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.

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.

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.

BACKGROUND: Pre-exposing plants to abiotic stresses can induce stress memory, which is crucial for adapting to subsequent stress exposure. Although numerous genes involved in salt stress response have been identified, the understanding of memory responses to salt stress remains limited.
RESULTS: In this study, we conducted physiological and transcriptional assays on maize plants subjected to recurrent salt stress to characterize salt stress memory. During the second exposure to salt stress, the plants exhibited enhanced salt resistance, as evidenced by increased proline content and higher POD and SOD activity, along with decreased MDA content, indicative of physiological memory behavior. Transcriptional analysis revealed fewer differentially expressed genes and variations in response processes during the second exposure compared to the first, indicative of transcriptional memory behavior. A total of 2,213 salt stress memory genes (SMGs) were identified and categorized into four response patterns. The most prominent group of SMGs consisted of genes with elevated expression during the first exposure to salt stress but reduced expression after recurrent exposure to salt stress, or vice versa ([+ / -] or [- / +]), indicating that a revised response is a crucial process in plant stress memory. Furthermore, nine transcription factors (TFs) (WRKY40, WRKY46, WRKY53, WRKY18, WRKY33, WRKY70, MYB15, KNAT7, and WRKY54) were identified as crucial factors related to salt stress memory. These TFs regulate over 53% of SMGs, underscoring their potential significance in salt stress memory.
CONCLUSIONS: Our study demonstrates that maize can develop salt stress memory, and the genes identified here will aid in the genetic improvement of maize and other crops.

Climate change-induced extreme weather events (heat, cold, drought, and flooding) will severely affect crop production. Increasing the resilience of crops to fluctuating environmental conditions is critically important. Here, we report that nanomaterials (NMs) with reactive oxygen species (ROS)-generating properties can be used as seed priming agents to simultaneously enhance the tolerance of maize seeds and seedlings to diverse and even multiple stresses. Maize seeds primed with 40 mg/L silver nanoparticles (AgNPs) exhibited accelerated seed germination and an increased germination rate, greater seedling vigor, and better seedling growth under drought (10% and 20% PEG), saline (50 and 100 mM NaCl), and cold (15 °C) stress conditions, indicating enhanced resilience to diverse stresses. Importantly, maize resistance to simultaneous multiple stresses (drought and cold, drought and salt, and salt and cold) was markedly enhanced. Under drought conditions, seed priming significantly boosted root hair density and length (17.3-82.7%), which enabled greater tolerance to water deficiency. RNA-seq analysis reveals that AgNPs seed priming induced a transcriptomic shift in maize seeds. Plant hormone signal transduction and MAPK signaling pathways were activated upon seed priming. Importantly, low-cost and environmentally friendly ROS-generating Fe-based NMs (Fe2O3 and Fe3O4 NPs) were also demonstrated to enhance the resistance of seeds and seedlings to drought, salt, and cold stresses. These findings demonstrate that a simple seed priming strategy can be used to significantly enhance the climate resilience of crops through modulated ROS homeostasis and that this approach could be a powerful nanoenabled tool for addressing worsening food insecurity.

With global climate change, the frequency and intensity of waterlogging events are increasing due to frequent and heavy precipitation. Little is known however about the response of plants to repeated waterlogging stress events. The aim is to clarify physiological regulation mechanisms of tomato plants under repeated waterlogging stress, and whether Trichoderma harzianum can alleviate waterlogging injury. We identified two genotypes of tomato, \'MIX-002\' and \'LA4440\', as waterlogging tolerant and sensitive genotypes, respectively, based on plant biomass accumulation. The two tomato genotypes were subjected to a waterlogging priming treatment for 2 days (excess water for 1 cm above substrate surface) followed by a recovery stage for 2 days, and then a second waterlogging stress for 5 days (excess water for 1 cm above substrate surface) followed by a second recovery stage for 3 days. Leaf physiological, plant growth parameters, and the expression of five key genes were investigated. We found that the two genotypes responded differently to waterlogging priming and stress in terms of photosynthesis, reactive oxygen species (ROS), and osmotic regulatory mechanisms. Waterlogging stress significantly increased H2O2 content of \'MIX-002\', while that of \'LA4440\' had no significant change. Under waterlogging stress, photosynthesis of the two genotypes treated with waterlogging priming returned to the control level. However, Trichoderma harzianum treatment during the second recovery stage did not show positive mitigative effects. The plants of \'LA4440\' with priming showed lower peroxidase (POD) activity and proline content but higher H2O2 content than that without priming under waterlogging stress. Under waterlogging stress with priming as compared to without priming, SODCC2 was downregulated in two tomatoes, and AGR2 and X92888 were upregulated in \'MIX-002\' but downregulated in \'LA4440\'. Overall, the two tomato genotypes exhibited distinct photosynthetic, ROS and osmotic regulatory mechanisms responding to the waterlogging stress. Waterlogging priming can induce stress memory by adjusting stomatal conductance, sustaining ROS homeostasis, regulating osmotic regulatory substances and key gene expressions mediated by H2O2, and thus alleviate the damage on tomato photosynthesis when waterlogging reoccurred.

