Identification of the genetic bases of plant-plant cooperation in the model plant Arabidopsis thaliana

Overview & Synopsis

Despite the importance of plant-plant interactions in the functioning of both natural ecosystems and agro-ecosystems, studies on plant-plant interactions still have two major gaps to be addressed, that is (i) the genetics of natural variation of plant-plant interactions and (ii) the relative importance of positive interactions within plant species. After writing two reviews on the state-of- the-art related to these gaps, I decided to understand the adaptive genetic bases of intraspecific positive plant-plant interactions in Arabidopsis thaliana at two geographical scales. To do so, I adopted an interdisciplinary approach between quantitative genetics, ecology and genome-wide association mapping. Firstly, based on a field experiment designed to study natural variation of genotype-by-genotype interactions among 52 whole-genome sequenced natural populations from the Midi-Pyrénées region, I identified two different strategies of positive interactions, i.e. kin cooperation and overyielding. Natural variation of positive interactions among these populations were mainly associated with biotic ecological factors varying at a fine spatial scale, such as presence of commensal bacteria or Shannon index of plant communities in the native habitats. Importantly, QTLs associated with variation of positive interactions were significantly enriched in genomic signatures of local adaptation. Secondly, based on a greenhouse experiment using 195 whole-genome sequenced accessions collected in a local French population located in a highly diverse and competitive environment, we revealed the existence of certain genotypic combinations that were benefitting reciprocally to each other’s presence, resulting in a ‘super overyielding’ strategy. Importantly, genetic dissimilarity at the QTLs associated with this strategy was detected for such pairs, supporting the ‘compatibility genes’ hypothesis as underlying this ‘super overyielding’ strategy. Finally, at both geographical scales, we detected a predominance of metabolism related gene functions underlying natural variation of positive interactions, which might be explained by their putative roles in (i) recruitment of similar microbiota by kin to explain kin cooperation, and (ii) potential complementary metabolite cross-feeding to explain overyielding. The next step is undoubtedly cloning of the candidate genes to identify causal associations, thereby allowing to start getting a glimpse on the genetic and molecular landscape associated with positive interactions in A. thaliana.