Plant Stress Memory Across Epigenetic, Metabolic, and Microbiome Layers: From Causal Evidence to Adaptive Resilience

Environmental history can modify how plants respond to later challenges, yet the biological states that retain and recall such information are not equally resolved. This review evaluates plant stress memory across epigenetic and transcriptional regulation, stress-conditioned metabolic states, and microbiome-associated environmental legacies using an explicit evidence hierarchy. We distinguish four progressively stronger criteria: persistence after stress removal, altered responsiveness upon rechallenge, a biologically relevant functional consequence, and perturbation-based support linking a proposed carrier or maintenance mechanism to recall. Selected chromatin systems currently provide the clearest causal examples, whereas metabolic states are more often supported as maintainers, amplifiers, or readouts of memory and microbiome-associated states are frequently better classified as persistent ecological or microbial legacies. We further assess established pairwise interactions among metabolism, chromatin regulation, root exudation, and microbial feedback while emphasizing that these connections do not yet demonstrate a universal epigenome-metabolome-microbiome memory circuit. The adaptive value of retained information depends on stress identity, sequence, recurrence, genotype, duration, and cost. Memory can improve stress tolerance and recovery, remain neutral, or reduce plasticity when obsolete information persists. We therefore frame adaptive resilience as an outcome of selective retention, efficient recall, and timely resetting rather than maximal memory strength. Future progress will require recovery-phase perturbation, longitudinal and spatial multi-omics, dynamic phenotyping, microbiome transfer and synthetic-community experiments, and field validation across genotypes and realistic stress sequences. For crop improvement, the central objective should be tunable stress memory that preserves useful environmental information without imposing persistent growth or yield penalties.

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