Plants have evolved to adapt and grow in hot and cold climatic conditions. Some also adapt to daily and seasonal temperature changes. Epigenetic modifications play an important role in regulating plant tolerance under such conditions. DNA methylation and post-translational modifications of histone proteins influence gene expression during plant developmental stages and under stress conditions, including cold and heat stress. While short-term modifications are common, some modifications may persist and result in stress memory that can be inherited by subsequent generations. Understanding the mechanisms of epigenomes responding to stress and the factors that trigger stress memory is crucial for developing climate-resilient agriculture, but such an integrated view is currently limited. This review focuses on the plant epigenetic stress memory during cold and heat stress. It also discusses the potential of machine learning to modify stress memory through epigenetics to develop climate-resilient crops.

UNASSIGNED: As precipitation patterns are predicted to become increasingly erratic, the functional maintenance of warm-temperate forests constitutes a key challenge for forest managers. In this study, 2-year-old Quercus acutissima seedlings were selected to elucidate the mechanisms whereby they respond to soil water fluctuations and the drought hardening effects on plant carbohydrate dynamics.
UNASSIGNED: Seedlings were trained under different soil water conditions for 2 months: drought (D), well-watered (W), 1-month drought and then 1-month well-watered (D-W), and 1-month well-watered and then 1-month drought (W-D). The functional traits involved in water- and carbon-use strategies were explored at the end of the hardening period. Compared with seedlings in group W, seedlings in groups D, D-W, and W-D had increased potential for carbon uptake (i.e., light saturated point, maximum ribulose-1,5-bisphosphate (RuBP) saturated rate, and electron transport rate) and water uptake (i.e., fine root-to-coarse root ratio) and downregulated growth and mitochondrial respiration to decrease carbon consumption. After water fluctuation hardening, we performed a successional dry-down experiment for 1 month to detect carbohydrate dynamics and explore the acclimation caused by prior hardening.
UNASSIGNED: Our results revealed that there were more soluble sugars allocated in the leaves and more starch allocated in the stems and roots of seedlings hardened in the D, W-D, and D-W treatments than that of seedlings hardened in the W treatment. No significant changes in total non-structural carbohydrates were found. In addition, we found near-zero (seedlings trained by D and D-W treatments) or negative (seedlings trained by W-D treatment) growth of structural biomass at the end of the dry-down experiment, which was significantly lower than that of W-hardened seedlings. This suggests that there was a shift in allocation patterns between carbon storage and growth under recurrent soil drought, which can be strengthened by drought memory. We conclude that Q. acutissima seedlings adjusted water- and carbon-use strategies in response to water fluctuations, whereas stress memory can enhance their overall performance in reoccurring drought. Therefore, taking advantage of stress memory is a promising management strategy in forest nurseries, and drought-trained seedlings might be more suitable for afforestation practices in sites characterized by fluctuating soil water content, considering the ongoing global climatic changes.

Plants face various adverse environmental conditions, particularly with the ongoing changes in global climate, which drastically affect the growth, development and productivity of crops. To cope with these stresses, plants have evolved complex mechanisms, and one of the crucial ways is to develop transcriptional memories from stress exposure. This induced learning enables plants to better and more strongly restart the response and adaptation mechanism to stress when similar or dissimilar stresses reoccur. Understanding the molecular mechanism behind plant transcriptional memory of stress can provide a theoretical basis for breeding stress-tolerant crops with resilience to future climates. Here we review the recent research progress on the transcriptional memory of plants under various stresses and the applications of underlying mechanisms for sustainable agricultural production. We propose that a thorough understanding of plant transcriptional memory is crucial for both agronomic management and resistant breeding, and thus may help to improve agricultural yield and quality under changing climatic conditions.