Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics

Abstract

Plants grow in dynamic environments where they can be exposed to a multitude of stressful factors, all of which affect their development, yield, and, ultimately, reproductive success. Plants are adept at rapidly acclimating to stressful conditions and are able to further fortify their defenses by retaining memories of stress to enable stronger or more rapid responses should an environmental perturbation recur. Indeed, one mechanism that is often evoked regarding environmental memories is epigenetics. Yet, there are relatively few examples of such memories; neither is there a clear understanding of their duration, considering the plethora of stresses in nature. We propose that this field would benefit from investigations into the processes and mechanisms enabling recovery from stress. An understanding of stress recovery could provide fresh insights into when, how, and why environmental memories are created and regulated. Stress memories may be maladaptive, hindering recovery and affecting development and potential yield. In some circumstances, it may be advantageous for plants to learn to forget. Accordingly, the recovery process entails a balancing act between resetting and memory formation. During recovery, RNA metabolism, posttranscriptional gene silencing, and RNA-directed DNA methylation have the potential to play key roles in resetting the epigenome and transcriptome and in altering memory. Exploration of this emerging area of research is becoming ever more tractable with advances in genomics, phenomics, and high-throughput sequencing methodology that will enable unprecedented profiling of high-resolution stress recovery time series experiments and sampling of large natural populations.

Keywords: DNA methylation; RNA metabolism; RNA turnover; abiotic stress; arabidopsis; epigenetics; gene silencing; plant memory; plants; stress recovery.

Fig. 1. Balancing act during recovery from a stress event.

Abiotic stress, such as dehydration, heat stress, and light stress, imposed by the sun during a hot, dry spell activates plant defenses that are essential for survival. However, stress is transient and is followed by a period of recovery during which the plant must strike a balance between investing resources in continued priming versus resetting. We speculate that the predominant response is resetting (forgetfulness). Most transcripts, proteins, metabolites, and physiological responses return to a prestress state. This recovery is likely to be an important evolutionary strategy. Nevertheless, the degree of memory will likely be critical as well, particularly in dynamic environments characterized by a repetitive stress. Thus, plants must balance the potential protection from future stress by forming stress memories with the potential growth and yield advantages of resetting if favorable conditions persist.

Fig. 2. Stress memory and the molecular pathways to recovery.

(A) A theoretical example of memory formation, where up to thousands of stress-inducible transcripts (blue lines) respond to the initial stress, concurrently with accumulation of signaling molecules and the release of repressive chromatin (red lines). Upon reexposure to a second stress, persistent signaling molecules and a retained accessible conformation of chromatin (solid lines) allow an enhanced stress response. The recovery period is a critical window where plant memory can be consolidated or resetting (dashed lines) can occur. (B) For instance, stress-induced changes in chromatin can be transient (possibly tied to regional accessibility for gene activation) or may persist, acting as a form of stress memory (90). (C) Similarly, signaling molecules may facilitate memory. In addition, signaling molecules can act during the recovery process; for instance, ABA may delay resumption of growth to enable embolism repair (113, 120). (D) KEA3 (potassium antiporter) activity accelerates recovery by relaxing non-photochemical quenching (NPQ) activity after dissipation of excess light stress (121). (E) Epigenetic silencing of FLC relies on the spreading of H3K27me3 specifically during transition to warm (recovery), consolidating repression and memory (66, 123, 124). (F) RNA decay reduces levels of stress-induced transcripts, resulting in resetting; impairment of decay may result in stress memory (161).

Fig. 3. Roles of RNA metabolism during stress recovery leading to memory or resetting.

Stress is characterized by increased expression of many genes. (A to C) During the recovery period following a stress, RNA metabolism can facilitate resetting of the transcriptome by (A) exonuclease decay pathways, (B) miRNA decay pathways, and (we speculate) (C) siRNA pathways as well. (D) Alternatively, transcriptome memory may be created by inhibiting RNA decay or through stabilizing specific transcripts.

Fig. 4. Relationship between mRNA stability and mRNA responsiveness [adapted from Ross (137)].

Following a change in transcription rate, an unstable transcript (TF2) can attain half its new steady state 10 times faster than the stable transcript (HK1). The dashed red line indicates the time point in which transcription increases 10-fold.

Fig. 5. RNA decay antagonizes sRNA production, PTGS, and RdDM.

The RNA decay and gene silencing pathways use the same substrate RNA molecules, creating an antagonism between the RNA decay machinery and the gene silencing machinery. Transcripts are continuously turned over by the RNA decay machinery to achieve steady-state abundance and to ensure quality control; however, perturbations or defects in the RNA turnover or quality control pathway can cause transcripts to enter into the gene silencing pathways, leading to PTGS and potentially stable and heritable TGS via the RdDM pathway. DRM2, DOMAINS REARRANGED METHYLTRANSFERASE 2.

Fig. 6. Summary of the costs and benefits associated with recovery and resetting versus memory.