Arabidopsis thaliana eIF4E1 and eIF(iso)4E Participate in Cold Response and Promote Translation of Some Stress-Related mRNAs

Abstract

Plant defense and adaptation to adverse environmental conditions rely on gene expression control, such as mRNA transcription, processing, stability, and translation. Sudden temperature changes are common in the era of global warming; thus, understanding plant acclimation responses at the molecular level becomes imperative. mRNA translation initiation regulation has a pivotal role in achieving the synthesis of the appropriate battery of proteins needed to cope with temperature stress. In this study, we analyzed the role of translation initiation factors belonging to the eIF4E family in Arabidopsis acclimation to cold temperatures and freezing tolerance. Using knockout (KO) and overexpressing mutants of AteIF4E1 or AteIF(iso)4E, we found that AteIF4E1 but not AteIF(iso)4E overexpressing lines displayed enhanced tolerance to freezing without previous acclimation at 4°C. However, KO mutant lines, eif(iso)4e-1 and eif4e1-KO, were more sensitive to the stress. Cold acclimation in wild-type plants was accompanied by increased levels of eIF4E1 and eIF(iso)4E transcript levels, polysomes (P) enrichment, and shifts of these factors from translationally non-active to active fractions. Transcripts, previously found as candidates for eIF(iso)4E or eIF4E1 selective translation, changed their distribution in both P and total RNA in the presence of cold. Some of these transcripts changed their polysomal distribution in the mutant and one eIF4E1 overexpressing line. According to this, we propose a role of eIF4E1 and eIF(iso)4E in cold acclimation and freezing tolerance by regulating the expression of stress-related genes.

The Arabidopsis eIF4E1 regulates NRT1.1‐mediated nitrate signaling at both translational and transcriptional levels

“…eIF4E1 encodes a translation initiation factor 4E, which recognizes mRNA 5′‐cap structure and interacts with eIF4G and other factors to form the initiation complex, leading to translation initiation (Jackson et al ., 2010; Aitken & Lorsch, 2012). eIF4E1 has been reported to function in virus resistance, flowering time, root and root hair growth, and cold response (Robaglia & Caranta, 2006; Bastet et al ., 2018; Bastet et al ., 2019; Zhu et al ., 2020; Salazar‐Diaz et al ., 2021; T. Liu et al ., 2022). We found that eIF4E1 plays a crucial role in primary nitrate response and nitrate metabolism (Figs 1, 2).…”

Plant eIF4E isoforms as factors of susceptibility and resistance to potyviruses

“…In contrast, double knockout of both eIF4E1 and eIF(iso)4E in Arabidopsis was lethal (Callot and Gallois, 2014). Arabidopsis eIF4E1 or eIF(iso)4E inactivation decreased tolerance to low temperatures (Salazar-Dıáz et al, 2021), while had no effect on elf18-induced resistance against the bacteria Pseudomonas syringae pv. maculicola (Wang et al, 2022).…”

ICE‐SCREAM comes in different flavors: Angiosperms encode two types of ICE proteins predicted to differ in their regulation by OST1 and MPK3/6

“…Cold-responsive translation initiation factors can also cause the translation of certain transcripts, preferentially under low temperature conditions to presumably contribute to cold acclimation; the identified transcripts included putative regulators of ICE (Salazar-Díaz et al, 2021).…”

“…Interestingly, Singha et al (2014) reported that distinct codons were preferred for MPK KINASE KINASE (MPKKK) proteins in rice which they suggest might cause low expression under normal conditions and higher expression under stress conditions. Cold‐responsive translation initiation factors can also cause the translation of certain transcripts, preferentially under low temperature conditions to presumably contribute to cold acclimation; the identified transcripts included putative regulators of ICE (Salazar‐Díaz et al, 2021).…”