Drought Stress Memory At The Plant Cycle Level: A Review Part 3

2.4. Epigenetic and Molecular Mechanisms Involved in Transcriptional Memory Establishment

Epigenetic modifications related to a given stress modulate gene expression during a subsequent stress. They can contribute to transcriptional memory through memory genes, non-memory genes, and transcription factors. 

Memory genes refer to genes that control the formation and preservation of memories and play an important role in our lives. Research shows that genetic factors have a significant impact on memory, but it also shows that environment and personal behavior can also significantly affect memory.

Human memory is divided into short-term memory and long-term memory. Short-term memory is our short-term storage ability for things, while long-term memory is our long-term storage ability for things. Our memory can be improved through continuous exercise, which in turn changes our memory genes.

Many studies have shown that through regular exercise, memorizing things, and learning new skills or languages, people's memory and brain function will be enhanced. Adequate exercise and good eating habits will also help you maintain good health and strong brain function.

Positive behavior and a positive attitude also have a positive impact on people's memory. In life, optimistic people are better at handling stress and emotions, making it easier to form and preserve memories.

Therefore, we should pay attention to our behaviors and habits, take appropriate methods to promote brain health, and continue to exercise and learn to enhance our memory. Trying new things and developing healthy habits can help make your brain healthier, improve your memory, and lead to a more positive way of thinking. It can be seen that we need to improve memory, and Cistanche deserticola can significantly improve memory, because Cistanche deserticola can also regulate the balance of neurotransmitters, such as increasing the levels of acetylcholine and growth factors. These substances are very important for memory and learning. In addition, Cistanche deserticola can also improve blood flow and promote oxygen delivery, which can ensure that the brain receives sufficient nutrients and energy, thereby improving brain vitality and endurance.

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Two distinct marks have been characterized on memory genes during recovery periods that followed dehydration stress periods in Arabidopsis thaliana [25]. These memory marks include histone modifications, such as the maintenance of a high level of trimethylated histone H3Lys4 nucleosomes (H3K4me3) and stalled Ser5P RNA Polymerase II (Ser5P pol II) at stress memory genes during recovery, even though their transcription level was low during recovery. 

These epigenetic marks play a role in transcriptional memory since they are enriched during stress periods and maintained at a certain level during recovery periods [5]. The accumulation of H3K4me3 is not specific to drought memory, as it has also been observed in heat stress memory [49] and salinity [11]. 

In contrast, elevated levels of Ser5P pol II have been poorly described in plants but were shown to be prevalent in genes involved in development and response to stimuli in animals [50]. 

The factors or genes that cause ser5P pol II and H3K4me3 association with memory genes and transcriptional stress memory are still unknown. The histone H3K4 methyltransferase ATX1 (TRITHORAX-LIKE 1) is necessary but not sufficient, as the transcriptional memory response in the atx1 mutant is attenuated but not eliminated. Similarly, the involvement of ABA and ABA-regulated transcription factors such as AREB1, AREB2 (ABSCISIC ACID– RESPONSIVE ELEMENT BINDING PROTEIN 1 and 2, respectively), and ABF3 (ABSCISIC ACID RESPONSIVE ELEMENTS-BINDING FACTOR 3) is important for the magnitude of induction of some memory genes, but not essential for the memory response to occur [25]. 

More recently, the potential implication of DNA methylation in drought stress memory was demonstrated in the resurrection plant Boea hygrometrica [51]. Up-regulation of memory genes including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, was associated with promoter methylation variations in the CG and CHG contexts. 

Although these epigenetic modifications are generally not meiotically inherited, they can, in some cases, be passed on to the next generation and form a transgenerational memory. This mechanism could be of great interest for breeding purposes, especially towards the improvement of long-term plant adaptation to fluctuating environments [10,52]. Non-memory genes are involved in transcriptional memory by playing a role in the implementation of epigenetic marks on memory genes. 

Non-memory genes have been identified, such as a [−/=] putative methyltransferase with a DNA-binding domain and a [+/=] gene annotated "nucleosome remodeling factor" [34]. The activity of transcription factors (TF) is involved in stress memory, although the transcriptional memory pattern of a TF does not necessarily determine the memory pattern of its targets (even if direct). 

For example, the memory expression pattern of the bHLH MYC2 transcription factor under repeated dehydration stresses did not correlate with the non-memory expression pattern of its target gene RD22 [27]. Both in Zea mays and Arabidopsis thaliana, about 10% of the drought stress memory genes encoded TFs, but some families were identified as species-specific. 

For instance, the NAC (NAM, ATAF and CUC) family TFs with a [+/+] signature and the integrase-type AP2/ERF (APETALA 2/ERE binding factor) family members with a [+/−] signature were highly represented in maize, while TFs from the AP2/ERF, bHLH (basic helix-loop-helix) and ZF (Zinc finger) families were more specific to Arabidopsis thaliana [26]. One additional level in memory gene regulation could involve small RNAs, in particular microRNA (miRNA), as shown for heat stress (HS) memory. 

