Structural variation in the IAMH2 3′ UTR underlies hypocotyl elongation during light adaptation in Arabidopsis thaliana

Abstract

Plant hypocotyls are central to seedling establishment in variable light environments. Although core photoreceptor pathways regulating hypocotyl elongation are well defined, the molecular basis of natural variation in this trait—particularly through posttranscriptional regulation—remains poorly understood. Here, we report that a high-altitude, high-light-adapted Arabidopsis ecotype from Tibet exhibits longer hypocotyls under low light compared to a low-altitude ecotype from Sichuan. Using recombinant inbred lines combined with fine-mapping and near-isogenic line validation, we identified the major locus LA1 (Light Adaptation 1) and pinpointed IAMH2 as the causal gene. Full-length transcriptomics revealed a natural structural variant in the IAMH2 3′ UTR of high-altitude ecotypes that alters its length and disrupts a poly(U) motif. We further show that in low-altitude ecotypes, the RNA-binding proteins C3H14/C3H15 directly bind this poly(U)-rich region to posttranscriptionally downregulate IAMH2 mRNA levels, thereby attenuating IAMH2-dependent IAA accumulation and hypocotyl elongation. Analysis of 38 globally representative ecotype genomes confirmed that IAMH2 3′ UTR variation correlates with light intensity and elevation, supporting its role in environmental adaptation. Collectively, our work reveals a previously unknown C3H14/C3H15–IAMH2 posttranscriptional module that dynamically adjusts hypocotyl elongation in response to light, providing new insights into the plasticity and adaptive evolution of seedling photomorphogenesis.