Plant environmental memory: implications, mechanisms and opportunities for plant scientists and beyond

Plants, being sessile organisms, have evolved extraordinary plasticity to cope with fluctuating environments. They continuously process environmental information, adjusting growth and development to optimize survival and reproduction. This capacity for information integration, extending to influence subsequent life stages or even future generations, is termed 'plant environmental memory.' This memory provides adaptive significance by optimizing future developmental trade-offs, although it may also constrain future development and survival. Because plant memory contributes to the realized phenotype, it is subject to natural selection and varies between populations depending on the environment, potentially playing a critical role in local adaptation. Recent research has revealed a sophisticated and multilayered molecular basis for plant memory, encompassing epigenetic modifications, genetic regulation, and metabolic processes. These mechanisms enable the storage of information in molecular forms, potentially persisting across generations. The reversible nature of plant memory is crucial, allowing for transient or stable (mitotically/meiotically) modifications, with dissipation of memory acting as a vital component. Abiotic and biotic stressors (pathogens, temperature extremes, drought, salinity) induce memory responses, often involving rapid tissue-specific changes in gene expression. Epigenetic modifications (histone modifications, DNA methylation) are key regulators, presenting a considerable potential for rapid and repeated adaptation, though challenges remain in identifying specific pathways and translating this information into strategies for climate change resilience. Mathematical modeling offers a crucial tool to understand plant memory, predict future responses, and guide management strategies in both natural and agricultural settings. The review explores the ecological and evolutionary consequences of plant memory, detailing molecular mechanisms and the role of computational biology in connecting environmental cues to responses.

The review draws on a substantial body of recent research demonstrating the intricate nature of plant memory. It highlights studies focusing on the ecological and evolutionary consequences of plants' responses to past environments, examining the molecular mechanisms (epigenetic, genetic, and metabolic) underlying within- and transgenerational phenotypic plasticity. The contributions of computational biology are showcased, specifically regarding the links between environmental cues and responses. Key examples from various plant species are used to illustrate these concepts, including studies on Arabidopsis thaliana, Populus, Quercus, Plantago, Oryza, Biscutella, Taraxacum, Nicotiana, and Raphanus, among others. These studies highlight the diverse ways in which plants adapt to both abiotic and biotic factors, emphasizing the importance of considering genotype-by-environment interactions.

This is a review article; therefore, it does not employ a traditional methodology section. The authors instead synthesized existing literature on plant environmental memory. Their approach involved a comprehensive search of relevant publications, focusing on studies that investigated the ecological consequences of plant memory, the underlying molecular mechanisms, and the application of mathematical models in understanding this phenomenon. The authors selected examples across various plant species and environmental contexts to represent the current state of knowledge and highlight areas requiring further investigation. Their analysis spans multiple disciplines, including ecology, evolution, molecular biology, and computational biology, showcasing the interdisciplinary nature of plant memory research.

The review underscores that plant environmental memory evolves when environmental cues accurately predict future selection pressures. Temporal autocorrelation (similar environmental conditions across time) is crucial for the evolution of both within-generation and transgenerational memory. The time span between the cue and selection event determines whether within-generation or transgenerational memory is favored. Several examples illustrate this, including studies showing that parental exposure to heat can advance flowering in subsequent generations, particularly under conditions of temporally autocorrelated heat stress. The research also demonstrates that biotic factors, such as herbivory and competition, can significantly influence the evolution of plant memory. For instance, maternal plants experiencing high water availability produce more dormant seeds, an adaptation likely driven by density dependence. Studies on herbivory resistance highlight the transgenerational inheritance of enhanced defenses, mediated by epigenetic mechanisms. The review further explores the molecular mechanisms involved in plant memory, focusing on the regulation of flowering time through vernalization (involving FLOWERING LOCUS C (FLC) and epigenetic modifications), heat stress memory (involving heat shock transcription factors and epigenetic modifications), and immune system priming (involving DNA methylation and small interfering RNAs). The intricate interplay between genetic and epigenetic regulation is a recurring theme. The role of metabolism, often underestimated, is discussed, showing its potential influence on both within-generation and transgenerational memory. The review advocates for mathematical modeling as an indispensable tool for understanding and predicting plant responses, highlighting both mechanistic models and machine learning approaches. Combining experimental data with modeling enhances predictive power and facilitates the identification of adaptive traits. The review concludes by identifying key research areas needing attention, including the exploration of plant responses in more complex natural conditions, the role of genotype × environment interactions, and a greater focus on long-lived species.

This review synthesizes a broad range of studies to present a comprehensive view of plant environmental memory. The findings emphasize the importance of temporal autocorrelation in environmental factors for the evolution of plant memory and the intricate interplay between various molecular mechanisms, particularly epigenetic regulation, and metabolic pathways. The significant contribution of mathematical modeling for prediction and understanding plant responses is discussed. The results highlight the adaptive significance of plant memory and its potential for applications in agriculture and conservation. The review addresses several outstanding questions regarding the molecular mechanisms and ecological implications of plant memory, promoting further interdisciplinary research.

Plant environmental memory is a complex yet essential phenomenon affecting plant adaptation and evolution. The review highlights the multilayered molecular mechanisms and ecological conditions underlying memory formation and transmission. Further research should focus on understanding plant memory in more realistic field settings, incorporating diverse genotypes and long-lived species. Integrating experimental data with sophisticated models will improve our ability to predict plant responses to climate change and guide agricultural and conservation strategies. Multidisciplinary collaboration is vital for advancing this critical area of research.

While comprehensive, the review acknowledges that research on plant memory is still ongoing. Many studies are conducted under controlled laboratory conditions, potentially overlooking the complexity of interactions in natural environments. The review also notes a relative lack of research on long-lived species and the need for long-term field studies to fully understand transgenerational memory effects. Finally, incorporating multiple environmental cues simultaneously in experiments and models is a challenge requiring further methodological development.