The translational landscape of Arabidopsis mitochondria

Abstract

Messenger RNA translation is a complex process that is still poorly understood in eukaryotic organelles like mitochondria. Growing evidence indicates though that mitochondrial translation differs from its bacterial counterpart in many key aspects. In this analysis, we have used ribosome profiling technology to generate a genome-wide snapshot view of mitochondrial translation in Arabidopsis. We show that, unlike in humans, most Arabidopsis mitochondrial ribosome footprints measure 27 and 28 bases. We also reveal that respiratory subunits encoding mRNAs show much higher ribosome association than other mitochondrial mRNAs, implying that they are translated at higher levels. Homogenous ribosome densities were generally detected within each respiratory complex except for complex V, where higher ribosome coverage corroborated with higher requirements for specific subunits. In complex I respiratory mutants, a reorganization of mitochondrial mRNAs ribosome association was detected involving increased ribosome densities for certain ribosomal protein encoding transcripts and a reduction in translation of a few complex V mRNAs. Taken together, our observations reveal that plant mitochondrial translation is a dynamic process and that translational control is important for gene expression in plant mitochondria. This study paves the way for future advances in the understanding translation in higher plant mitochondria.

An Update on Mitochondrial Ribosome Biology: The Plant Mitoribosome in the Spotlight

“…An interaction between partially edited mRNAs and mitoribosomes has also been indicated by the results of mitoribosomal profiling in Arabidopsis [56], supporting earlier studies which showed that complete editing of mitochondrial mRNAs is not a pre-requisite for their translation. However, the mitoribosome-associated mRNAs are more fully edited than the total pool of RNAs.…”

“…A mitoribosomal profiling analysis of the Arabidopsis translatome has revealed strikingly different mitoribosome association levels with different mtRNAs. mRNAs encoding subunits of OXPHOS complexes showed much higher ribosome loading levels compared to mitochondrial transcripts of ribosomal proteins or those encoding c-type cytochrome maturation factors, implying that the OXPHOS proteins are translated preferentially [50,56]. Low levels of mitoribosome footprints were detected for maturase (MatR) and the TatC protein also known as MttB although these proteins are not identified by mass spectrometry [57].…”

Topologies of N6‐adenosine methylation (m6A) in land plant mitochondria and their putative effects on organellar gene expression

“…Cm 6 AG). Analyses of ribosome footprint of Arabidopsis mitochondria did not reveal any new translated mtORFs in Arabidopsis mitochondria (Planchard et al , ). However, computational analysis indicated high similarity between the common m 6 A motifs in the coding regions of known genes and mtORFs of Brassicales mitochondrial RNAs (i.e.…”

The PPR-related splicing cofactor MSP1/EMB1025 protein, encoded by At4g20090, encode an essential protein that is required for the splicing ofnad1intron 1 and for the biogenesis of complex I in Arabidopsis mitochondria

“…Complexes, I, III, IV, V and the ribosomes are all assemblies of subunits that are expressed by both nuclear-and organellar loci, thus necessitating complex mechanism to regulate the expression and accumulation of the organellar-localized proteins during development and various growth conditions (Gualberto et al 2014, Hammani and Giege 2014, Law et al 2014. Accordingly, organellar ribosome footprint analyses indicate that mitochondria-encoded mRNAs are differentially translated, while the synthesis of plastidial proteins directly correlate with the abundances of the mature transcript with the organelles (Chotewutmontri and Barkan 2016, Planchard, et al 2018.…”

“…Accumulating data indicate that the regulation of RNA-processing plays a pivotal role in the expression of organellar genes in plants (Brown et al 2014, Gualberto and Kuhn 2014, Hammani and Giege 2014, Schmitz-Linneweber et al 2015. The significance of posttranscriptional regulation in plant mitochondria is further reflected by the extended half-lives of many mtRNAs, and the fact that their translation seemed uncoupled from their transcription (Kühn et al 2007, Kühn et al 2005, Planchard et al 2018. Accordingly, altered mtRNA metabolism often result with severe growth and developmental defect phenotypes.…”