A Unique Mitochondrial Transcription Factor B Protein in Dictyostelium discoideum

Manna, Sam; Le, Phuong Thi; Berthou, Christian

doi:10.1371/journal.pone.0070614

Cited by 6 publications

(11 citation statements)

References 59 publications

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“…produced undetectable amounts of transcripts, coexpression with Tfb1m improved transcription efficiency dramatically, to the point where it was suggested that Tfb1m may be the sole transcription factor necessary for mitochondrial transcription in D. discoideum (Manna et al, 2013). As illustrated above, mitochondrial function is dependent on nuclear-encoded protein import and this is facilitated by the TOM/TIM complexes in mitochondria.…”

Section: Dictyostelium Discoideum Homo Sapiensmentioning

confidence: 95%

“…While being shown to initiate transcription, RpmA, did so inefficiently, suggesting that, like other eukaryotes D. discoideum requires mitochondrial transcription factors for mtDNA transcription. Manna et al, (2013) identified and characterised a D. discoideum mitochondrial transcription factor B. Identified as tfb1m, this gene is 1,458 bp in size, with a corresponding amino acid sequence 485 residues in length, and approximately 56 kDa in molecular weight.…”

Section: Mitochondrial Transcriptionmentioning

confidence: 99%

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The Dictyostelium model for mitochondrial biology and disease

Pearce¹,

Annesley²,

Fisher³

2019

Int. J. Dev. Biol.

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The unicellular slime mould Dictyostelium discoideum is a valuable eukaryotic model organism in the study of mitochondrial biology and disease. As a member of the Amoebozoa, a sister clade to the animals and fungi, Dictyostelium mitochondrial biology shares commonalities with these organisms, but also exhibits some features of plants. As such it has made significant contributions to the study of eukaryotic mitochondrial biology. This review provides an overview of the advances in mitochondrial biology made by the study of Dictyostelium and examines several examples where Dictyostelium has and will contribute to the understanding of mitochondrial disease. The study of Dictyostelium's mitochondrial biology has contributed to the understanding of mitochondrial genetics, transcription, protein import, respiration, morphology and trafficking, and the role of mitochondria in cellular differentiation. Dictyostelium is also proving to be a versatile model organism in the study both of classical mitochondrial disease e.g. Leigh syndrome, and in mitochondria-associated neurodegenerative diseases like Parkinson's disease. The study of mitochondrial diseases presents a unique challenge due to the cryptic nature of their genotypephenotype relationship. The use of Dictyostelium can contribute to resolving this problem by providing a genetically tractable, haploid eukaryotic organism with a suite of readily characterised phenotype readouts of cellular signalling pathways. Dictyostelium has provided insight into the signalling pathways involved in multiple neurodegenerative diseases and will continue to provide a significant contribution to the understanding of mitochondrial biology and disease.

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Section: Dictyostelium Discoideum Homo Sapiensmentioning

confidence: 95%

Section: Mitochondrial Transcriptionmentioning

confidence: 99%

The Dictyostelium model for mitochondrial biology and disease

Pearce¹,

Annesley²,

Fisher³

2019

Int. J. Dev. Biol.

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“…This evolutionary relationship is supported by complementation studies. E. coli ksgA mutants lack methylated rRNA and are resistant to the aminoglycoside antibiotic kasugamycin [3,4]. The introduction of a mtTFB homolog into these mutants restores methylation and sensitivity to kasugamycin [4].…”

mentioning

confidence: 99%

“…E. coli ksgA mutants lack methylated rRNA and are resistant to the aminoglycoside antibiotic kasugamycin [3,4]. The introduction of a mtTFB homolog into these mutants restores methylation and sensitivity to kasugamycin [4]. Furthermore, the methyltransferase activity of mtTFB has been implicated in aminoglycoside-induced deafness, a disease involving hypermethylation of mutated mitochondrial small subunit rRNA and increased aminoglycoside sensitivity [3].…”

mentioning

confidence: 99%

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Emerging Insights into the Moonlighting Functions and Evolutionary Origins of Mitochondrial RNA Methyltransferases

Manna

Harman²

2015

IJGS

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Phylogenetic Reconstruction Shows Independent Evolutionary Origins of Mitochondrial Transcription Factors from an Ancient Family of RNA Methyltransferase Proteins

Harris

Goldman

2018

J Mol Evol

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Here, we generate a robust phylogenetic framework for the rRNA adenine N(6)-methyltransferase (RAMTase) protein family that shows a more ancient and complex evolutionary history within the family than previously reported. RAMTases occur universally by descent across the three domains of life, and typical orthologs within the family perform methylation of the small subunits of ribosomal RNA (rRNA). However, within the RAMTase family, two different groups of mitochondrial transcription factors, mtTFB1 and mtTFB2, have evolved in eukaryotes through neofunctionalization. Previous phylogenetic analyses have suggested that mtTFB1 and mtTFB2 comprise sister clades that arose via gene duplication, which occurred sometime following the endosymbiosis event that produced the mitochondrion. Through dense and taxonomically broad sampling of RAMTase family members especially within bacteria, we found that these eukaryotic mitochondrial transcription factors, mtTFB1 and mtTFB2, have independent origins in phylogenetically distant clades such that their divergence most likely predates the last universal common ancestor of life. The clade of mtTFB2s comprises orthologs in Opisthokonts and the clade of mtTFB1s includes orthologs in Amoebozoa and Metazoa. Thus, we clearly demonstrate that the neofunctionalization producing the transcription factor function evolved twice independently within the RAMTase family. These results are consistent with and help to elucidate outcomes from prior experimental studies, which found that some members of mtTFB1 still perform the ancestral rRNA methylation function, and the results have broader implications for understanding the evolution of new protein functions. Our phylogenetic reconstruction is also in agreement with prior studies showing two independent origins of plastid RAMTases in Viridiplantae and other photosynthetic autotrophs. We believe that this updated phylogeny of RAMTases should provide a robust evolutionary framework for ongoing studies to identify and characterize the functions of these proteins within diverse organisms.Electronic supplementary materialThe online version of this article (10.1007/s00239-018-9842-z) contains supplementary material, which is available to authorized users

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A Unique Mitochondrial Transcription Factor B Protein in Dictyostelium discoideum

Cited by 6 publications

References 59 publications

The Dictyostelium model for mitochondrial biology and disease

The Dictyostelium model for mitochondrial biology and disease

Emerging Insights into the Moonlighting Functions and Evolutionary Origins of Mitochondrial RNA Methyltransferases

Phylogenetic Reconstruction Shows Independent Evolutionary Origins of Mitochondrial Transcription Factors from an Ancient Family of RNA Methyltransferase Proteins

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