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.

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.

Highly repetitive adverse environmental conditions are encountered by plants multiple times during their lifecycle. These repetitive encounters with stresses provide plants an opportunity to remember and recall the experiences of past stress-associated responses, resulting in better adaptation towards those stresses. In general, this phenomenon is known as plant stress memory. According to our current understanding, epigenetic mechanisms play a major role in plants stress memory through DNA methylation, histone, and chromatin remodeling, and modulating non-coding RNAs. In addition, transcriptional, hormonal, and metabolic-based regulations of stress memory establishment also exist for various biotic and abiotic stresses. Plant memory can also be generated by priming the plants using various stressors that improve plants\' tolerance towards unfavorable conditions. Additionally, the application of priming agents has been demonstrated to successfully establish stress memory. However, the interconnection of all aspects of the underlying mechanisms of plant stress memory is not yet fully understood, which limits their proper utilization to improve the stress adaptations in plants. This review summarizes the recent understanding of plant stress memory and its potential applications in improving plant tolerance towards biotic and abiotic stresses.

Plants are continuously exposed to various environmental stresses. Because they can not escape stress, they have to develop mechanisms of remembering stress exposures somatically and passing it to the progeny. We studied the Arabidopsis thaliana ecotype Columbia plants exposed to cold stress for 25 continuous generations. Our study revealed that multigenerational exposure to cold stress resulted in the changes in the genome and epigenome (DNA methylation) across generations. Main changes in the progeny were due to the high frequency of genetic mutations rather than epigenetic changes; the difference was primarily in single nucleotide substitutions and deletions. The progeny of cold-stressed plants exhibited the higher rate of missense non-synonymous mutations as compared to the progeny of control plants. At the same time, epigenetic changes were more common in the CHG (C = cytosine, H = cytosine, adenine or thymine, G = guanine) and CHH contexts and favored hypomethylation. There was an increase in the frequency of C to T (thymine) transitions at the CHH positions in the progeny of cold stressed plants; because this type of mutations is often due to the deamination of the methylated cytosines, it can be hypothesized that environment-induced changes in methylation contribute to mutagenesis and may be to microevolution processes and that RNA-dependent DNA methylation plays a crucial role. Our work supports the existence of heritable stress response in plants and demonstrates that genetic changes prevail.

UNASSIGNED: To withstand high temperatures that would be lethal to a plant in the naïve state, land plants must establish heat stress memory. The acquisition of heat stress tolerance via heat stress memory in algae has only been observed in the red alga \'Bangia\' sp. ESS1.
UNASSIGNED: In this study, we further evaluated the intrinsic ability of this alga to establish heat stress memory by monitoring hydrogen peroxide (H2O2) production and examining the relationship between heat stress memory and the expression of genes encoding nitrogen transporters, since heat stress generally reduces nitrogen absorption. Next, genes encoding nitrogen transporters were selected from our unpublished transcriptome data of \'Bangia\' sp. ESS1.
UNASSIGNED: We observed a reduction in H2O2 content when heat stress memory was established in the alga. In addition, six ammonium transporter genes, a single-copy nitrate transporter gene and two urea transporter genes were identified. Two of these nitrogen transporter genes were induced by heat stress but not by heat stress memory, two genes showed heat stress memory-dependent expression, and one gene was induced by both treatments. Heat stress memory therefore differentially regulated the expression of the nitrogen transporter genes by reducing heat stress-inducible gene expression and inducing heat stress memory-dependent gene expression.
UNASSIGNED: These findings point to the functional diversity of nitrogen transporter genes, which play different roles under various heat stress conditions. The characteristic effects of heat stress memory on the expression of individual nitrogen transporter genes might represent an indispensable strategy for reducing the threshold of sensitivity to recurrent high-temperature conditions and for maintaining nitrogen absorption under such conditions in \'Bangia\' sp. ESS1.

Plants can be primed to withstand otherwise lethal heat stress (HS) through exposure to a preceding temporary and mild HS, commonly known as the \'thermopriming stimulus\'. Plants have also evolved mechanisms to establish \'memories\' of a previous stress encounter, or to reset their physiology to the original cellular state once the stress has ended. The priming stimulus triggers a widespread change of transcripts, proteins, and metabolites, which is crucial for maintaining the memory state but may not be required for growth and development under optimal conditions or may even be harmful. In such a scenario, recycling mechanisms such as autophagy are crucial for re-establishing cellular homeostasis and optimizing resource use for post-stress growth. While pivotal for eliminating heat-induced protein aggregates and protecting plants from the harmful impact of HS, recent evidence implies that autophagy also breaks down heat-induced protective macromolecules, including heat shock proteins, functioning as a resetting mechanism during the recovery from mild HS. This review provides an overview of the latest advances in understanding the multifaceted functions of autophagy in HS responses, with a specific emphasis on its roles in recovery from mild HS, and the modulation of HS memory.

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.

All species are well adapted to their environment. Stress causes a magnitude of biochemical and molecular responses in plants, leading to physiological or pathological changes. The response to various stresses is genetically predetermined, but is also controlled on the epigenetic level. Most plants are adapted to their environments through generations of exposure to all elements. Many plant species have the capacity to acclimate or adapt to certain stresses using the mechanism of priming. In most cases, priming is a somatic response allowing plants to deal with the same or similar stress more efficiently, with fewer resources diverted from growth and development. Priming likely relies on multiple mechanisms, but the differential expression of non-coding RNAs, changes in DNA methylation, histone modifications, and nucleosome repositioning play a crucial role. Specifically, we emphasize the role of BRM/CHR17, BRU1, FGT1, HFSA2, and H2A.Z proteins as positive regulators, and CAF-1, MOM1, DDM1, and SGS3 as potential negative regulators of somatic stress memory. In this review, we will discuss the role of epigenetic factors in response to stress, priming, and the somatic memory of stress exposures.

Plants are highly sensitive to various environmental stresses, which can hinder their growth and reduce yields. In this study, we investigated the potential of seed priming with salicylic acid (SA), gibberellic acid (GA3), and sodium chloride (NaCl) to mitigate the adverse effects of salinity stress in Hordeum vulgare at the germination and early seedling stages. Exposing H. vulgare seeds to salt stress reduced the final germination percentage and seedling shoot and root growth. Interestingly, all seed treatments significantly improved salt-induced responses, with GA3 being more effective in terms of germination performance, plant growth, and photosynthesis. SA priming exhibited promising effects on antioxidant defense mechanisms, proline, sugar, and ascorbic acid production. Notably, SA priming also suppressed reactive oxygen species accumulation and prevented lipid peroxidation. These findings highlight the ability of SA to manage crosstalk within the seed, coordinating many regulatory processes to support plant adaptation to salinity stress.