Translational reprogramming under heat stress: a plant's perspective

Abstract

Plants experience dynamic and sometimes extreme fluctuations in temperature on hourly, daily and seasonal scales, which are becoming increasingly challenging as climate change progresses. To maximize fitness and chances of survival, plants continuously adjust their growth, development and physiology to their temperature environment. Changes in protein synthesis are central to these acclimatization processes, enabling rapid and precise modulation of cellular functions. In this review, we discuss the molecular mechanisms driving heat-induced translational reprogramming, integrating insights from animal and yeast systems with current knowledge and emerging hypotheses in plants. We revisit the core stages of translation-initiation, elongation and termination-and the roles of associated translation factors while also exploring emerging areas of interest, including biomolecular condensates, RNA modifications and cis-regulatory elements. Finally, we consider how a deeper understanding of translational control could be harnessed to enhance crop resilience in the face of climate change.

Keywords: heat stress; protein synthesis; temperature sensing; translation; translation factors.

Figure 1.

Overview of canonical translation in eukaryotes. (a) Translation initiation is governed by eukaryotic initiation factors (eIFs) and begins with the binding of the cap-binding complex (eIF4E and eIF4G) to the mRNA’s 5′ m⁷Gppp cap and the association of PABPs with eIF4G and the poly-A tail, resulting in mRNA circularization. eIF4G recruits DEAD-box helicases eIF4A and eIF4B to unwind RNA secondary structures. In parallel, the 43S pre-initiation complex (PIC), composed of the 40S ribosomal subunit, ternary complex (TC, consisting of eIF2-GTP and the initiator tRNA), eIF1, eIF1A, eIF3 and eIF5 assembles, binds to the mRNA and interacts with the cap-binding complex to form the 48S scanning complex. The 48S complex scans the 5′ UTR in 5′ to 3′ direction to identify the initiation codon, whereupon it adopts a closed conformation, stabilizing the initiator tRNA in the peptidyl (P)-site. eIF1 and eIF5 dissociate, triggering eIF2-GTP hydrolysis and the release of eIF2-GDP, eIF3, eIF4 and PABPs. Subsequently, eIF5B-GTP mediates 60S subunit joining with the aid of eIF1A. Hydrolysis of eIF5B-GTP results in the formation of the functional 80S ribosome, ready for peptide elongation. (b) The elongation cycle commences when an aminoacyl-tRNA, escorted by eukaryotic elongation factor 1A (eEF1A)-GTP, binds the mRNA codon in the ribosomal aminoacyl (A)-site, triggering GTP hydrolysis by eEF1A and securing the tRNA’s position. The ribosome’s peptidyl transferase centre (PTC) catalyses peptide bond formation between the A-site tRNA’s amino acid and the nascent polypeptide chain on the P-site tRNA, transferring the chain to the A-site. eEF2-GTP then binds, and GTP hydrolysis drives translocation of the ribosome along the mRNA, moving the peptidyl-tRNA to the P-site and the deacylated tRNA to the exit (E)-site. The A-site is freed for the next aminoacyl-tRNA, and the cycle continues until a stop codon signals termination. (c) Termination occurs when a stop codon (UAA, UAG or UGA) enters the ribosome’s A-site. Stop codons are recognized by eukaryotic release factor 1 (eRF1). eRF1, aided by eRF3, triggers hydrolysis of the bond between the polypeptide chain and the tRNA in the P-site, catalysed by the ribosome’s PTC. Following polypeptide release, ABCE1 facilitates the dissociation of ribosomal subunits, mRNA and deacylated tRNA.

Figure 2.

Regulation of eukaryotic initiation factors during heat stress. (a) Under non-stress conditions, eukaryotic initiation factors promote canonical translation initiation, resulting in efficient translation even of structurally complex housekeeping mRNAs. Active TOR complex 1 (TORC1) promotes translation via phosphorylation of eIF4E binding protein (4EBP) and ribosomal protein S6 kinase 1 (S6K1), inhibiting 4EBP but activating S6K1. S6K1 subsequently phosphorylates eIF4B, leading to its recruitment by eIF4A/eIF4G. In parallel, active, GTP-containing ternary complexes (TCs) are constantly replenished by the GDP–GTP exchange factor eIF2B. (b) Under heat stress, hypo-phosphorylated 4EBP binds to and inhibits eIF4E, while inactive S6K1 does the same with eIF3. Additionally, the TC’s eIF2α subunit becomes phosphorylated, causing the TC to be sequestered by eIF2B. eIF4G undergoes a conformational change that leads to the release of eIF4A. The eIF4E/4G complex, alongside other initiation factors, the 40S ribosomal subunit and many housekeeping mRNAs, is recruited into stress granules. These processes jointly cause a global reduction in canonical translation. eIF4A can independently promote the translation of some structurally simple mRNAs encoding heat shock proteins (HSPs), while other heat-induced mRNAs employ an internal ribosomal entry site (IRES) to enable cap-independent translation. Numbers represent initiation factors, solid arrows indicate positive regulation and perpendicular lines indicate inhibition. The processes depicted here were shown to regulate translation under heat stress in animals and/or yeast; while many signalling components are conserved, it is currently unclear whether the same mechanisms operate in plants.