In Arabidopsis thaliana, thermotolerance is compromised in miRNA pathway mutants such as ago1 (argonaute1) and dcl1 (dicer-like1) [53]. Functional analysis demonstrated that mir156 is specifically required for HS memory through the repression of its targets SPL2 (SQUAMOSA promoter binding protein-like 2) and SPL11. 

In addition, mir156 over-expression enhanced and prolonged the HS memory effect [53]. In Medicago sativa (alfalfa) mir156 over-expressor lines showed improved drought stress tolerance [54], and drought-responsive miRNAs have been identified in numerous crop species including legumes [55], cereals ([56] for a review) and Solanum lycopersicum [57]. To what extent miRNA could mediate drought stress memory remains to be elucidated.

2.5. Plant Biomass and Productivity

Plant biomass production and yield are the main macroscopic indicators of drought stress memory, as they integrate the different molecular mechanisms and physiological processes involved in plant response to repeated stresses. 

For instance, primed Triticum aestivum plants at the tillering stage produced higher yields than non-primed plants after subsequent stresses, likely through modulations of growth hormone levels (i.e., higher cytokinin, indole-3-acetic acid, gibberellin contents, and lower ABA content in the primed plants) [29]. 

Priming at the seed stage can have long-lasting effects. Osmopriming Triticum aestivum seeds with polyethylene glycol (PEG) before the occurrence of drought at tillering and jointing stages led to sustained relative growth rate during stress and higher final grain yield production [30]. However, drought stress memory cannot be generalized, since its establishment is species and genotype-dependent. 

The transcriptional memory differences that exist between Arabidopsis thaliana and Zea mays subjected to repeated dehydration stresses (described above) may reflect differences in photosynthetic and related metabolism functions between C3 and C4 plants [26], while we hypothesize that differences in physiological memory between crops allocating more of their resources to non-reproductive organs (e.g., tuber) versus those remobilizing resources towards seeds could be explained by contrasted source-sink relationships. 

Differences in drought stress memory abilities between genotypes have been highlighted in several species. In Solanum tuberosum, although priming induced an increase of tuber amino acid content in the two varieties Sarnav and Unica, priming only resulted in a higher tuber yield for the Sarnav variety [42]. 

In Triticum aestivum, the higher tolerance of the Luhan cultivar than the Yuangmai cultivar has been related to a higher stress memory ability in response to recurrent droughts [28].

2.6. Trade-off between Stress Memory and Stress Forgetfulness (Memory Resetting)

Plant priming induced by a preexposure to first stress can allow a faster or more intense response to subsequent stress [24], and its cost is estimated to be relatively low compared to naïve plants which constitutively express stress-related genes [6,9,58,59]. 

Yet, sustaining a primed state via short-term (morphological acclimation, physiological changes, molecular and metabolic alterations) and long-term mechanisms (epigenetic processes) is energy-consuming and can negatively impact other biological processes such as plant growth (including photosynthesis and resource allocation) or development [22]. 

As such, it can be advantageous to learn to forget. Resetting (aka stress forgetfulness) has been proposed as the main plant strategy to fine-tune growth in fluctuating and unpredictable environmental conditions [22]. Throughout the plant cycle, alternating periods of establishing memory and resetting it could be driven by RNA metabolism, post-transcriptional gene silencing, or RNA-directed DNA methylation [22]. 

To our knowledge, the resetting of a plant-primed state after a drought event has not been studied yet. However, in the case of heat stress memory, resetting involves autophagy-mediated degradation of HSP proteins during recovery to reset the cell proteome [60]. Thus, stress memory establishment and its resetting appear to be coordinated by fine-tuned mechanisms that modulate memory duration (e.g., four days in a study of heat stress memory) [60]. As a result, this process contributes to alleviating the negative impact of recurrent stresses on plant biomass production [9]. 

Too little tangible evidence is currently available to understand the dynamics and the regulation of the trade-off between stress memory and stress resetting, thus opening a huge science front for the coming years. To that end, we propose a conceptual analysis framework (Figure 3) including stress memory, stress forgetfulness, and recovery memory that could help in understanding the dynamics of these processes. 

This conceptual framework follows the general concept initially developed by Couchoud et al. [61], which involves the characterization of different parameters during both water stress and recovery periods: impact of the first stress, dynamics of the recovery after each stress, and duration of stress memory. 

Finally, a better characterization of the regulatory dynamics underlying stress memory would make it possible to predict plant responses to multiple stresses based on process-based modeling. Moreover, thanks to technical advances and the increased availability of more powerful tools and methods, a deeper understanding of the dynamics of stress memory/forgetfulness will be possible.

These tools include high-throughput phenotyping of shoots and roots that allow screening of a large number of genotypes under controlled conditions (major plant phenotyping centers are part of the International Plant Phenotyping Network; www.plant-phenotyping.org, accessed on 7 September 2021). 

Molecular tools and methods based on multiomics and systems biology approaches can help in identifying the main regulators that are necessary for genetic improvement [62]. 

