Reversible chromatin remodeling enables Prosopis cineraria survival under recurrent heat extremes

Recurrent seasonal heat and drought raise fundamental questions about how long-lived desert plants sustain physiological function across temperature extremes. We have used seasonal profiling at six time points with multilayered omics studies (Hi-C, transcriptomic, histone marks, and DNA methylation) to understand how Prosopis cineraria, a native Arabian desert legume tree, responds to different temperatures and the underlying mechanisms. A clear pattern emerges during peak heat. chromatin boundaries are selectively weakened, and candidate topological domains merge, activating clusters of heat-protective genes that gain active promoter and enhancer marks (H3K4me3 and H3K27ac). In the cool season, immune and developmental gene regulation is coupled with flowering, consistent with a temporal risk-strategy that shifts reproduction away from lethal heat. At the same time, promoter CHH methylation near transposable elements, together with reduced active promoter and enhancer marks (H3K4me3/H3K27ac), points to a proactive developmental phase rather than just surviving the stress. Integrating physiological data, we connect chromatin activation to an SA-ABA reciprocal seasonal profile, MIZ1-associated hydrotropism, and Stay-Green-mediated delayed senescence through chlorophyll retention. With Landscape genomics and phylogenetics, we further identified a housekeeping PEPC with a high predicted melting temperature that could sustain a malate-derived carbon supply, buffering metabolism under heat. Together, these findings reveal that reversible epigenetic gating enables desert trees to survive and recover from extreme seasonal stress.