Multi-scale characterization of cold response reveals immediate and long-term impacts on cell physiology up to seed composition

Early sowing can help summer crops escape drought and can mitigate the impacts of climate change on them, but it exposes them to cold stress during initial developmental stages, which has both immediate and long-term effects on development and physiology. To understand how early night-chilling stress impacts plant development and the yield, we studied the reference sunflower line XRQ under controlled, semi-controlled and field conditions. We performed high-throughput imaging of the whole plant parts and obtained physiological and transcriptomic data from leaves, hypocotyls and roots. We observed morphological reductions in early stages under field and controlled conditions, with a decrease in root development, an increase in reactive oxygen species content in leaves and changes in lipid composition in hypocotyls. A long-term increase in leaf chlorophyll suggests a stress memory mechanism that was supported by transcriptomic induction of histone coding genes. We highlighted leaf transcriptomes in cold-acclimation genes such as chaperone, heat shock and late embryogenesis abundant proteins. We identified genes in hypocotyls involved in lipid, cutin, suberin and phenylalanine ammonia lyase biosynthesis and ROS scavenging. This comprehensive study describes new phenotyping methods and candidate genes to understand phenotypic plasticity better in response to chilling and study stress memory in sunflower.