Gene downregulation and photosynthetic disruption in Lactuca sativa under simulated microgravity and hypomagnetic field stress

• Lettuce shows distinct stress responses to altered magnetic fields and microgravity. • Gene changes reveal core plant adaptation to diverse stressors. • Microgravity and hypomagnetism impact key cellular processes. • Our results suggest plant resilience for space agriculture goals. • Molecular analysis details plant adaptation to extreme environments. Terrestrial plants evolved under constant gravity and a dynamic geomagnetic field (GMF). We investigated lettuce ( Lactuca sativa L.) responses to hypomagnetic fields (hMF) and simulated microgravity (s-µG) using a Random Positioning Machine and a Triaxial Helmholtz Coil System. Morphological, biochemical, and transcriptomic analyses revealed significant gene regulatory changes (P < 0.05, Log2 fold change >1 or <-1) impacting energy metabolism, ion homeostasis, and stress responses. hMF induced a targeted stress response, altering root architecture, reducing chlorophyll, and modulating reactive oxygen species (ROS), reflecting resource conservation. Conversely, s-µG triggered a systemic reorganization of cellular architecture, disrupting protein processing, organelle positioning, and photosynthetic efficiency. Differential ROS and non-photochemical quenching (NPQ) responses highlighted unique adaptive challenges. Despite these differences, shared gene expression patterns revealed core adaptive mechanisms, showcasing lettuce's ability to activate conserved pathways under diverse stressors. hMF upregulated genes related to stress and energy management, while downregulating photosynthesis related genes. s-µG downregulated genes related to cellular functions. Notably, s-µG induced a complex reprogramming, characterized by selective metabolic activation and broad suppression of essential processes. Our findings provide critical insights into plant adaptation to altered environments, suggesting plant resilience in terrestrial and extraterrestrial contexts.