Untranslated yet indispensable-UTRs act as key regulators in the environmental control of gene expression

Abstract

To survive and thrive in a dynamic environment, plants must continuously monitor their surroundings and adjust their development and physiology accordingly. Changes in gene expression underlie these developmental and physiological adjustments, and are traditionally attributed to widespread transcriptional reprogramming. Growing evidence, however, suggests that post-transcriptional mechanisms also play a vital role in tailoring gene expression to a plant's environment. Untranslated regions (UTRs) act as regulatory hubs for post-transcriptional control, harbouring cis-elements that affect an mRNA's processing, localization, translation, and stability, and thereby tune the abundance of the encoded protein. Here, we review recent advances made in understanding the critical function UTRs exert in the post-transcriptional control of gene expression in the context of a plant's abiotic environment. We summarize the molecular mechanisms at play, present examples of UTR-controlled signalling cascades, and discuss the potential that resides within UTRs to render plants more resilient to a changing climate.

Keywords: Abiotic stress; RNA processing; RNA structure; RNA-binding protein (RBP); alternative splicing; gene expression; post-transcriptional regulation; translation; untranslated region (UTR).

Fig. 1.

Post-transcriptional mechanisms controlling gene expression in plants. After transcription by RNA polymerase II (RNA Pol II), a pre-mRNA undergoes processing, which includes attachment of the m⁷G cap structure at the 5' end, cleavage and polyadenylation at the 3' end, as well as splicing and nucleotide modifications such as m⁶A (1). The resulting mature mRNA is then tightly packed into a ribonucleoprotein complex and exported into the cytoplasm through nuclear pore complexes (2). Some cytoplasmic mRNAs will immediately undergo translation (3), which is tightly regulated at the level of initiation (and includes recruitment of the pre-initiation complex, scanning of the 5' UTR, and assembly of the full ribosome at the AUG initiation codon). RNAs can also be sequestered into biomolecular condensates, from which they are later re-released (4). Finally, mRNAs are subjected to degradation (5), which can be a result of mRNA quality control or specific RNA modifications; it can also occur co-translationally or within biomolecular condensates. Solid arrows indicate movement of molecular components during translation; dotted arrows indicate the mRNA’s progression through consecutive stages of gene expression. Blue spheres represent proteins or (ribonucleo)protein complexes; numbers within the spheres indicate specific eukaryotic initiation factors (eIFs).

Fig. 2.

Regulatory features of 5' and 3' UTRs and their role in environmental responses. (A) UTRs act as hubs for post-transcriptional regulation of mRNA function and thereby ultimately determine the abundance of the encoded protein. Regulatory features of UTRs include binding sites for RBPs, miRNAs, and lncRNAs, uORFs, RNA secondary structures such as hairpins and RNA G-quadruplexes (RG4s), as well as sites for splicing, nucleotide modification, and polyadenylation, the latter determined with the help of far (FUE) and near upstream elements (NUE). (B–I) Examples of UTR-mediated regulatory processes that operate in response to environmental signals. (B) PNT1 recruits the active phyB photoreceptor under red light, inhibiting translation of PORA mRNA and thereby regulating plant greening. (C) PhyB, together with the splicing factors RRC1 and SFPS, triggers intron retention in the PIF3 5' UTR; the retained intron contains a uORF that down-regulates PIF3 translation in the light and thereby promotes seedling de-etiolation. (D) Binding of the lncRNA cis-NATPHO1.2 triggers structural rearrangements in the 5' UTR and coding region of the rice PHO1.2 mRNA under phosphate starvation and thereby increases access of the large ribosomal subunit to the initiation codon. Translation of PHO1.2 increases, and elevated levels of PHO1.2 transporter allow for efficient redistribution of inorganic phosphate (Pi). (E) A thermosensitive hairpin in the PIF7 5' UTR adopts a more relaxed conformation at elevated temperatures, which acts as a translational enhancer. Increased levels of PIF7 subsequently promote temperature-induced hypocotyl elongation. (F) MiR156/157 bind to the 3' UTR of SPL3 and trigger the transcript’s degradation via ARGONAUTE 1 (AGO1). MiR156/157 levels are reduced at elevated temperature, allowing SPL3 protein to accumulate and induce flowering. (G) An m⁶A modification in the PIF4 3' UTR under red light destabilizes the transcript, thereby promoting photomorphogenesis. (H) Formation of an RG4 in the CORG1 3' UTR at low temperature prevents degradation of the transcript and thereby attenuates growth in the cold. (I) Selection of a distal polyadenylation site in the HKT1 3' UTR enhances translation under salt stress; increased production of the HKT1 transporter subsequently increases export of sodium ions and thereby promotes salt tolerance in Spartina alterniflora. Arrows indicate positive regulation; blunt arrows indicate negative regulation; dotted arrows denote environmental effects. Ribosomes are depicted in bright blue.