Higher plants are sedentary organisms which inevitably endure a variety of environmental stresses throughout the life cycle. Abiotic stresses can be atmospheric like cold, heat and UV irradiation; or can also be edaphic like salinity, drought, and heavy metal toxicity (Wani and Gosal, 2011; Surekha et al., 2015). Of all these, cold stress is regarded as a major environmental factor which limits agricultural expansion and crop productivity in hilly terrains (Sanghera et al., 2011). Non-freezing low temperatures deteriorate plant growth physiology by inducing chilling injuries like photosynthesis-associated damages, chlorosis, unregulated apoptosis, loss of membrane fluidity and ultimately wilting (Wani et al., 2016). Depending on the extent of sensitivity among plants, cold stress has been sub-divided into two types. Chilling stress is characterized by 0–15°C, whereas temperatures below 0°C cause freezing stress (Wani et al., 2013). By virtue of cold acclimation and associated alterations at the molecular and biochemical levels, temperate climatic plants exhibit greater ranges of cold tolerance compared to their tropical and sub-tropical counterparts (Yamaguchi-Shinozaki and Shinozaki, 2006). Deciphering the epigenomic landscape in plants exposed to cold conditions is a rapidly developing field (Hu et al., 2011). Intricate research focussing on epigenetic processes during cold stress has led to the identification of molecular targets which can be genetically manipulated to generate cold tolerant lines.

Vernalization is a floral regulatory process preventing precocious flowering during autumn or winter. It gradually promotes flowering competence after prolonged exposures to cold conditions in a species-dependent manner (Kim et al., 2009). Physiologically, vernalization is a “memory response” which is correlated with epigenetic regulation, as observed in the model plant Arabidopsis thaliana (Song et al., 2012).

Vernalization in the Arabidopsis ecotypes is regulated by FLC, Vernalization 1 (VRN1), VRN2 and Vernalization Insensitive 3 (VIN3). Cold stress induces the expression of VIN3, a homeodomain finger containing gene encoding protein. VIN3 associates with an unidentified complex and triggers repressive H3K27me3 and H3K9me in the FLC chromatin (Kim and Sung, 2017; Figure 1). The complex also initiates loss of H3 acetylation and H3K4 methylation, thus suppressing FLC expression and promoting vernalization. It appears that the VIN3 and FLC families actually co-evolved to ensure proper epigenetic regulation of vernalization (Kim and Sung, 2013). In another instance, the H3K27 methyltransferase, SET DOMAIN GROUP 7 (SDG7) negatively regulated the temporal expression of VIN3 in Arabidopsis under control conditions (Figuer 1). Abiding by the FLC-VIN3 regulatory model, sdg7 Arabidopsis mutants exhibited partial vernalization even without cold exposure (Lee et al., 2015). The polycomb group (PcG) proteins along with two homologous trans-acting epigenome readers, VIVIPAROUS 1/ABA-INSENSITIVE 3-LIKE 1 (VAL1) and VAL2 stably repress FLC during prolonged cold treatment (Yuan et al., 2016). The epigenome readers recognized the cis-acting Cold Memory Elements and H3K27me3 to directly associate with LIKE HETEROCHROMATIN PROTEIN 1. This increased H3K27me3 in the FLC nucleation region leading to its repression during vernalization (Yuan et al., 2016; Figure 1).

The scaffold protein, FRIGIDA (FRI) recruits epigenetic factors to regulate vernalization-related floral gene expression in winter annual accessions of Arabidopsis (Hu et al., 2014). It was reported that the TF, WRKY34 promotes the expression of the ubiquitin E3 ligase, CULLIN 3A which proteasomally degrades FRI and triggers the accumulation of lncRNA, Cold Induced Long Antisense Intragenic RNA (ColdAIR) in the late phases of vernalization. High ColdAIR levels reduce H3K4me3 in FLC and facilitates flowering after vernalization (Hu et al., 2014; Figure 1).

Trans-generational repression of FLC during vernalization is maintained as a cellular memory via the mitotic inheritance of the repressive histone marks in the chromatin (Achrem et al., 2012). However, repeated brief cold exposures due to local weather disturbances degrade the central floral regulator, CONSTANS (CO) and delay flowering in Arabidopsis. The E3-ubiquitin ligase HOS1 together with its target, CO serve as the molecular integrator of the photoperiodic and cold stress pathways (Jung et al., 2012). Research in temperate cereal crops (Triticum spp., Hordeum vulgare, Avena sativa, Secale cereale etc.) has verified the increase in gene activating H3K9me3 and decrease in gene suppressing H3K27me3 in VRN1 during vernalization (Oliver et al., 2009). Such variations in H3K methylation status signify vernalization memory in cereals (Banerjee and Roychoudhury, 2017c). However, increased H3K27me3 and decreased H3K4me3 levels in VRN2 and Flowering Locus T1 (FT1) were observed in both the vernalized and non-vernalized seedlings. This depicts that unlike in VRN1, cold treatment does not modify the chromatin of these genes (Achrem et al., 2012). Vernalization in cereal crops is supposedly mediated by DNA demethylation. The PcG proteins recognizing H3K27me3 sites inhibit VRN2 and FT expression in the germinating caryopses but refrain from regulating VRN1 expression in the shoot apices (Li and Liu, 2010). Such spatial regulation of epigenetic factors complicates the systemic overview of cold treatment in plants. Vernalized Arabidopsis seedlings exposed to 30°C, directly after cold treatment exhibited low H3K27me3 at the FLC locus (Bouche et al., 2015). Thus cold shock memory imprinted in the plant epigenome is ushered by the condition-dependent reversible alteration of chromatin architecture.

Epigenetic regulation under cold stress is a manifestation of multiple crosstalks (Figure 1) and plant intelligence. Another crosstalk among the genes involved in flowering, vernalization and generation of cold tolerance can be hypothesized in Triticum monococcum where VRN1 initiates the regulatory cascade to down-regulate cold acclimation genes like CORs and CBFs (Galiba et al., 2009). Thus, it is quintessential to design an epigenomic blueprint acting as a global database of chromatin alterations occurring at low temperatures. Molecular characterization of the epigenetic stress memory is crucially required to integrate plant behavioral responses with intelligence. Stress conditions induce the production of volatile organic carbons which often act as inter-species communicating molecules (Ueda et al., 2012). The epigenetic regulation of such metabolite synthesis during cold stress remains to be elucidated. Genome-wide association studies followed by epiallele mining and subsequent annotations on next generation sequencing platforms should be undertaken to unravel the intricate epigenomic landscape especially in staple crops exposed to cold stress. Understanding the spatio-temporal expression of such epialleles, their interactions with small RNAs during cold stress and stringent mapping of candidate quantitative trait loci can identify potential molecular targets which can be engineered to generate tolerant phenotypes. These can then be recommended for field trials.

AR and SW suggested the title of the opinion article. AB designed the article, drafted the entire manuscript and arranged the references. AR incorporated all the necessary modifications. All the authors checked and confirmed the final version of the manuscript.