The Genomic Architecture of Competitive Response of Arabidopsis thaliana Is Highly Flexible Among Plurispecific Neighborhoods

Plants are daily challenged by multiple abiotic and biotic stresses. A major biotic constraint corresponds to competition with other plant species. Although plants simultaneously interact with multiple neighboring species throughout their life cycle, there is still very limited information about the genetics of the competitive response in the context of plurispecific interactions. Using a local mapping population of Arabidopsis thaliana, we set up a genome wide association study (GWAS) to estimate the extent of genetic variation of competitive response in 12 plant species assemblages, based on three competitor species (Poa annua, Stellaria media, and Veronica arvensis). Based on five phenotypic traits, we detected strong crossing reaction norms not only between the three bispecific neighborhoods but also among the plurispecific neighborhoods. The genetic architecture of competitive response was highly dependent on the identity and the relative abundance of the neighboring species. In addition, most of the enriched biological processes underlying competitive responses largely differ among neighborhoods. While the RNA related processes might confer a broad range response toolkit for multiple traits in diverse neighborhoods, some processes, such as signaling and transport, might play a specific role in particular assemblages. Altogether, our results suggest that plants can integrate and respond to different species assemblages depending on the identity and number of each neighboring species, through a large range of candidate genes associated with diverse and unexpected processes leading to developmental and stress responses.