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