Landscape of submitochondrial protein distribution

Vögtle, F.-Nora; Burkhart, Julia M.; Gonczarowska-Jorge, Humberto; Küçükköse, Cansu; Taşkin, Aslı Aras; Kopczynski, Dominik; Ahrends, Robert; Mossmann, Dirk; Sickmann, Albert; Zahedi, René P.; Meisinger, Chris

doi:10.1038/s41467-017-00359-0

Cited by 147 publications

(142 citation statements)

References 59 publications

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“…Initial experiments were conducted by performing parallel tagging and purification with MM‐APEX2 and cytosolic APEX2, or APEX2‐Htb1 and cytosolic APEX2, respectively. For each pair, the MS data revealed a high enrichment of proteins that are in proximity of the respective APEX2 fusion: biotinylation by MM‐APEX2 led to the purification of at least 80 mitochondrial matrix proteins and inner mitochondrial membrane proteins exposed to the matrix side (based on the assignment by , see below). All these proteins were absent in the eluate obtained after cytosolic APEX2 PL (Table S1).…”

Section: Resultsmentioning

confidence: 99%

APEX2‐mediated proximity labeling resolves protein networks in Saccharomyces cerevisiae cells

et al. 2019

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Enzyme‐catalyzed proximity labeling (PL) with the engineered ascorbate peroxidase APEX2 is a novel approach to map organelle compartmentalization and protein networks in living cells. Current procedures developed for mammalian cells do not allow delivery of the cosubstrate, biotin‐phenol, into living yeast cells. Here, we present a new method based on semipermeabilized yeast cells. Combined with stable isotope labeling by amino acids in cell culture (SILAC), we demonstrate proteomic mapping of a membrane‐enclosed and a semiopen compartment, the mitochondrial matrix and the nucleus. APEX2 PL revealed nuclear proteins that were previously not identified by conventional techniques. One of these, the Yer156C protein, is highly conserved but of unknown function. Its human ortholog, melanocyte proliferating gene 1, is linked to developmental processes and dermatological diseases. A first characterization of the Yer156C neighborhood reveals an array of proteins linked to proteostasis and RNA binding. Thus, our approach establishes APEX2 PL as another powerful tool that complements the methods palette for the model system yeast.

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Section: Resultsmentioning

confidence: 99%

APEX2‐mediated proximity labeling resolves protein networks in Saccharomyces cerevisiae cells

et al. 2019

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“…In addition to mitochondria-encoded genes, approximately 1,000 nuclear genes function in the mitochondria, many of which are involved in expression and regulation of mitochondrial genes and formation of the multi-subunit cytochrome b and c complexes (Vögtle et al 2017). Among Saccharomyces species, multiple cyto-nuclear incompatibilities have been shown to contribute to reproductive isolation.…”

Section: Cyto-nuclear Interactions In Saccharomyces Evolutionmentioning

confidence: 99%

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Peris

et al. 2018

Preprint

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Over time, species evolve substantial phenotype differences. Yet, genetic analysis of these traits is limited by reproductive barriers to those phenotypes that distinguish closely related species. Here, we conduct a genome-wide non-complementation screen to identify genes that contribute to a major difference in thermal growth profile between two Saccharomyces species. S. cerevisiae is capable of growing at temperatures exceeding 40C, whereas S. uvarum cannot grow above 33C but outperforms S. cerevisiae at 4C. The screen revealed only a single nuclear-encoded gene with a modest contribution to heat tolerance, but a large effect of the species' mitochondrial DNA (mitotype). Furthermore, we found that, while the S. cerevisiae mitotype confers heat tolerance, the S. uvarum mitotype confers cold tolerance. Recombinant mitotypes indicate multiple genes contribute to thermal divergence. Mitochondrial allele replacements showed that divergence in the coding sequence of COX1 has a moderate effect on both heat and cold tolerance, but it does not explain the entire difference between the two mitochondrial genomes. Our results highlight a polygenic architecture for interspecific phenotypic divergence and point to the mitochondrial genome as an evolutionary hotspot for not only reproductive incompatibilities, but also thermal divergence in yeast.

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“…They are also involved in cell ageing and apoptosis. This functional diversity is almost entirely dependent on the products of nuclear genes whose total number constitutes a significant part of the eukaryotic proteomes (Vögtle et al, ). Yet in nearly all eukaryotic organisms, mitochondria also harbour a quantitatively minimal amount of genetic information (Burger, Gray, & Lang, ) whose mutational alteration may result in drastic phenotypic changes such as the mitochondrially inherited diseases in human (Vafai & Mootha, ) or lethality.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial genetics revisited

Dujon

2020

Yeast

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Mitochondrial genetics started decades ago with the discovery of yeast mutants that ignored the Mendelian rules of inheritance. Today, the many known DNA sequences of this second eukaryotic genome illustrate its eccentricity in terms of informational content and functional organisation, suggesting a yet incomplete understanding of its evolution. The hereditary transmission of mitochondrial alleles relies on complex mixes of molecular and cellular mechanisms in which recombination and limited sampling, two sources of rapid genetic changes, play central roles. It is also under the influence of invasive genetic elements whose inconstant distribution in mitochondrial genomes suggests rapid turnovers in evolving populations. This susceptibility to changes contrasts with the development of specific functional interactions between the mitochondrial and nuclear genetic compartments, a trend that is prone to limit the genetic exchanges between distinct lineages. It is perhaps this opposition and the discordant inheritance between mitochondrial and nuclear genomes that best explain the maintenance of a second genome and a second independent protein synthesising machinery in eukaryotic cells.

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Landscape of submitochondrial protein distribution

Cited by 147 publications

References 59 publications

APEX2‐mediated proximity labeling resolves protein networks in Saccharomyces cerevisiae cells

APEX2‐mediated proximity labeling resolves protein networks in Saccharomyces cerevisiae cells

Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Mitochondrial genetics revisited

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