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Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial...

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Autores principales: Pogoda, Cloe S., Keepers, Kyle G., Nadiadi, Arif Y., Bailey, Dustin W., Lendemer, James C., Tripp, Erin A., Kane, Nolan C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6467859/
https://www.ncbi.nlm.nih.gov/pubmed/31016002
http://dx.doi.org/10.1002/ece3.5056
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author Pogoda, Cloe S.
Keepers, Kyle G.
Nadiadi, Arif Y.
Bailey, Dustin W.
Lendemer, James C.
Tripp, Erin A.
Kane, Nolan C.
author_facet Pogoda, Cloe S.
Keepers, Kyle G.
Nadiadi, Arif Y.
Bailey, Dustin W.
Lendemer, James C.
Tripp, Erin A.
Kane, Nolan C.
author_sort Pogoda, Cloe S.
collection PubMed
description Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial genomes. Here, we examine patterns of mitochondrial evolution specifically looking at intron size, number, and position across 58 species from 21 genera of lichenized Ascomycete fungi, representing a broad range of fungal diversity and niches. Our results show that the cox1gene always contained the highest number of introns out of all the mitochondrial protein‐coding genes, that high intron sequence similarity (>90%) can be maintained between different genera, and that lichens have undergone at least two instances of complete, genome‐wide intron loss consistent with evidence for genome streamlining via loss of parasitic, noncoding DNA, in Phlyctis boliviensisand Graphis lineola. Notably, however, lichenized fungi have not only undergone intron loss but in some instances have expanded considerably in size due to intron proliferation (e.g., Alectoria fallacina and Parmotrema neotropicum), even between closely related sister species (e.g., Cladonia). These results shed light on the highly dynamic mitochondrial evolution that is occurring in lichens and suggest that these obligate symbiotic organisms are in some cases undergoing recent, broad‐scale genome streamlining via loss of protein‐coding genes as well as noncoding, parasitic DNA elements.
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spelling pubmed-64678592019-04-23 Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria Pogoda, Cloe S. Keepers, Kyle G. Nadiadi, Arif Y. Bailey, Dustin W. Lendemer, James C. Tripp, Erin A. Kane, Nolan C. Ecol Evol Original Research Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial genomes. Here, we examine patterns of mitochondrial evolution specifically looking at intron size, number, and position across 58 species from 21 genera of lichenized Ascomycete fungi, representing a broad range of fungal diversity and niches. Our results show that the cox1gene always contained the highest number of introns out of all the mitochondrial protein‐coding genes, that high intron sequence similarity (>90%) can be maintained between different genera, and that lichens have undergone at least two instances of complete, genome‐wide intron loss consistent with evidence for genome streamlining via loss of parasitic, noncoding DNA, in Phlyctis boliviensisand Graphis lineola. Notably, however, lichenized fungi have not only undergone intron loss but in some instances have expanded considerably in size due to intron proliferation (e.g., Alectoria fallacina and Parmotrema neotropicum), even between closely related sister species (e.g., Cladonia). These results shed light on the highly dynamic mitochondrial evolution that is occurring in lichens and suggest that these obligate symbiotic organisms are in some cases undergoing recent, broad‐scale genome streamlining via loss of protein‐coding genes as well as noncoding, parasitic DNA elements. John Wiley and Sons Inc. 2019-03-21 /pmc/articles/PMC6467859/ /pubmed/31016002 http://dx.doi.org/10.1002/ece3.5056 Text en © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Pogoda, Cloe S.
Keepers, Kyle G.
Nadiadi, Arif Y.
Bailey, Dustin W.
Lendemer, James C.
Tripp, Erin A.
Kane, Nolan C.
Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title_full Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title_fullStr Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title_full_unstemmed Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title_short Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
title_sort genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6467859/
https://www.ncbi.nlm.nih.gov/pubmed/31016002
http://dx.doi.org/10.1002/ece3.5056
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