Avoiding organelle mutational meltdown across eukaryotes with or without a germline bottleneck
Autor: | Konstantinos Giannakis, David M. Edwards, Robert C. Glastad, Iain G. Johnston, Ellen C. Røyrvik, Joanna M. Chustecki, Arunas L. Radzvilavicius |
---|---|
Jazyk: | angličtina |
Rok vydání: | 2021 |
Předmět: |
0106 biological sciences
0301 basic medicine Heredity Arabidopsis Gene Expression 01 natural sciences Mitochondrial Dynamics Biochemistry Germline Negative selection Mice Mutation Rate Cell Cycle and Cell Division Biology (General) Energy-Producing Organelles Organelle Biogenesis General Neuroscience Eukaryota Gene Expression Regulation Developmental Heteroplasmy Mitochondrial DNA Mitochondria Nucleic acids Cell Processes Drosophila Cellular Structures and Organelles General Agricultural and Biological Sciences Research Article QH301-705.5 Genetic Speciation Forms of DNA DNA recombination Gene Conversion Biology Bioenergetics DNA Mitochondrial General Biochemistry Genetics and Molecular Biology 03 medical and health sciences Genetic model Genetics Animals Humans Gene conversion Plastid Germ-Line Mutation Organelles General Immunology and Microbiology Models Genetic Biology and life sciences Organisms DNA Cell Biology 030104 developmental biology Germ Cells Mutational meltdown Evolutionary biology Mutagenesis Mutation 010606 plant biology & botany |
Zdroj: | e3001153 PLoS Biology PLoS Biology, Vol 19, Iss 4, p e3001153 (2021) |
Popis: | Mitochondrial DNA (mtDNA) and plastid DNA (ptDNA) encode vital bioenergetic apparatus, and mutations in these organelle DNA (oDNA) molecules can be devastating. In the germline of several animals, a genetic “bottleneck” increases cell-to-cell variance in mtDNA heteroplasmy, allowing purifying selection to act to maintain low proportions of mutant mtDNA. However, most eukaryotes do not sequester a germline early in development, and even the animal bottleneck remains poorly understood. How then do eukaryotic organelles avoid Muller’s ratchet—the gradual buildup of deleterious oDNA mutations? Here, we construct a comprehensive and predictive genetic model, quantitatively describing how different mechanisms segregate and decrease oDNA damage across eukaryotes. We apply this comprehensive theory to characterise the animal bottleneck with recent single-cell observations in diverse mouse models. Further, we show that gene conversion is a particularly powerful mechanism to increase beneficial cell-to-cell variance without depleting oDNA copy number, explaining the benefit of observed oDNA recombination in diverse organisms which do not sequester animal-like germlines (for example, sponges, corals, fungi, and plants). Genomic, transcriptomic, and structural datasets across eukaryotes support this mechanism for generating beneficial variance without a germline bottleneck. This framework explains puzzling oDNA differences across taxa, suggesting how Muller’s ratchet is avoided in different eukaryotes. A comprehensive model for mitochondrial and plasmid DNA segregation, supported by with genomic, transcriptomic, and single-cell data, shows how the attritional effects of Muller’s ratchet can be avoided in the organelles of diverse eukaryotes. |
Databáze: | OpenAIRE |
Externí odkaz: |