In the face of rising global temperatures, the mechanisms behind an organism\'s ability to acclimate to heat stress remain enigmatic. The rice leaf folder, Cnaphalocrocis medinalis, traditionally viewed as temperature-sensitive, paradoxically exhibits robust larval acclimation to heat stress. This study used the heat-acclimated strain HA39, developed through multigenerational exposure to 39°C during the larval stage, and the unacclimated strain HA27 reared at 27°C to unravel the transgenerational effects of heat acclimation and its regulatory mechanisms. Heat acclimation for larvae incurred a fitness cost in pupae when exposed to high temperature, yet a significant transgenerational effect surfaced, revealing heightened fitness benefit in pupae from HA39, even without additional heat exposure during larval recovery at 27°C. This transgenerational effect exhibited a short-term memory, diminishing after two recovery generations. Moreover, the effect correlated with increased superoxide dismutase (SOD) enzyme activity and expression levels of oxidoreductase genes, representing physiological and molecular foundations of heat acclimation. Heat-acclimated larvae displayed elevated DNA methylation levels, while pupae from HA39, in recovery generations, exhibited decreased methylation indicated by the upregulation of a demethylase gene and downregulation of two methyltransferase genes at high temperatures. In summary, heat acclimation induces DNA methylation, orchestrating heat-stress memory and influencing the expression levels of oxidoreductase genes and SOD activity. Heat-stress memory enhances the acclimation of the migratory insect pest to global warming.

The persistence of plant populations depends crucially on successful regeneration. Yet, little is known about the effects of consecutive winter and spring frost events on the regeneration stage of trees from different seed sources, although this will partly determine the success of climate warming-driven poleward range shifts. In a common garden experiment with European beech (Fagus sylvatica) seedlings from winter 2015/2016 to autumn 2017, we studied how simulated successive spring and winter frost events affect leaf-out dates, growth performance, and survival rates of 1- to 2-year-old seedlings from provenances differing in climate at origin. We further investigated the combined effects of successive frost events. The first spring frost after germination led to a mortality rate up to 75%, resulting in reduced seedling numbers but better frost tolerance of the survivors, as reflected in a weaker impact of the following winter frost event in the survivors compared to the non-acclimated control. Final plant height was most strongly reduced by the spring frost in the second year. The winter frost event delayed leaf-out by up to 40 days, leading to severe growth impairment in 2017. Our results indicate partly successful frost acclimation and/or the selection of frost-hardier individuals, because the negative growth effects of consecutive frost events did not add up after exposure to more than one event. Both mechanisms may help to increase the frost tolerance of beech offspring. Nevertheless, mortality after the first spring frost was high, and frost exposure generally caused growth reductions. Thus, achieving higher frost tolerance may not be sufficient for beech seedlings to overcome frost-induced reductions in competitive strength caused by winter frost damage and delayed leaf enfolding.

Transcriptional memory allows organisms to store information about transcriptional reprogramming in response to a stimulus. In plants, this often involves the response to an abiotic stress, which in nature may be cyclical or recurring. Such transcriptional memory confers sustained induction or enhanced re-activation in response to a recurrent stimulus, which may increase chances of survival and fitness. Heat stress (HS) has emerged as an excellent model system to study transcriptional memory in plants, and much progress has been made in elucidating the molecular mechanisms underlying this phenomenon. Here, we review how histone turnover and transcriptional co-regulator complexes contribute to reprogramming of transcriptional responses.

