Preferential Ribosome Loading on the Stress-Upregulated mRNA Pool Shapes the Selective Translation under Stress Conditions

Abstract

The reprogramming of gene expression is one of the key responses to environmental stimuli, whereas changes in mRNA do not necessarily bring forth corresponding changes of the protein, which seems partially due to the stress-induced selective translation. To address this issue, we systematically compared the transcriptome and translatome using self-produced and publicly available datasets to decipher how and to what extent the coordination and discordance between transcription and translation came to be in response to wounding (self-produced), dark to light transition, heat, hypoxia, Pi starvation and the pathogen-associated molecular pattern (elf18) in Arabidopsis. We found that changes in total mRNAs (transcriptome) and ribosome-protected fragments (translatome) are highly correlated upon dark to light transition or heat stress. However, this close correlation was generally lost under other four stresses analyzed in this study, especially during immune response, which suggests that transcription and translation are differentially coordinated under distinct stress conditions. Moreover, Gene Ontology (GO) enrichment analysis showed that typical stress responsive genes were upregulated at both transcriptional and translational levels, while non-stress-specific responsive genes were changed solely at either level or downregulated at both levels. Taking wounding responsive genes for example, typical stress responsive genes are generally involved in functional categories related to dealing with the deleterious effects caused by the imposed wounding stress, such as response to wounding, response to water deprivation and response to jasmonic acid, whereas non-stress-specific responsive genes are often enriched in functional categories like S-glycoside biosynthetic process, photosynthesis and DNA-templated transcription. Collectively, our results revealed the differential as well as targeted coordination between transcriptome and translatome in response to diverse stresses, thus suggesting a potential model wherein preferential ribosome loading onto the stress-upregulated mRNA pool could be a pacing factor for selective translation.

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

“…In the first instance, this may reflect a transient pausing of elongation, without eliciting mRNA degradation, which resumes as cells begin to acclimate to the new conditions, as was observed in yeast (Shalgi et al., 2013 ). Simultaneously, preferential translation may be occurring for light stress‐associated genes to facilitate an acclimatory response (Chen et al., 2021 ). The concordance between total and polysome‐associated mRNA levels was also uncoupled rapidly upon transition to recovery, but is eventually re‐established after 30 min (Figure S5 c).…”

“…Preferential translation may also permit a cell to make rapid changes in protein levels independently of transcription (Muñoz & Castellano, 2012 ). In order to prioritise resources during adverse conditions, translation is often globally repressed with the exception of a subset of transcripts required for stress responses (Chen et al., 2021 ; Juntawong et al., 2014 ). The repression of translation can involve degradation or transcriptional repression of genes encoding ribosomal proteins or translational factors (Munchel et al., 2011 ; Sheikh et al., 1999 ); however, a more rapid response is facilitated through dissociation of transcripts from initiation factors and ribosomes (Bresson et al., 2020 ; Liu & Qian, 2014 ).…”

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

“…In the first instance, this may reflect a transient pausing of elongation, without eliciting mRNA degradation, which resumes as cells begin to acclimate to the new conditions, as was observed in yeast (Shalgi et al 2013). Simultaneously, preferential translation may be occurring for light stress-associated genes to facilitate an acclimatory response (Chen et al 2021). The concordance between total and polysome-bound mRNA levels was also uncoupled rapidly upon transition to recovery, but is eventually re-established after 30 minutes (Figure S4 C).…”

“…Preferential translation may permit a cell to make rapid changes in protein levels independently of transcription (Muñoz and Castellano 2012). As prioritisation of energy and resources is often paramount during adverse conditions, translation is often repressed globally with the exception of a subset of transcripts required for stress responses (Chen et al 2021; Juntawong et al 2014). The repression of translation can involve degradation or transcriptional repression of genes encoding ribosomal proteins or translational factors (Sheikh et al 1999; Munchel et al 2011); however, a more rapid response is facilitated through dissociation of transcripts from initiation factors and ribosomes (Liu and Qian 2014; Bresson et al 2020).…”

Synergism and antagonism in plant acclimation to abiotic stress combinations

“…The cellular mRNA pool associated with actively translating ribosomes is termed translatome and undergoes rapid and profound reorganization upon environmental changes, e.g., upon wounding (Chen et al 2021) or following the shift of low light-acclimated plants to high light (Moore et al 2021). Only this pool is used to synthesize de novo proteins.…”