Transcriptional natural variation at FLM induces synergistic pleiotropy in Arabidopsis thaliana

Investigating the evolution of complex phenotypes and the underlying molecular bases of their variation is critical to understand how organisms adapt to the environment. We used leaf growth as a model trait as it is highly integrative of internal and external cues and relies on functions at different levels of the plant organization. Applying classical quantitative genetics on a recombinant inbred line population derived from a Can-0 x Col-0 cross, we identified the MADS-box transcription factor FLOWERING LOCUS M (FLM) as a player of the phenotypic variation for leaf growth and colour. Interestingly, we showed that allelic variation at FLM modulates plant growth strategy along the leaf economics spectrum, a trade-off between resource acquisition and resource conservation observable across thousands of plant species. We demonstrated that the functional differences at FLM relies on a single intronic substitution, disturbing transcript splicing and leading to a low expression of the active FLM transcript. Using phenotypic and climatic data across Arabidopsis natural populations, our work shows how noncoding genetic variation of a single gene may be adaptive through synergistic pleiotropy.