With the advent of transcriptomic techniques involving single-stranded RNA sequencing and chromatin isolation by RNA purification-based sequencing, transcriptomic studies of coding and non-coding RNAs have been executed efficiently. These studies acknowledged the role of non-coding RNAs in modulating gene expression. Long non-coding RNAs (lncRNAs) are a kind of non-coding RNAs having lengths of >200 nucleotides, playing numerous roles in plant developmental processes such as photomorphogenesis, epigenetic changes, reproductive tissue development, and in regulating biotic and abiotic stresses. Epigenetic changes further control gene expression by changing their state to \"ON-OFF\" and also regulate stress memory and its transgenerational inheritance. With well-established regulatory mechanisms, they act as guides, scaffolds, signals, and decoys to modulate gene expression. They act as a major operator of post-transcriptional modifications such as histone and epigenetic modifications, and DNA methylations. The review elaborates on the roles of lncRNAs in plant immunity and also discusses how epigenetic markers alter gene expression in response to pest/pathogen attack and influences chromatin-associated stress memory as well as transgenerational inheritance of epigenetic imprints in plants. The review further summarizes some research studies on how histone modifications and DNA methylations resist pathogenic and pest attacks by activating defense-related genes.

High temperature is one of the most devastating environmental factors that severely impede plant growth multi-laterally and threatens global food security. Global warming and the predicted steady rise in temperature emphasize the urgent need to improve heat stress resilience of crop plants to meet the growing food demand. Although known for several years, a memory-based mechanism termed \"priming-induced stress tolerance\" or \"acquired stress tolerance\" has gained the attention of the plant science community in recent years. Thermopriming is one such phenomenon that enhances the plant tolerance to subsequent heat stress and promotes growth. The memory of the foregoing mild increase in temperature is captured and retained as dormant signals, which upon exposure to subsequent high temperature aids in mounting a faster, stronger, and sensitized response. Such acquired thermotolerance is more effective than the basal endurance of the plant due to altered molecular regulatory networks. Thereupon, thermopriming can be used as a convenient tool to study and improve plant response to heat stress. In this chapter, the protocol to study thermopriming-mediated short- and long-term acquired thermotolerance is described in detail.

Marine ecosystems are facing escalating environmental fluctuations owing to climate change and human activities, imposing pressures on marine species. To withstand recurring environmental challenges, marine organisms, especially benthic species lacking behavioral choices to select optimal habitats, have to utilize well-established strategies such as the antioxidant defense system (ADS) to ensure their survival. Therefore, understanding of the mechanisms governing the ADS-based response is essential for gaining insights into adaptive strategies for managing environmental challenges. Here we conducted a comparative analysis of the physiological and transcriptional responses based on the ADS during two rounds of \'hypersalinity-recovery\' challenges in two model congeneric invasive ascidians, Ciona robusta and C. savignyi. Our results demonstrated that C. savignyi exhibited higher tolerance and resistance to salinity stresses at the physiological level, while C. robusta demonstrated heightened responses at the transcriptional level. We observed distinct transcriptional responses, particularly in the utilization of two superoxide dismutase (SOD) isoforms. Both Ciona species developed physiological stress memory with elevated total SOD (T-SOD) and glutathione (GSH) responses, while only C. robusta demonstrated transcriptional stress memory. The regulatory distinctions within the Nrf2-Keap1 signalling pathway likely explain the formation disparity of transcriptional stress memory between both Ciona species. These findings support the \'context-dependent stress memory hypothesis\', emphasizing the emergence of species-specific stress memory at diverse regulatory levels in response to recurrent environmental challenges. Our results enhance our understanding of the mechanisms of environmental challenge management in marine species, particularly those related to the ADS.
UNASSIGNED: The online version contains supplementary material available at 10.1007/s42995-024-00228-y.

Plants have evolved interconnected regulatory pathways which enable them to respond and adapt to their environments. In plants, stress memory enhances stress tolerance through the molecular retention of prior stressful experiences, fostering rapid and robust responses to subsequent challenges. Mounting evidence suggests a close link between the formation of stress memories and effective future stress responses. However, the mechanism by which environmental stressors trigger stress memory formation is poorly understood. Here, we review the current state of knowledge regarding the RNA-based regulation on stress memory formation in plants and discuss research challenges and future directions. Specifically, we focus on the involvement of microRNAs (miRNAs), small interfering RNAs (siRNAs), long non-coding RNAs (lncRNAs), and alternative splicing (AS) in stress memory formation. miRNAs regulate target genes via post-transcriptional silencing, while siRNAs trigger stress memory formation through RNA-directed DNA methylation (RdDM). lncRNAs guide protein complexes for epigenetic regulation, and AS of pre-mRNAs is crucial to plant stress memory. Unraveling the mechanisms underpinning RNA-mediated stress memory formation not only advances our knowledge of plant biology but also aids in the development of improved stress tolerance in crops, enhancing crop performance and global food security.

