Translation machinery reprogramming in programmed cell death in Saccharomyces cerevisiae

Francesco Monticolo,Emanuela Palomba,Maria Luisa Chiusano

doi:10.1038/s41420-020-00392-x

Francesco Monticolo, Emanuela Palomba + Show 1 more

Open Access

https://doi.org/10.1038/s41420-020-00392-x

Copy DOI

Abstract

Programmed cell death involves complex molecular pathways in both eukaryotes and prokaryotes. In Escherichia coli, the toxin–antitoxin system (TA-system) has been described as a programmed cell death pathway in which mRNA and ribosome organizations are modified, favoring the production of specific death-related proteins, but also of a minor portion of survival proteins, determining the destiny of the cell population. In the eukaryote Saccharomyces cerevisiae, the ribosome was shown to change its stoichiometry in terms of ribosomal protein content during stress response, affecting the relative proportion between ohnologs, i.e., the couple of paralogs derived by a whole genome duplication event. Here, we confirm the differential expression of ribosomal proteins in yeast also during programmed cell death induced by acetic acid, and we highlight that also in this case pairs of ohnologs are involved. We also show that there are different trends in cytosolic and mitochondrial ribosomal proteins gene expression during the process. Moreover, we show that the exposure to acetic acid induces the differential expression of further genes coding for products related to translation processes and to rRNA post-transcriptional maturation, involving mRNA decapping, affecting translation accuracy, and snoRNA synthesis. Our results suggest that the reprogramming of the overall translation apparatus, including the cytosolic ribosome reorganization, are relevant events in yeast programmed cell death induced by acetic acid.

Highlights

Programmed cell deaths (PCDs) are a group of diversified processes that are triggered by stress or developmental events, occurring in both prokaryotes and eukaryotes[1,2,3,4]
They are accompanied by Gene Ontology (GO) terms related to ribosome biogenesis, rRNA processing, and translation at 200 min (Fig. 2, Supplemental Table S2)
We show that transcriptomic changes extensively involve genes associated with ribosome biogenesis and rRNA maturation, inducing mRNA decapping and affecting translation accuracy, indicating a reprogramming of the cell translational apparatus during the exposure

Summary

Introduction

Programmed cell deaths (PCDs) are a group of diversified processes that are triggered by stress or developmental events, occurring in both prokaryotes and eukaryotes[1,2,3,4]. Specific events involving translation processes during PCD have been reported. Reduce MazE levels in the cell, favoring the release of the MazF toxin[13] This endoribonuclease can produce leaderless mRNAs14 and modify 16S rRNA structure in the ribosomes, producing the “stress ribosomes”[15,16,17]. These events dramatically affect the overall translational process[18], determining the parallel production of “death” (ClpP, SlyD, YfiD, ElaC, YgcR, and YfbU) and of “survival”

Methods

Results

Conclusion