Stress Memory Research Articles

Drought stress induces early flowering and the stress tolerance of offspring in Petunia hybrida.

Petunia hybrida (Solanaceae) exhibits high sensitivity to water scarcity, especially during flowering. This study investigated changes in the flowering time of P. hybrida in response to water deficit over a 7-week period. Various levels of water stress-i.e., light, moderate, and severe-were imposed on plants grown in a greenhouse, and these were compared to a control group grown alongside. Remarkably, early flowering was observed under severe stress in P. hybrida for the first time, occurring 5.3 days earlier than in the control group. Furthermore, seeds collected from control and treatment plants were then used to assess drought stress memory in offspring. Seedlings were cultivated in a dehydration medium containing either PEG 8000 or a control MS medium. In the PEG 8000 medium, seedlings from parents exposed to moderate and severe drought stresses exhibited higher drought tolerance than those from well-watered conditions. Moreover, they also displayed significantly longer roots, more leaves, and a lower ion leakage rate. Taken together, these findings demonstrated the presence of positive transgenerational effects on progeny. Thus, while parental drought stress during reproduction stage may affect seed quality, it can enhance drought tolerance in the next generation via induction of stress memory.

Epigenetic Modifications in Genome Help Remembering the Stress Tolerance Strategy Adopted by the Plant.

Genetic information in eukaryotic organisms is stored, replicated, transcribed, and inherited through the nucleus of a cell. Epigenetic modifications in the genetic material, including DNA methylation, histone modification, changes in non-coding RNA (ncRNA) biogenesis, and chromatin architecture play important roles in determining the genomic landscape and regulating gene expression. Genome architecture (structural features of chromatin, affected by epigenetic modifications) is a major driver of genomic functions/activities. Segregation of euchromatin (transcriptionally active) from heterochromatin (transcriptionally repressed chromosome) and positioning of genes in specific nuclear space in eukaryotic cells emphasise non-randomness in the organization of the genetic information. Not only does the base sequence of a gene carry the genetic information but the covalent modifications of bases, three-dimensional positioning of the genome, and chromatin loops are vital for switching on/off the gene and regulating its expression during growth/environmental stress. The epigenetic dynamics depend on the activities of writers and erasers under changing environmental conditions. The discovery of non-coding RNAs (one of the players in de novo methylation of DNA), increased DNA methylation protein (guide for the DNA demethylase), and methylation monitoring sequence (that helps keep a balance between DNA demethylation and methylation) have been some of the new developments in the era of epigenomics. To respond to environmental stimuli, plants depend on modulating gene expression through different mechanisms including biochemical, molecular, genetic, and epigenetic alterations. Studies on plants might provide better insights into epigenetic stress memory and molecular bases of adaptability to enable (epi)genome editing of crops for climate resilience and sustainable agriculture in the present era of multifaceted climate change.

Drought priming-induced stress memory improves subsequent drought or heat tolerance via activation of γ-aminobutyric acid-regulated pathways in creeping bentgrass.

Recurrent drought can induce stress memory in plants to induce tolerance to subsequent stress, such as high temperature or drought. Drought priming (DP) is an effective approach to improve tolerance to various stresses; however, the potential mechanism of DP-induced stress memory has not been fully resoved. We examined DP-regulated subsequent drought tolerance or thermotolerance associated with changes in physiological responses, GABA and NO metabolism, heat shock factor(HSF) and dehydrin (DHN) pathways in perennial creeping bentgrass. Plants can recover after two cycle of DP, and DP-treated plants had significantly higher tolerance to subsequent drought or heat stress, with higher leaf RWC, Chl content, photochemical efficiency, and cell membrane stability. DP significantly alleviated oxidative damage through enhancing total antioxidant capacity in response to subsequent drought or heat stress. Endogenous GABA was significantly increased by DP through activating glutamic acid decarboxylase activity and inhibiting GABA transaminase activity. DP also enhanced accumulation of NO, depending on NOS activity, under subsequent drought or heat stress. Transcript levels of multiple transcription factors, heat shock proteins, and DHNs in the HSF and DHN pathways were up-regulated by DP under drought or heat stress, but there were differences between DP-regulated heat tolerance and drought tolerance in these pathways. The findings indicate that under recurrent moderate drought, DP improves subsequent tolerance to drought or heat stress in relation to GABA-regulated pathways, providing new insight into understanding of the role of stress memory in plant adaptation to complex environmental stresses.

Geraniol attenuates oxidative stress and neuroinflammation-mediated cognitive impairment in D galactose-induced mouse aging model.

