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Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus

BACKGROUND: Rockweeds are among the most important foundation species of temperate rocky littoral shores. In the Baltic Sea, the rockweed Fucus vesiculosus is distributed along a decreasing salinity gradient from the North Atlantic entrance to the low-salinity regions in the north-eastern margins, t...

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Autores principales: Rugiu, Luca, Panova, Marina, Pereyra, Ricardo Tomás, Jormalainen, Veijo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6958763/
https://www.ncbi.nlm.nih.gov/pubmed/31931708
http://dx.doi.org/10.1186/s12864-020-6470-y
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author Rugiu, Luca
Panova, Marina
Pereyra, Ricardo Tomás
Jormalainen, Veijo
author_facet Rugiu, Luca
Panova, Marina
Pereyra, Ricardo Tomás
Jormalainen, Veijo
author_sort Rugiu, Luca
collection PubMed
description BACKGROUND: Rockweeds are among the most important foundation species of temperate rocky littoral shores. In the Baltic Sea, the rockweed Fucus vesiculosus is distributed along a decreasing salinity gradient from the North Atlantic entrance to the low-salinity regions in the north-eastern margins, thus, demonstrating a remarkable tolerance to hyposalinity. The underlying mechanisms for this tolerance are still poorly understood. Here, we exposed F. vesiculosus from two range-margin populations to the hyposaline (2.5 PSU - practical salinity unit) conditions that are projected to occur in the region by the end of this century as a result of climate change. We used transcriptome analysis (RNA-seq) to determine the gene expression patterns associated with hyposalinity acclimation, and examined the variation in these patterns between the sampled populations. RESULTS: Hyposalinity induced different responses in the two populations: in one, only 26 genes were differentially expressed between salinity treatments, while the other population demonstrated up- or downregulation in 3072 genes. In the latter population, the projected future hyposalinity induced an acute response in terms of antioxidant production. Genes associated with membrane composition and structure were also heavily involved, with the upregulation of fatty acid and actin production, and the downregulation of ion channels and alginate pathways. Changes in gene expression patterns clearly indicated an inhibition of the photosynthetic machinery, with a consequent downregulation of carbohydrate production. Simultaneously, energy consumption increased, as revealed by the upregulation of genes associated with respiration and ATP synthesis. Overall, the genes that demonstrated the largest increase in expression were ribosomal proteins involved in translation pathways. The fixation rate of SNP:s was higher within genes responding to hyposalinity than elsewhere in the transcriptome. CONCLUSIONS: The high fixation rate in the genes coding for salinity acclimation mechanisms implies strong selection for them. The among-population differentiation that we observed in the transcriptomic response to hyposalinity stress suggests that populations of F. vesiculosus may differ in their tolerance to future desalination, possibly as a result of local adaptation to salinity conditions within the Baltic Sea. These results emphasise the importance of considering interspecific genetic variation when evaluating the consequences of environmental change.
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spelling pubmed-69587632020-01-17 Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus Rugiu, Luca Panova, Marina Pereyra, Ricardo Tomás Jormalainen, Veijo BMC Genomics Research Article BACKGROUND: Rockweeds are among the most important foundation species of temperate rocky littoral shores. In the Baltic Sea, the rockweed Fucus vesiculosus is distributed along a decreasing salinity gradient from the North Atlantic entrance to the low-salinity regions in the north-eastern margins, thus, demonstrating a remarkable tolerance to hyposalinity. The underlying mechanisms for this tolerance are still poorly understood. Here, we exposed F. vesiculosus from two range-margin populations to the hyposaline (2.5 PSU - practical salinity unit) conditions that are projected to occur in the region by the end of this century as a result of climate change. We used transcriptome analysis (RNA-seq) to determine the gene expression patterns associated with hyposalinity acclimation, and examined the variation in these patterns between the sampled populations. RESULTS: Hyposalinity induced different responses in the two populations: in one, only 26 genes were differentially expressed between salinity treatments, while the other population demonstrated up- or downregulation in 3072 genes. In the latter population, the projected future hyposalinity induced an acute response in terms of antioxidant production. Genes associated with membrane composition and structure were also heavily involved, with the upregulation of fatty acid and actin production, and the downregulation of ion channels and alginate pathways. Changes in gene expression patterns clearly indicated an inhibition of the photosynthetic machinery, with a consequent downregulation of carbohydrate production. Simultaneously, energy consumption increased, as revealed by the upregulation of genes associated with respiration and ATP synthesis. Overall, the genes that demonstrated the largest increase in expression were ribosomal proteins involved in translation pathways. The fixation rate of SNP:s was higher within genes responding to hyposalinity than elsewhere in the transcriptome. CONCLUSIONS: The high fixation rate in the genes coding for salinity acclimation mechanisms implies strong selection for them. The among-population differentiation that we observed in the transcriptomic response to hyposalinity stress suggests that populations of F. vesiculosus may differ in their tolerance to future desalination, possibly as a result of local adaptation to salinity conditions within the Baltic Sea. These results emphasise the importance of considering interspecific genetic variation when evaluating the consequences of environmental change. BioMed Central 2020-01-13 /pmc/articles/PMC6958763/ /pubmed/31931708 http://dx.doi.org/10.1186/s12864-020-6470-y Text en © The Author(s). 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rugiu, Luca
Panova, Marina
Pereyra, Ricardo Tomás
Jormalainen, Veijo
Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title_full Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title_fullStr Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title_full_unstemmed Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title_short Gene regulatory response to hyposalinity in the brown seaweed Fucus vesiculosus
title_sort gene regulatory response to hyposalinity in the brown seaweed fucus vesiculosus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6958763/
https://www.ncbi.nlm.nih.gov/pubmed/31931708
http://dx.doi.org/10.1186/s12864-020-6470-y
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