Epigenetic Stress Memory and Adaptive Responses in Plants: Metabolic Reprogramming, Organelle Signalling and Systemic Acclimation.

Abstract

Plants frequently encounter recurring, sequential and combined environmental stresses, yet their adaptive capacity cannot be explained solely by immediate signalling and short-term acclimation. Increasing evidence indicates that prior stress exposure can leave molecular, metabolic and physiological imprints that alter the magnitude, speed and quality of later responses, thereby giving rise to stress memory and adaptive plasticity. In plants, these persistent states are increasingly linked to epigenetic regulation, including changes in chromatin accessibility, histone modifications, DNA methylation, RNA-directed DNA methylation and non-coding RNA-mediated control. However, stress memory is not determined by chromatin regulation alone. It is also shaped by metabolic and cellular reprogramming involving osmolyte accumulation, redox buffering, energy redistribution, protein quality control, autophagy, selective protein turnover and membrane remodelling, all of which help sustain cellular homeostasis during stress and recovery. In parallel, chloroplasts, mitochondria and the endoplasmic reticulum act as stress-sensitive organelles that relay their functional state to the nucleus through retrograde signalling, while long-distance systemic communication mediated by reactive oxygen species, calcium waves, electrical and hydraulic signals, hormones and peptides coordinates whole-plant acclimation. This review synthesizes these layers into a unified framework and argues that plant resilience under fluctuating environments depends on the interaction between stress memory, metabolic plasticity, organelle-derived signalling and systemic acquired acclimation. Particular attention is given to the distinction between transient acclimation and true memory, the balance between maintenance and resetting of stress-induced states and the developmental and fitness trade-offs associated with persistent preparedness. This review also highlights major gaps that continue to limit the field, including the lack of standardized criteria for defining stress memory, insufficient causal validation of epigenetic marks, weak integration of chromatin and metabolic states with whole-plant phenotypes, and the limited translation of memory-associated mechanisms into crop performance under realistic field conditions. Overall, this review provides a comprehensive framework for understanding how plants not only respond to stress, but also encode, retain and deploy information from prior exposure to optimize subsequent adaptation.