D-galactose (D-gal) administration was proven to induce cognitive impairment and aging in rodents' models. Geraniol (GNL) belongs to the acyclic isoprenoid monoterpenes. GNL reduces inflammation by changing important signaling pathways and cytokines, and thus it is plausible to be used as a medicine for treating disorders linked to inflammation. Herein, we examined the therapeutic effects of GNL on D-gal-induced oxidative stress and neuroinflammation-mediated memory loss in mice. The study was conducted using six groups of mice (6 mice per group). The first group received normal saline, then D-gal (150 mg/wt) dissolved in normal saline solution (0.9%, w/v) was given orally for 9 weeks to the second group. In the III group, from the second week until the 10th week, mice were treated orally (without anesthesia) with D-gal (150 mg/kg body wt) and GNL weekly twice (40 mg/kg body wt) four hours later. Mice in Group IV were treated with GNL from the second week up until the end of the experiment. For comparison of young versus elderly mice, 4 month old (Group V) and 16-month-old (Group VI) control mice were used. We evaluated the changes in antioxidant levels, PI3K/Akt levels, and Nrf2 levels. We also examined how D-gal and GNL treated pathological aging changes. Administration of GNL induced a significant increase in spatial learning and memory with spontaneously altered behavior. Enhancing anti-oxidant and anti-inflammatory effects and activating PI3K/Akt were the mechanisms that mediated this effect. Further, GNL treatment upregulated Nrf2 and HO-1 to reduce oxidative stress and apoptosis. This was confirmed using 99mTc-HMPAO brain flow gamma bioassays. Thus, our data suggested GNL as a promising agent for treating neuroinflammation-induced cognitive impairment.

Stress memory in crops: what we have learned so far

Stress memory in crops: what we have learned so far

Application of Thermal Imaging for Assessing Desiccation Stress Memory in Sugarcane and Sorghum Cultivars

Application of Thermal Imaging for Assessing Desiccation Stress Memory in Sugarcane and Sorghum Cultivars

Characteristics of Stress Memory and Acoustic Emission for Siltstone under Different Previous Stresses

Characteristics of Stress Memory and Acoustic Emission for Siltstone under Different Previous Stresses

High-resolution kinetics of herbivore-induced plant volatile transfer reveal clocked response patterns in neighboring plants.

Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.

High-resolution kinetics of herbivore-induced plant volatile transfer reveal clocked response patterns in neighboring plants

Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.

DNA methylation: an emerging paradigm of gene regulation under drought stress in plants.

Drought is an enormous threat to global crop production. In order to ensure food security for the burgeoning population, we must develop drought tolerant crop varieties. This necessitates the identification of drought-responsive genes and understanding the mechanisms involved in their regulation. DNA methylation is a widely studied mechanism of epigenetic regulation of gene expression, which is known to play vital role in conferring tolerance to various biotic and abiotic stress factors. The recent advances in next-generation sequencing (NGS) technologies, has allowed unprecedented access to genome-wide methylation marks, with single base resolution. The most important roles of DNA methylation have been studied in terms of gene body methylation (gbM), which is associated with regulation of both transcript abundance and its stability. The availability of mutants for the various genes encoding enzymes involved in methylation of DNA has allowed ascertainment of the biological significance of methylation. Even though a vast number of reports have emerged in the recent past, where both genome-wide methylation landscape and locus specific changes in DNA methylation have been studied, a conclusive picture with regards to the biological role of DNA methylation is still lacking. Compounding this, is the lack of sufficient evidence supporting the heritability of these epigenetic changes. Amongst the various epigenetic variations, the DNA methylation changes are observed to be the most stable. This review describes the drought-induced changes in DNA methylation identified across different plant species. We also briefly describe the stress memory contributed by these changes. The identification of heritable, drought-induced methylation marks would broaden the scope of crop improvement in the future.

The role of priming and memory in rice environmental stress adaptation: Current knowledge and perspectives.

Plant responses to abiotic stresses are dynamic, following the unpredictable changes of physical environmental parameters such as temperature, water and nutrients. Physiological and phenotypical responses to stress are intercalated by periods of recovery. An earlier stress can be remembered as 'stress memory' to mount a response within a generation or transgenerationally. The 'stress priming' phenomenon allows plants to respond quickly and more robustly to stressors to increase survival, and therefore has significant implications for agriculture. Although evidence for stress memory in various plant species is accumulating, understanding of the mechanisms implicated, especially for crops of agricultural interest, is in its infancy. Rice is a major food crop which is susceptible to abiotic stresses causing constraints on its cultivation and yield globally. Advancing the understanding of the stress response network will thus have a significant impact on rice sustainable production and global food security in the face of climate change. Therefore, this review highlights the effects of priming on rice abiotic stress tolerance and focuses on specific aspects of stress memory, its perpetuation and its regulation at epigenetic, transcriptional, metabolic as well as physiological levels. The open questions and future directions in this exciting research field are also laid out.

