Cold adaptation strategies in plants-An emerging role of epigenetics and antifreeze proteins to engineer cold resilient plants

Abstract

Cold stress adversely affects plant growth, development, and yield. Also, the spatial and geographical distribution of plant species is influenced by low temperatures. Cold stress includes chilling and/or freezing temperatures, which trigger entirely different plant responses. Freezing tolerance is acquired via the cold acclimation process, which involves prior exposure to non-lethal low temperatures followed by profound alterations in cell membrane rigidity, transcriptome, compatible solutes, pigments and cold-responsive proteins such as antifreeze proteins. Moreover, epigenetic mechanisms such as DNA methylation, histone modifications, chromatin dynamics and small non-coding RNAs play a crucial role in cold stress adaptation. Here, we provide a recent update on cold-induced signaling and regulatory mechanisms. Emphasis is given to the role of epigenetic mechanisms and antifreeze proteins in imparting cold stress tolerance in plants. Lastly, we discuss genetic manipulation strategies to improve cold tolerance and develop cold-resistant plants.

Keywords: DNA methylation; antifreeze proteins; cold acclimation; freezing stress; genetic engineering.

FIGURE 1

Representative diagram of cold responsive signaling pathway in plants. Plants sense cold/freezing signals through membrane receptor (RLK and LRR-RLK) and membrane rigidification. Cold sensing activates calcium channels (CNGC/GRL) that lead to increase Ca²⁺ in cytoplasm, which in turn activates of Ca²⁺ related protein likases (CaM, CML, CDPKs, and CBLs) and downstream signaling including MAPK signaling. These signaling cascades finally interacts with ICE1 and controls expression of CBFs/COR genes. COR genes encode proteins required for the biosynthesis of osmoprotectants, cryoprotectants, protein kinases, lipid, hormone, and stress-responsive proteins that are directly involved in cold tolerance. In addition, COR gene-dependent responses involve expression of diverse cold-induced transcription factors, which regulates CBFs expression in either positive or negative manner. The cold/freezing stress and increased Ca²⁺ activates the NADPH to generate more ROS. ROS and Ca²⁺ regulate each other’s concentration, and this cross talk controls the expression of defense gene in the nucleus. Cold/freezing stress also triggers NO synthesis that is essential for cold acclimation response through CBF dependent manner. In another cold signaling pathway, 14-3-3 protein get phosphorylation by CRPK1 followed by translocation from the cytoplasm to the nucleus where it interacts with CBFs and trigger its degradation through the 26S proteasome pathway. In Arabidopsis, clock related MYB proteins RVE4/RVE8 plays an direct transcriptional activators of DREB1 expression in cold stress. In unstressed condition CCA1 and LHY suppressed DREB1 expression, wheras in stressed condition RVE4/RVE8 translocate from cytoplasm to the nucleus and induces the expression of CBFs/DREB1 through cis acting element EE by rapidly degrading CCA1and LHY. Abbreviations: RLK, receptors like protein kinases; LRR-RLK leucine-rich repeats receptor-like protein kinase; CNGC, cyclic nucleotide-gated calcium channel; GLRs, glutamate-like receptor homologs; Ca²⁺, calcium ion; calcium binding proteins like CaM, calmodulin; CML, CaM-like proteins; CDPKs, Ca²⁺ dependent protein kinases; CBLs, calcineurin B-like proteins; MAPK, mitogen-activated protein kinase; CBFs, C-repeat Binding Factors; ICE, Inducer of CBF Expression; COR, cold-responsive; ROS, reactive oxygen species; NO, nitric oxide; CRPK1, cold-responsive protein kinase 1; RVE4/8, reveille4/8; lhy-cca1-Like1 (/LCL1); CCA1, circadian clock’s oscillator component circadian clock-associated1; LHY, late elongated hypocotyl; EE, cis acting element; TFs, transcription factors; DREB1, dehydration responsive element binding-protein 1.

FIGURE 2

Epigenetic components involved in cold stress response in plants. Cold is sensed by upstream sensors followed by the activation of downstream gene expression. Under normal temperature conditions, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 15 (HOS15) interacts with HISTONE DEACETYLASE 2C (HD2C), and represses COLD RESPONSIVE (COR) gene expression by deacetylation. However, under cold stress conditions, HOS15 promotes HD2C degradation by ubiquitination, resulting in the increase of H3 acetylation on COR promoters. HOS15 also recruits CBFs to the COR promoters to activate COR gene expression. The chromatin remodeler PICKLE (PKL) modulates the chromatin status of COR genes through H3K27me3-dependent silencing. Also, under cold miR397a leads to the up-regulation of COR genes and enhanced cold tolerance.

FIGURE 3

Different morphological, biochemical, physiological and molecular mitigation strategy acquired by plants upon cold stress. Change in different mitigation strategy are indicated by arrow (up) indicates increased concentration/expression, whereas arrow (down) indicates decreased concentration/expression). Abbreviations: Ca²⁺, calcium ion; NO, nitric oxide; MAPK, mitogen-activated protein kinase; COR genes, cold responsive genes; AFPs, antifreeze proteins; HSPs, heat shock proteins; CSPs, cold shock proteins.