Recent advances in epigenetics allowed the construction of "epi-populations" that can reveal "epi-alleles" whose variants can also be considered as breeding targets [10]. Then, once the candidate genes have been identified, genome editing tools such as CRISPR-Cas9 [63] will be useful for gene functional validation. Finally, speed-breeding techniques, by shortening the growth cycle of plants, would greatly accelerate the genetic improvement of crops [64].

3. Water Stress Memory and the Plant x Microbiome Interplay

Soil microorganisms establish strong interactions with plants about nutrient acquisition, protection against pathogens, and beneficial physico-chemical changes in the soil. Soil moisture is a key driver of microbial community composition and activity. Due to the much more rapid turnover of soil microorganisms compared to plants, individual-level memory is less relevant for soil microbes at the community scale. Instead, the term "legacy" is typically used for describing the effects of changes in environmental conditions on soil microbial community over time [65].

Microbial adaptation to drought periods followed by rewetting involves different coping mechanisms, such as sporulation or the production of osmolytes to resist osmotic stress, which is related to life strategies along a drought-resistant to opportunistic gradient [66]. 

In addition to the inherent large and rapid change in soil water potential, rewetting triggers C and N mineralization bursts that constitute an additional modification in soil environmental conditions [67,68]. Advances in molecular microbiology over the last decades, based on next-generation sequencing and including metagenomics and metatranscriptomics, have shed light on the dynamic responses of soil microorganisms and their activity to dry-wet cycles. 

Exposing a microbial community to drought can improve its resistance to subsequent drought and rewetting events [69,70]. More generally, the legacy effects of past drought conditions can shape the response of soil microbial communities to future droughts [65,70,71]. 

As a consequence, microbial legacy can affect major soil functions such as decomposition [72] or decomposition-related mechanisms [73,74], which will directly influence the plant's nutritional status and likely affect ecosystem properties. For example, the effects of an anomalously warm year can contribute to changes in ecosystem functioning which are related to plant-microbial interactions and can persist several years after a drought event [75].

Do stress legacy effects of drought on microorganisms modify the response of plants to subsequent stress? Microbial communities that are adapted to water stress can improve plant fitness and resistance to drought [76–78]. Similarly, microbial communities subjected to previous drought conditions can alter the direction of plant-soil feedback [79]. Conversely, do plant memory effects shape the response of soil microorganisms to a subsequent drought? 

Increased rhizodeposition under moderate drought stress is a generally observed trend, despite species-specific variability, which is expected to directly stimulate microbial community functioning [80]. Under suboptimal conditions, plants can select beneficial microorganisms in their rhizosphere through the exudation of different compounds that are available for soil microorganisms [81]. 

For instance, root secretions of hormones involved in plant immune responses, such as salicylic acid and jasmonic acid, can shape the rhizosphere and root microbiome assembly and functionality [77]. The enrichment of soil with plant-protective microorganisms can be beneficial for the plant during its cycle, but also for further plant generations growing in the same soil [82]. 

The soil legacy effect could thus be a key driver of terrestrial plant community composition and productivity, with effects that persist over time [76]. We suggest they should explicitly be taken into account when addressing an extended framework of plant stress memory. The challenge, however, is that microbial legacy takes place over longer periods than plant memory effects since time is required for changes in composition and activity to become established in a fundamentally dynamic community.

4. Conclusions

Plant water stress memory involves processes associated with photosynthesis, energy mechanisms, osmotic adjustment, cellular protective functions, and water status maintenance. 

Memory mechanisms are best known at the shoot level, yet it is essential to characterize those at the root level. Indeed, the role of the root system in water and nutrient uptake is crucial for plant growth, development, and yield. From a wider point of view, the close interaction between root system memory and the microbiome legacy in the soil represents the next challenge to tackle. 

Most studies on plant memory have been conducted on cereal or vegetative storage crops, while legume stress memory has scarcely been addressed. However, legumes are a model of choice for understanding the memory of plants in interaction with soil microorganisms, due to their ability to establish symbiotic relationships with rhizobium and mycorrhizal fungi. 

A more holistic and dynamic approach to plant resilience would i) bring plant-microbial interactions into the picture and ii) improve the understanding of recovery memory after a stress period and the fine trade-off between plant memory and forgetfulness. Increased knowledge of plant resilience, which includes stress memory, thus appears to open up new perspectives in the general context of food security under a changing climate.
Author Contributions: Writing-original draft preparation, C.J.; writing-review and editing, C.J., C.S., R.L.B., V.V., and M.P.; supervision, M.P. All authors have read and agreed to the published version of the manuscript.

Funding: This work was conducted through the ARECOVER project of the Plant2Pro Carnot Institute and the EAUPTIC project supported by the "Fond Unique Interministériel" (3870401/1), BPI France (0097244/00), the Regional Council of Burgundy (0133465/00), Dijon Metropole (2018-118-20180820), and the "Fonds Européen de Développement Régional" (2018-6200FEO003S01889). CJ was supported by a Ph.D. grant from Université de Bourgogne.

Conflicts of Interest: The authors declare no conflict of interest.

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