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

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Science Advances  19 Feb 2016:
Vol. 2, no. 2, e1501340
DOI: 10.1126/sciadv.1501340

Figures

  • 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.

Tables

  • Table 1 Examples of stress priming in plants.
    SpeciesTreatmentOutcomeReference
    Nicotiana sylvestrisMethyl jasmonateRapid nicotine accumulation(5)
    Arabidopsis thalianaABASensitize light-triggered stomatal opening(11)
    DehydrationImproved water retention(9, 10)
    Excess lightIncreased oxidative stress/excess light tolerance(12, 18)
    Osmotic/oxidative stressAltered Ca2+ signals under osmotic stress(17, 19)
    BABAIncreased systemic acquired resistance; abiotic stress resistance(15, 28)
    SAImproved heat tolerance(7)
    ColdVernalization response(21)
    Zea maysDehydrationImproved water retention(24, 25)
    SA/BABAImproved cold tolerance(16)
    Triticum aestivumDroughtIncreased grain fill under drought(26)
    SaltImproved resistance to salt stress(13)
    SAIncreased salinity tolerance(20)
    Conyza bonariensisParaquatIncreased oxidative stress recovery(27)
    Solanum lycopersicumSaltImproved resistance to salt stress(6)
    Cucumis sativusSA/BABAImproved cold tolerance(16)
    Oryza sativaSA/BABAImproved cold tolerance(16)
    Sinapis albaSAImproved heat tolerance(8)
  • Table 2 Examples of transgenerational stress priming in plants.
    SpeciesPriming treatmentPhysiological responseReference
    Polygonum
    persicaria
    DroughtIncreased root growth and biomass, and improved
    drought tolerance (cumulative effect) in progeny
    (110)
    Low lightOffspring produced more shoot tissue relative to root tissue(37)
    Arabidopsis
    thaliana
    BABADescendants exhibit biotic stress resistance(36)
    Mild heat (30.8°C)Progeny (F3) displayed improved heat tolerance(38)
    Herbivory damage
    (Pieris rapae); methyl
    jasmonate
    Progeny of treated parents displayed improved resistance
    to herbivory (reduced growth of P. rapae). This was
    shown to persist after a generation without herbivory
    (33)
    Short-wavelength radiation
    (ultraviolet C); flagellin
    Increased genomic flexibility in the form of
    increased homologous recombination
    (32)
    Mimulus
    guttatus
    Herbivory damage
    (simulated)
    Increased trichome density in progeny(34)
    Picea abiesDay length and temperature during
    seed production
    Determines progeny developmental program(30, 31, 35)
    Raphanus
    raphanistrum
    Herbivory damage
    (P. rapae); jasmonic acid
    Enhanced herbivory resistance in
    progeny of treated parents
    (29)
    Solanum
    lycopersicum
    Herbivory damage
    (Helicoverpa zea);
    methyl jasmonate
    Progeny of treated plants demonstrated
    improved resistance to herbivory
    (33)

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