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Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi

INTRODUCTION: Intraspecific genomic variability affects a species’ adaptive potential toward climatic conditions. Variation in gene content across populations and environments may point at genomic adaptations to specific environments. The lichen symbiosis, a stable association of fungal and photobio...

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Autores principales: Merges, Dominik, Dal Grande, Francesco, Valim, Henrique, Singh, Garima, Schmitt, Imke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10073550/
https://www.ncbi.nlm.nih.gov/pubmed/37032854
http://dx.doi.org/10.3389/fmicb.2023.1097787
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author Merges, Dominik
Dal Grande, Francesco
Valim, Henrique
Singh, Garima
Schmitt, Imke
author_facet Merges, Dominik
Dal Grande, Francesco
Valim, Henrique
Singh, Garima
Schmitt, Imke
author_sort Merges, Dominik
collection PubMed
description INTRODUCTION: Intraspecific genomic variability affects a species’ adaptive potential toward climatic conditions. Variation in gene content across populations and environments may point at genomic adaptations to specific environments. The lichen symbiosis, a stable association of fungal and photobiont partners, offers an excellent system to study environmentally driven gene content variation. Many of these species have remarkable environmental tolerances, and often form populations across different climate zones. Here, we combine comparative and population genomics to assess the presence and absence of genes in high and low elevation genomes of two lichenized fungi of the genus Umbilicaria. METHODS: The two species have non-overlapping ranges, but occupy similar climatic niches in North America (U. phaea) and Europe (U. pustulata): high elevation populations are located in the cold temperate zone and low elevation populations in the Mediterranean zone. We assessed gene content variation along replicated elevation gradients in each of the two species, based on a total of 2050 individuals across 26 populations. Specifically, we assessed shared orthologs across species within the same climate zone, and tracked, which genes increase or decrease in abundance within populations along elevation. RESULTS: In total, we found 16 orthogroups with shared orthologous genes in genomes at low elevation and 13 at high elevation. Coverage analysis revealed one ortholog that is exclusive to genomes at low elevation. Conserved domain search revealed domains common to the protein kinase superfamily. We traced the discovered ortholog in populations along five replicated elevation gradients on both continents and found that the number of this protein kinase gene linearly declined in abundance with increasing elevation, and was absent in the highest populations. DISCUSSION: We consider the parallel loss of an ortholog in two species and in two geographic settings a rare find, and a step forward in understanding the genomic underpinnings of climatic tolerances in lichenized fungi. In addition, the tracking of gene content variation provides a widely applicable framework for retrieving biogeographical determinants of gene presence/absence patterns. Our work provides insights into gene content variation of lichenized fungi in relation to climatic gradients, suggesting a new research direction with implications for understanding evolutionary trajectories of complex symbioses in relation to climatic change.
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spelling pubmed-100735502023-04-06 Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi Merges, Dominik Dal Grande, Francesco Valim, Henrique Singh, Garima Schmitt, Imke Front Microbiol Microbiology INTRODUCTION: Intraspecific genomic variability affects a species’ adaptive potential toward climatic conditions. Variation in gene content across populations and environments may point at genomic adaptations to specific environments. The lichen symbiosis, a stable association of fungal and photobiont partners, offers an excellent system to study environmentally driven gene content variation. Many of these species have remarkable environmental tolerances, and often form populations across different climate zones. Here, we combine comparative and population genomics to assess the presence and absence of genes in high and low elevation genomes of two lichenized fungi of the genus Umbilicaria. METHODS: The two species have non-overlapping ranges, but occupy similar climatic niches in North America (U. phaea) and Europe (U. pustulata): high elevation populations are located in the cold temperate zone and low elevation populations in the Mediterranean zone. We assessed gene content variation along replicated elevation gradients in each of the two species, based on a total of 2050 individuals across 26 populations. Specifically, we assessed shared orthologs across species within the same climate zone, and tracked, which genes increase or decrease in abundance within populations along elevation. RESULTS: In total, we found 16 orthogroups with shared orthologous genes in genomes at low elevation and 13 at high elevation. Coverage analysis revealed one ortholog that is exclusive to genomes at low elevation. Conserved domain search revealed domains common to the protein kinase superfamily. We traced the discovered ortholog in populations along five replicated elevation gradients on both continents and found that the number of this protein kinase gene linearly declined in abundance with increasing elevation, and was absent in the highest populations. DISCUSSION: We consider the parallel loss of an ortholog in two species and in two geographic settings a rare find, and a step forward in understanding the genomic underpinnings of climatic tolerances in lichenized fungi. In addition, the tracking of gene content variation provides a widely applicable framework for retrieving biogeographical determinants of gene presence/absence patterns. Our work provides insights into gene content variation of lichenized fungi in relation to climatic gradients, suggesting a new research direction with implications for understanding evolutionary trajectories of complex symbioses in relation to climatic change. Frontiers Media S.A. 2023-03-22 /pmc/articles/PMC10073550/ /pubmed/37032854 http://dx.doi.org/10.3389/fmicb.2023.1097787 Text en Copyright © 2023 Merges, Dal Grande, Valim, Singh and Schmitt. 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 Microbiology
Merges, Dominik
Dal Grande, Francesco
Valim, Henrique
Singh, Garima
Schmitt, Imke
Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title_full Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title_fullStr Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title_full_unstemmed Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title_short Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi
title_sort gene abundance linked to climate zone: parallel evolution of gene content along elevation gradients in lichenized fungi
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10073550/
https://www.ncbi.nlm.nih.gov/pubmed/37032854
http://dx.doi.org/10.3389/fmicb.2023.1097787
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