuring microbiota is only partly described in plants. In addition, most association genetic studies on microbiota are often carried out outside the native habitats where the host evolve and the identification of signatures of local adaptation on the candidate genes has been overlooked. To fill these gaps and dissect the genetic architecture driving adaptive plant-microbiota interactions, we adopted a Genome-Environmental-Association (GEA) analysis on 141 whole-genome sequenced natural populations of Arabidopsis thaliana characterized in situ for their leaf and root bacterial communities and a large range of environmental descriptors (i.e. climate, soil and plant communities). Across 194 microbiota traits, a much higher fraction of among-population variance was explained by the host genetics than by ecology, with the plant neighborhood as the main ecological driver of microbiota variation. Importantly, the relative importance of host genetics and ecology expressed a phylogenetic signal at the family and genus level. In addition, the polygenic architecture of adaptation to bacterial communities was highly flexible between plant compartments and seasons. Relatedly, signatures of local adaptation were stronger on QTLs of the root microbiota in spring. Finally, we provide evidence that plant immunity, in particular the FLS2 gene, is a major source of adaptive genetic variation structuring bacterial assemblages in A. thaliana.

microbiology↗

Genomic local adaptation of a generalist plant species to pollinator communities and abiotic factors

The reproductive success of generalist flowering plants is influenced by a complex ecological network that includes interactions with a diverse pollinator community and abiotic factors. However, knowledge about of the adaptative potential of plants to complex ecological networks and the underlying genetic mechanisms is still limited. Based on a pool-sequencing approach of 21 natural populations of Brassica incana in Southern Italy, we combined a genome-environmental association analysis with a genome scan for signature of selection to discover genetic variants associated with ecological variation. We demonstrated that B. incana is locally adapted both to the identity of functional categories and overall pollinator interactions. Interestingly, we observed only few shared candidate genes associated with long-tongue bees, soil texture, and temperature variation. Our results highlight the genomic architecture of generalist flowering plant adaptation to complex biotic interactions, and the importance of considering multiple environmental factors to describe the adaptive landscape of plant populations.

plant biology↗

Rapid genomic evolution in Brassica rapa with bumblebee selection in experimental evolution

BackgroundInsect pollinators shape rapid phenotypic evolution of traits related to floral attractiveness and plant reproductive success. However, the underlying genomic changes remain largely unknown despite their importance in predicting adaptive responses to natural or to artificial selection. Based on a nine-generation experimental evolution study with fast cycling Brassica rapa plants adapting to bumblebees, we investigate the genomic evolution associated with the previously observed parallel phenotypic evolution. In this current evolve and resequencing (E&R) study, we conduct a genomic scan of the allele frequency changes along the genome in bumblebee-pollinated and hand-pollinated plants and perform a genomic principal component analysis (PCA). ResultsWe highlight rapid genomic evolution associated with the observed phenotypic evolution mediated by bumblebees. Controlling for genetic drift, we observe significant changes in allelic frequencies at multiple loci. However, this pattern differs according to the replicate of bumblebee-pollinated plants, suggesting putative non-parallel genomic evolution. Finally, our study underlines an increase in genomic differentiation implying the putative involvement of multiple loci in short-term pollinator adaptation. ConclusionsOverall, our study enhances our understanding of the complex interactions between pollinator and plants, providing a steppingstone towards unravelling the genetic basis of plant genomic adaptation to biotic factors in the environment.

evolutionary biology↗

In situ relationships between microbiota and potential pathobiota in Arabidopsis thaliana

A current challenge in microbial pathogenesis is to identify biological control agents that may prevent and/or limit host invasion by microbial pathogens. In natura, hosts are often infected by multiple pathogens. However, most of the current studies have been performed under laboratory controlled conditions and by taking into account the interaction between a single commensal species and a single pathogenic species. The next step is therefore to explore the relationships between host-microbial communities (microbiota) and microbial members with potential pathogenic behavior (pathobiota) in a realistic ecological context. In the present study, we investigated such relationships within root and leaf associated bacterial communities of 163 ecologically contrasted Arabidopsis thaliana populations sampled across two seasons in South-West of France. In agreement with the theory of the invasion paradox, we observed a significant humped-back relationship between microbiota and pathobiota -diversity that was robust between both seasons and plant organs. In most populations, we also observed a strong dynamics of microbiota composition between seasons. Accordingly, the potential pathobiota composition was explained by combinations of season-specific microbiota OTUs. This result suggests that the potential biomarkers controlling pathogens invasion are highly dynamic.

microbiology↗