Possible role of plant nucleoredoxins in context of ‘stress memory adaptation’ for oxidative stress as revealed by in-silico and citation network analysis

Plants being sessile constantly phase encountered stresses throughout their life both abiotic and biotic stresses. Due to these stresses, plants need to possess some memory and currently there is need to correlate ecological constraints and importance of stress memory. Stress priming deals with the plant's capacity to memorize stress onslaught and adapt to recurring stress. Oxidative stress is one such abiotic stress which disturbs the cell homeostasis and redox balance inside the cell which is thereby countered by plant's antioxidant machinery. Thus, plants need to have some kind of memory to encounter future oxidative stress. Redoxins such as glutaredoxin (GRX), thioredoxin (TRX), peroxiredoxin (PRX), nucleoredoxin (NRX) etc. are enzymatic antioxidants which plays vital role in the plant growth and development. NRXs have been lesser characterized in plants as per existing literature and scientometric analysis in present work sheds light on the importance of plant NRXs. Nucleoredoxin, possessing antioxidant properties and the ability to scavenge ROS, may play a crucial role in molecular priming mechanisms. The citation network analysis using VOSviewer server also showed the importance of current research and relation of NRXs with terms like ROS, gene expression regulation, plant gene, phytohormones and plant immunity. Later the Cicer arietinum NRX sequence was bioinformatically characterized using several tools for better understanding. Currently, there is growing evidence and research on this ‘stress memory concept’ and how different molecular players are related to it.

Drought priming reduces Calligonum mongolicum sensitivity to recurrent droughts via coordinated regulation of osmolytes, antioxidants, and hormones.

Pre-exposure of plants to abiotic stressors may induce stress memory and improve tolerance to subsequent stresses. Here, 3-month-old Calligonum mongolicum seedlings were exposed to drought (60 days) with (primed) or without (unprimed) early drought exposure of 50 days, to determine whether this enhances seedling resistance and investigate possible underlying mechanisms. Compared to unprimed, primed seedlings had higher biomass, shoot relative water content (15% and 22%), chlorophyll a, chlorophyll b, and carotenoids. They also had more superoxide anions (O2 -• ) and H2 O2 scavenging mechanisms through higher activity of SOD, CAT, APX, and dehydroascorbate reductase in assimilating shoots and roots, resulting in less ROS and oxidative stress damage. Plants also had higher ABA and JA but lower SA, likely reflecting an adaptive response to subsequent stress. Primed seedlings accumulated more IAA and brassinosteroids, which may account for their better growth. Accumulation of glycine betaine, pro, and total amino acids in assimilating shoots and roots of primed seedlings led to reduced osmotic stress. Drivers of responses of non-primed and primed seedlings to drought varied. Responses of primed seedlings were primarily characterized by more photosynthetic pigments, increased oxidative scavenging of O2 -• and H2 O2 , more phytohormones and osmolytes. Early drought priming of drought stress memory in C. mongolicum seedlings may provide a useful management approach to improve seedling establishment in vegetation restoration programs.

Heat stress memory differentially regulates the expression of nitrogen transporter genes in the filamentous red alga 'Bangia' sp. ESS1.

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. 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. 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. 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.

Revisiting plant stress memory: mechanisms and contribution to stress adaptation.

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.

A cell-wall-modifying gene-dependent CLE26 peptide signaling confers drought resistance in Arabidopsis.

Plants respond to various environmental stimuli in sophisticated ways. Takahashi et al. (2018) revealed that CLAVATA3/EMBRYO SURROUNDING REIGON-related 25 (CLE25) peptide is produced in roots under drought stress and transported to shoots, where it induces abscisic acid biosynthesis, resulting in drought resistance in Arabidopsis. However, the drought-related function of the CLE26 peptide, which has the same amino acid sequence as CLE25 (except for one amino acid substitution), is still unknown. In this study, a phenotypic analysis of Arabidopsis plants under repetitive drought stress treatment indicates that CLE26 is associated with drought stress memory and promotes survival rate at the second dehydration event. Additionally, we find that a loss-of-function mutant of a cell-wall-modifying gene, XYLANASE1 (XYN1), exhibits improved resistance to drought, which is suppressed by the mutation of CLE26. XYN1 is down-regulated in response to drought in wild-type plants. A further analysis shows that the synthetic CLE26 peptide is well transported in both xyn1 and drought-pretreated wild-type plants but not in untreated wild-type plants. These results suggest a novel cell wall function in drought stress memory; short-term dehydration down-regulates XYN1 in xylem cells, leading to probable cell wall modification, which alters CLE26 peptide transport, resulting in drought resistance under subsequent long-term dehydration.

