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Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys

Bioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can chall...

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Autores principales: Radzvilavicius, Arunas L., Johnston, Iain G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650085/
https://www.ncbi.nlm.nih.gov/pubmed/36386853
http://dx.doi.org/10.3389/fgene.2022.974472
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author Radzvilavicius, Arunas L.
Johnston, Iain G.
author_facet Radzvilavicius, Arunas L.
Johnston, Iain G.
author_sort Radzvilavicius, Arunas L.
collection PubMed
description Bioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can challenge cellular bioenergetics, providing a penalty to the appearance and adaptation of new mutations. Here we show that organelle “bottlenecks,” mechanisms increasing cell-to-cell oDNA variability during development, can overcome this mixture penalty and facilitate the adaptation of beneficial mutations. We show that oDNA heteroplasmy and bottlenecks naturally emerge in evolutionary simulations subjected to fluctuating environments, demonstrating that this evolvability is itself evolvable. Usually thought of as a mechanism to clear damaging mutations, organelle bottlenecks therefore also resolve the tension between intracellular selection for pure cellular oDNA populations and the “bet-hedging” need for evolvability and adaptation to new environments. This general theory suggests a reason for the maintenance of organelle heteroplasmy in cells, and may explain some of the observed diversity in organelle maintenance and inheritance across taxa.
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spelling pubmed-96500852022-11-15 Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys Radzvilavicius, Arunas L. Johnston, Iain G. Front Genet Genetics Bioenergetic organelles—mitochondria and plastids—retain their own genomes (mtDNA and ptDNA), and these organelle DNA (oDNA) molecules are vital for eukaryotic life. Like all genomes, oDNA must be able to evolve to suit new environmental challenges. However, mixed oDNA populations in cells can challenge cellular bioenergetics, providing a penalty to the appearance and adaptation of new mutations. Here we show that organelle “bottlenecks,” mechanisms increasing cell-to-cell oDNA variability during development, can overcome this mixture penalty and facilitate the adaptation of beneficial mutations. We show that oDNA heteroplasmy and bottlenecks naturally emerge in evolutionary simulations subjected to fluctuating environments, demonstrating that this evolvability is itself evolvable. Usually thought of as a mechanism to clear damaging mutations, organelle bottlenecks therefore also resolve the tension between intracellular selection for pure cellular oDNA populations and the “bet-hedging” need for evolvability and adaptation to new environments. This general theory suggests a reason for the maintenance of organelle heteroplasmy in cells, and may explain some of the observed diversity in organelle maintenance and inheritance across taxa. Frontiers Media S.A. 2022-10-28 /pmc/articles/PMC9650085/ /pubmed/36386853 http://dx.doi.org/10.3389/fgene.2022.974472 Text en Copyright © 2022 Radzvilavicius and Johnston. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Radzvilavicius, Arunas L.
Johnston, Iain G.
Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title_full Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title_fullStr Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title_full_unstemmed Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title_short Organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
title_sort organelle bottlenecks facilitate evolvability by traversing heteroplasmic fitness valleys
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650085/
https://www.ncbi.nlm.nih.gov/pubmed/36386853
http://dx.doi.org/10.3389/fgene.2022.974472
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