Mitoribosomal regulation of OXPHOS biogenesis in plants

Abstract

The ribosome filter hypothesis posits that ribosomes are not simple non-selective translation machines but may also function as regulatory elements in protein synthesis. Recent data supporting ribosomal filtering come from plant mitochondria where it has been shown that translation of mitochondrial transcripts encoding components of oxidative phosphorylation complexes (OXPHOS) and of mitoribosomes can be differentially affected by alterations in mitoribosomes. The biogenesis of mitoribosome was perturbed by silencing of a gene encoding a small-subunit protein of the mitoribosome in Arabidopsis thaliana. As a consequence, the mitochondrial OXPHOS and ribosomal transcripts were both upregulated, but only the ribosomal proteins were oversynthesized, while the OXPHOS subunits were actually depleted. This finding implies that the heterogeneity of plant mitoribosomes found in vivo could contribute to the functional selectivity of translation under distinct conditions. Furthermore, global analysis indicates that biogenesis of OXPHOS complexes in plants can be regulated at different levels of mitochondrial and nuclear gene expression, however, the ultimate coordination of genome expression occurs at the complex assembly level.

Keywords: OXPHOS; coordination of gene expression; mitochondrial translation; mitoribosome; ribosome filter hypothesis; ribosome heterogeneity.

FIGURE 1

Heterogeneity of mitoribosomes differentially affects the translation of mitochondrial OXPHOS and ribosomal proteins (based on Kwaśniak et al., 2013). In rps10 protein synthesis is carried out by a heterogeneous population of mitoribosomes characterized by an excess of free LSU subunits and a portion of SSUs lacking the S10 protein (black asterisk). Decreased translation of OXPHOS in rps10 results mainly from the reduced number of ribosomes per mRNA, whereas increased translation of mitoribosomal proteins results from enhanced ribosomal loading and also increased ribosomal density. In consequence, OXPHOS proteins are depleted, whereas mitoribosomal proteins over-abundant in rps10 mitochondria compared to wild-type ones. The amount of proteins translated by mitoribosomes is represented by the size of the black bands.