Photosynthesis-related genetic and transcriptomic variations contribute to adaptive trait diversity in global Arabidopsis thaliana populations

Photosynthesis is the foundational process for carbon fixation in terrestrial ecosystems. Although allelic variations in photosynthesis-related genes have the potential to enhance carbon assimilation efficiency, their functional roles in local adaptation are still not well understood. In this study, we systematically examined the genetic and transcriptomic diversity among globally distributed natural accessions of Arabidopsis thaliana, focusing on 1,103 genes associated with photosynthetic pathways. By assembling chloroplast genomes from 28 representative accessions and integrating whole-genome and transcriptome sequencing data from over 1,000 accessions, we identified extensive allelic variation. Notably, 34.0% of these genes exhibited regulatory variations through expression quantitative trait locus mapping, including key components such as Rubisco and Rubisco activase. Functional validation demonstrated that overexpression of these genes increased cotyledon size and root length. Additionally, genome-wide and transcriptome-wide association studies revealed that natural selection acting on these allelic variations significantly contributes to local environmental adaptation. Our findings elucidate the connection between genetic variation in photosynthetic pathways and their ecological significance, providing valuable insights for optimizing carbon fixation in dynamic environments.