Transgenerational plasticity in plants enables rapid adaptation to environmental changes, allowing organisms and their offspring to adapt to the environment without altering their underlying DNA. In this study, we investigated the plasticity of transgenerational salinity tolerance of rice plants using a reciprocal transplant experimental strategy. Our aim was to assess whether nongenetic environment-induced phenotypic modifications and transgenerational salinity affect the salinity tolerance of progeny while excluding nuclear genomic factors for two generations. Using salt-tolerant and salt-sensitive rice genotypes, we observed that the parentally salt-stressed salt-sensitive genotype displayed greater growth performance, photosynthetic activity, yield performance, and transcriptional responses than did the parentally nonstressed salt-sensitive plants under salt stress conditions. Surprisingly, salt stress-exposed salt-tolerant progeny did not exhibit as much salinity tolerance as salt stress-exposed salt-sensitive progeny under salt stress. Our findings indicate that the phenotypes of offspring plants differed based on the environment experienced by their ancestors, resulting in heritable transgenerational phenotypic modifications in salt-sensitive genotypes via maternal effects. These results elucidated the mechanisms underlying transgenerational plasticity in salinity tolerance, providing valuable insights into how plants respond to changing environmental conditions.

The influence of epigenetic factors on plant defense responses and the balance between growth and defense is becoming a central area in plant biology. It is believed that the biosynthesis of secondary metabolites can be regulated by epigenetic factors, but this is not associated with the formation of a \"memory\" to the previous biosynthetic status. This review shows that some epigenetic effects can result in epigenetic memory, which opens up new areas of research in secondary metabolites, in particular flavonoids. Plant-controlled chromatin modifications can lead to the generation of stress memory, a phenomenon through which information regarding past stress cues is retained, resulting in a modified response to recurring stress. How deeply are the mechanisms of chromatin modification and memory generation involved in the control of flavonoid biosynthesis? This article collects available information from the literature and interactome databases to address this issue. Visualization of the interaction of chromatin-modifying proteins with the flavonoid biosynthetic machinery is presented. Chromatin modifiers and \"bookmarks\" that may be involved in the regulation of flavonoid biosynthesis through memory have been identified. Through different mechanisms of chromatin modification, plants can harmonize flavonoid metabolism with: stress responses, developmental programs, light-dependent processes, flowering, and longevity programs. The available information points to the possibility of developing chromatin-modifying technologies to control flavonoid biosynthesis.

Drought priming is known to enhance plant low temperature tolerance, whereas polystyrene nanoplastic contamination exerts detrimental effects on plant growth. This study investigates the less-explored influence of nanoplastic contamination on cold stress tolerance in drought-primed plants. We compared the photosynthetic carbon assimilation, carbohydrate metabolism, reactive oxygen species metabolism, and grain yield between the non-primed and drought-primed wheat grown in both nanoplastic-contaminated and healthy soils. Our results reveal that the beneficial effects of drought priming on photosynthetic carbon assimilation and the efficiency of the \"water-water\" cycle were compromised in the presence of nanoplastics (nPS). Additionally, nPS exposure disturbed carbohydrate metabolism, which impeded source-to-sink transport of sugar and resulted in reduced grain yield in drought-primed plants under low temperature conditions. These findings unveil the suppression of nPS on drought-primed low-temperature tolerance (DPLT) in wheat plants, suggesting an intricate interplay between the induction of stress tolerance and responses to nPS contamination. The study raises awareness about a potential challenge for future crop production.