Rewiring of aminoacyl-tRNA synthetase localization and interactions in plants with extensive mitochondrial tRNA gene loss

Warren, Jessica M.; Broz, Amanda K.; Martinez-Hottovy, Ana; Elowsky, Christian; Christensen, Alan C.; Sloan, Daniel B

doi:10.1101/2022.01.27.478071

Cited by 6 publications

(19 citation statements)

References 89 publications

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“…However, the most notable and consistent exception to this appears to be the cytosolic phenylalanine aaRS. This enzyme is the only of the cytosolic aaRSs to be expressed as two different subunits, which likely hinders retargeting and functional replacement of its mitochondrial aaRS counterpart (Pett and Lavrov 2015;Warren and Sloan 2022). Therefore, in cases of mitochondrial tRNA-Phe loss, the native mitochondrial phenylalanine aaRS is retained and presumably must adapt to charge the newly imported cytosolic tRNA.…”

Section: Multisubunit Complexes and Extent Of Protein-protein Interac...mentioning

confidence: 99%

Incompatibility and interchangeability in molecular evolution

Sloan¹,

Warren²,

Williams³

et al. 2022

Preprint

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There is remarkable variation in the rate at which genetic incompatibilities in molecular interactions accumulate. In some cases, minor changes – even single nucleotide substitutions – create major epistatic incompatibilities when hybridization forces new variants to function in a novel genetic background from an isolated population. In other cases, genes or even entire functional pathways can be horizontally transferred between anciently divergent evolutionary lineages that span the tree of life with little evidence of incompatibilities. In this review, we explore whether there are general principles that can explain why certain genes are prone to epistatic incompatibilities while others maintain interchangeability. We summarize evidence pointing to four genetic features that may contribute to greater resistance to functional replacement: 1) function in multisubunit enzyme complexes and protein-protein interactions, 2) sensitivity to changes in gene dosage, 3) rapid rate of sequence evolution, and 4) overall importance to cell viability, which creates sensitivity to small perturbations in molecular function. We discuss the relative levels of support for these different hypotheses and lay out future directions that may help explain the striking contrasts in patterns of incompatibility and interchangeability throughout the history of molecular evolution.

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Section: Multisubunit Complexes and Extent Of Protein-protein Interac...mentioning

confidence: 99%

Incompatibility and interchangeability in molecular evolution

Sloan¹,

Warren²,

Williams³

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…In two cases (organellar AspRS and cytosolic TyrRS), the nominal p-value for increased rates on foreground branches was less than 0.05, but these comparisons did not remain significant after correction for multiple tests. *Organellar PheRS could also be a potential case of plastid specialization because Sileneae contains duplicate copies with one apparently functioning in the mitochondria and another apparently functioning in the plastids (Warren, et al 2022), but this analysis was run with the putative mt copy set as the foreground branches.…”

Section: Rates Of Aars Sequence Evolution In Sileneaementioning

confidence: 99%

“…Alignments of trimmed Sileneae aaRS nucleotide sequences and phylogenetic trees were taken from a previous study (Warren, et al 2022). The A. thaliana sequences that were originally used as outgroups were removed from the alignments.…”

Section: Sileneae Aars Positive Selection Analysismentioning

confidence: 99%

“…To perform phylogenetic tests for selection on Sileneae aaRSs, A. thaliana genes were pruned from the original trees (Warren, et al 2022), using the drop.tip function in the ape v5.4-1 package in R (Paradis and Schliep 2018). The phylotree.js tool (Shank, et al 2018) was then used to label branches as "Foreground" if they were inferred to meet one of the criteria described in the main text or Table 1 (i.e., new tRNA substrate, gain of mt import by a cytosolic aaRS, or specialization on plastid function).…”

Section: Sileneae Aars Positive Selection Analysismentioning

confidence: 99%

“…Therefore, it is not clear if and how organellar aaRS are able to charge these newly imported tRNAs in the mitochondria. Results from in silico analysis of putative targeting peptides and fluorescence microscopy assays of subcellular localization in Silenenae have identified two alternative pathways (Warren, et al 2022). In some cases, changes in tRNA import have been accompanied by retargeting of the corresponding cytosolic aaRS such that the ancestral pairing between tRNA and aaRS is maintained and simply relocated to a second compartment.…”

Section: Introductionmentioning

confidence: 99%

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Aminoacyl-tRNA synthetase evolution within the dynamic tripartite translation system of plant cells

Sloan

DeTar

Warren

2022

Preprint

Self Cite

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Eukaryotes maintain separate protein translation systems for nuclear and organellar genes, including distinct sets of tRNAs and aminoacyl-tRNA synthetases (aaRSs). In animals, mitochondrial-targeted aaRSs are expressed at lower levels and are less conserved in sequence than cytosolic aaRSs involved in translation of nuclear mRNAs, likely reflecting lower translational demands in mitochondria. In plants, translation is further complicated by the presence of plastids, which share most aaRSs with mitochondria. In addition, plant mitochondrial tRNA pools have a dynamic history of gene loss and functional replacement by tRNAs from other compartments. To investigate the consequences of these distinctive features of translation in plants, we analyzed sequence evolution in angiosperm aaRSs. In contrast to previously studied eukaryotic systems, we found that plant organellar and cytosolic aaRSs exhibit only a small difference in expression levels, and organellar aaRSs are slightly more conserved than cytosolic aaRSs. We hypothesize that these patterns result from high translational demands associated with photosynthesis in mature chloroplasts. We also investigated aaRS evolution in Sileneae, an angiosperm lineage with extensive mitochondrial tRNA replacement and aaRS retargeting. We predicted positive selection for changes in aaRS sequence resulting from these recent changes in subcellular localization and tRNA substrates but found little evidence for accelerated sequence divergence. Overall, the complex tripartite translation system in plant cells appears to have imposed more constraints on the long-term evolutionary rates of organellar aaRSs compared to other eukaryotic lineages, and plant aaRS protein sequences appear largely robust to more recent perturbations in subcellular localization and tRNA interactions.

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Incompatibility and Interchangeability in Molecular Evolution

Sloan

Warren

Williams

et al. 2022

Genome Biology and Evolution

View full text Add to dashboard Cite

There is remarkable variation in the rate at which genetic incompatibilities in molecular interactions accumulate. In some cases, minor changes – even single nucleotide substitutions – create major incompatibilities when hybridization forces new variants to function in a novel genetic background from an isolated population. In other cases, genes or even entire functional pathways can be horizontally transferred between anciently divergent evolutionary lineages that span the tree of life with little evidence of incompatibilities. In this review, we explore whether there are general principles that can explain why certain genes are prone to incompatibilities while others maintain interchangeability. We summarize evidence pointing to four genetic features that may contribute to greater resistance to functional replacement: 1) function in multisubunit enzyme complexes and protein-protein interactions, 2) sensitivity to changes in gene dosage, 3) rapid rate of sequence evolution, and 4) overall importance to cell viability, which creates sensitivity to small perturbations in molecular function. We discuss the relative levels of support for these different hypotheses and lay out future directions that may help explain the striking contrasts in patterns of incompatibility and interchangeability throughout the history of molecular evolution.

show abstract

Rewiring of aminoacyl-tRNA synthetase localization and interactions in plants with extensive mitochondrial tRNA gene loss

Cited by 6 publications

References 89 publications

Incompatibility and interchangeability in molecular evolution

Incompatibility and interchangeability in molecular evolution

Aminoacyl-tRNA synthetase evolution within the dynamic tripartite translation system of plant cells

Incompatibility and Interchangeability in Molecular Evolution

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