XRN4 and LARP1 Are Required for a Heat-Triggered mRNA Decay Pathway Involved in Plant Acclimation and Survival during Thermal Stress

Abstract

To survive adverse and ever-changing environmental conditions, an organism must be able to adapt. It has long been established that the cellular reaction to stress includes the upregulation of genes coding for specific stress-responsive factors. In the present study, we demonstrate that during the early steps of the heat stress response, 25% of the Arabidopsis seedling transcriptome is targeted for rapid degradation. Our findings demonstrate that this process is catalyzed from 5' to 3' by the cytoplasmic exoribonuclease XRN4, whose function is seemingly reprogrammed by the heat-sensing pathway. The bulk of mRNAs subject to heat-dependent degradation are likely to include both the ribosome-released and polysome associated polyadenylated pools. The cotranslational decay process is facilitated at least in part by LARP1, a heat-specific cofactor of XRN4 required for its targeting to polysomes. Commensurate with their respective involvement at the molecular level, LARP1 and XRN4 are necessary for the thermotolerance of plants to long exposure to moderately high temperature, with xrn4 null mutants being almost unable to survive. These findings provide mechanistic insights regarding a massive stress-induced posttranscriptional downregulation and outline a potentially crucial pathway for plant survival and acclimation to heat stress.

Global Analysis of Truncated RNA Ends Reveals New Insights into Ribosome Stalling in Plants

“…Cotranslation mRNA decay was also demonstrated to be mediated by XRN4 and involved in the reprogramming of gene expression under heat stress in Arabidopsis (Merret et al, 2013(Merret et al, , 2015. Here, we further demonstrate that footprints of ribosomes are widespread in the RNA degradome of various plant species.…”

Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function

“…For example, cotranslational decay appears to control rapid down-regulation of excess-light-activated transcripts during stress recovery in Arabidopsis plants (Crisp et al, 2017). Moreover, within 15 min of pronounced heat stress (38°C), approximately 25% of the Arabidopsis seedling transcriptome is targeted for XRN4-dependent degradation, including both polysome-associated and polysome-released mRNAs (Merret et al, 2013). The heat-induced decay of polysomal mRNAs is dependent on LA RELATED PROTEIN 1A (LARP1A).…”

“…The heat-induced decay of polysomal mRNAs is dependent on LA RELATED PROTEIN 1A (LARP1A). High heat triggers the accumulation of XRN4 and the decapping proteins DECAPPING1 (DCP1) and DCP2 in polysomes (Merret et al, 2013) and seems to coincide with ribosome pausing in 59 mRNA regions to elicit XRN4-dependent decay (Merret et al, 2015). It will be of interest to know how heat triggers the prerequisite mRNA decapping and whether the discrimination of mRNAs for heat-regulated turnover is integrated with the recently uncovered role of eIF5B1 in maintaining efficient translation of a subset of mRNAs, notably those that encode low-M r nonstress proteins, during heat stress in Arabidopsis (Zhang et al, 2017a).…”

Germination Potential of Dormant and Nondormant Arabidopsis Seeds Is Driven by Distinct Recruitment of Messenger RNAs to Polysomes

“…Cells debris were eliminated by centrifugation at 14,000g for 15 min at 4°C, and the supernatant was filtrated with Miracloth. Proteins were precipitated by adding 2 volumes of ethanol and incubated at 4°C for 6 h (Merret et al, 2013). After 15 min of centrifugation at 14,000g at 4°C, the pellet was solubilized with 23 Laemmli buffer.…”