Epigenetic stress memory in gymnosperms.

Gymnosperms are long-lived, cone-bearing seed plants that include some of the most ancient extant plant species. These relict land plants have evolved to survive in habitats marked by chronic or episodic stress. Their ability to thrive in these environments is partly due to their phenotypic flexibility, and epigenetic regulation likely plays a crucial part in this plasticity. We review the current knowledge on abiotic and biotic stress memory in gymnosperms and the possible epigenetic mechanisms underlying long-term phenotypic adaptations. We also discuss recent technological improvements and new experimental possibilities that likely will advance our understanding of epigenetic regulation in these ancient and hard-to-study plants.

From environmental responses to adaptation: the roles of plant lncRNAs.

As sessile organisms, plants are continuously exposed to heterogeneous and changing environments and constantly need to adapt their growth strategies. They have evolved complex mechanisms to recognize various stress factors, activate appropriate signaling pathways, and respond accordingly by reprogramming the expression of multiple genes at the transcriptional, post-transcriptional, and even epigenome levels to tolerate stressful conditions such as drought, high temperature, nutrient deficiency, and pathogenic interactions. Apart from protein-coding genes, long non-coding RNAs (lncRNAs) have emerged as key players in plant adaptation to environmental stresses. They are transcripts larger than 200 nucleotides without protein-coding potential. Still, they appear to regulate a wide range of processes, including epigenetic modifications and chromatin reorganization, as well as transcriptional and post-transcriptional modulation of gene expression, allowing plant adaptation to various environmental stresses. LncRNAs can positively or negatively modulate stress responses, affecting processes such as hormone signaling, temperature tolerance, and nutrient deficiency adaptation. Moreover, they also seem to play a role in stress memory, wherein prior exposure to mild stress enhances plant ability to adapt to subsequent stressful conditions. In this review, we summarize the contribution of lncRNAs in plant adaptation to biotic and abiotic stresses, as well as stress memory. The complex evolutionary conservation of lncRNAs is also discussed and provides insights into future research directions in this field.

Transcriptional patterns and histone modification signatures reveal dehydration memory behaviour in seedlings of Gossypium hirsutum

In nature, plants often experience recurring stress conditions. Some plants have evolved a memory response, which shows an enhanced reaction upon subsequent stress. However, whether cotton (Gossypium hirsutum L.) exhibits dehydration stress memory and the underlying mechanisms have remained unclear. Here, we characterized the responses to recurring dehydration stress in cotton seedlings from physiological changes, gene expression patterns and histone modification levels. Our results showed that short-term dehydration stress memory could develop in cotton seedlings. Transcriptome analysis identified 602 transcriptional dehydration memory genes (DMGs), and these genes could be divided into four distinct response patterns. A homology analysis indicated that conservation and species-specific memory responses existed between cotton and other plants. Chromatin immunoprecipitation - qPCR results revealed that the transcriptional behaviour of [+ /+ ] memory genes was related to the retention of increased H3K4me3 levels during the recovery stage and that H3K4me3 could act as a memory mark at the [+ /+ ] dehydration memory genes in cotton. A virus-induced gene silencing assay indicated that the histone demethylase gene GhJMJ17-A/D may participate in the transcriptional behaviour of [+ /+ ] memory genes in cotton. These results will improve the understanding of the mechanisms of formation and maintenance of dehydration stress memory in plants and will be useful for the improvement of cotton and other crops.

The Mediator kinase module enhances polymerase activity to regulate transcriptional memory after heat stress in Arabidopsis

Plants are often exposed to recurring adverse environmental conditions in the wild. Acclimation to high temperatures entails transcriptional responses, which prime plants to better withstand subsequent stress events. Heat stress (HS)-induced transcriptional memory results in more efficient re-induction of transcription upon recurrence of heat stress. Here, we identified CDK8 and MED12, two subunits of the kinase module of the transcription co-regulator complex, Mediator, as promoters of heat stress memory and associated histone modifications in Arabidopsis. CDK8 is recruited to heat-stress memory genes by HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2). Like HSFA2, CDK8 is largely dispensable for the initial gene induction upon HS, and its function in transcriptional memory is thus independent of primary gene activation. In addition to the promoter and transcriptional start region of target genes, CDK8 also binds their 3ʹ-region, where it may promote elongation, termination, or rapid re-initiation of RNA polymerase II (Pol II) complexes during transcriptional memory bursts. Our work presents a complex role for the Mediator kinase module during transcriptional memory in multicellular eukaryotes, through interactions with transcription factors, chromatin modifications, and promotion of Pol II efficiency.