Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics

Marine forests and kelps as their foundation species are threatened by ocean warming especially at the warm distributional edges. Previously identified genetic divergence and ecotypic differentiation within kelp species may allow to produce more resilient lineages by intraspecific outbreeding among...

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Published in:Frontiers in Marine Science
Main Authors: Daniel Liesner, Gareth A. Pearson, Inka Bartsch, Shivani Rana, Lars Harms, Sandra Heinrich, Kai Bischof, Gernot Glöckner, Klaus Valentin
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2022
Subjects:
Q
Online Access:https://doi.org/10.3389/fmars.2022.838793
https://doaj.org/article/49dd08c2b7ca4804875f6a706b63695c
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spelling ftdoajarticles:oai:doaj.org/article:49dd08c2b7ca4804875f6a706b63695c 2023-05-15T14:56:48+02:00 Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics Daniel Liesner Gareth A. Pearson Inka Bartsch Shivani Rana Lars Harms Sandra Heinrich Kai Bischof Gernot Glöckner Klaus Valentin 2022-03-01T00:00:00Z https://doi.org/10.3389/fmars.2022.838793 https://doaj.org/article/49dd08c2b7ca4804875f6a706b63695c EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fmars.2022.838793/full https://doaj.org/toc/2296-7745 2296-7745 doi:10.3389/fmars.2022.838793 https://doaj.org/article/49dd08c2b7ca4804875f6a706b63695c Frontiers in Marine Science, Vol 9 (2022) temperature performance marine forest genotype inbreeding outbreeding gene expression Science Q General. Including nature conservation geographical distribution QH1-199.5 article 2022 ftdoajarticles https://doi.org/10.3389/fmars.2022.838793 2022-12-31T12:45:20Z Marine forests and kelps as their foundation species are threatened by ocean warming especially at the warm distributional edges. Previously identified genetic divergence and ecotypic differentiation within kelp species may allow to produce more resilient lineages by intraspecific outbreeding among populations. In a mechanistic investigation of heat stress, heterosis (hybrid vigour), and underlying gene expression patterns, we assessed the thermal performance of inbred (selfings) and outbred (reciprocal crosses) sporophytes of the N-Atlantic kelp Laminaria digitata among clonal isolates from two divergent populations; one from the temperate North Sea (Helgoland) and one from the Arctic (Spitsbergen). First, we investigated the upper thermal tolerance of microscopic sporophytes in a 14-day experiment applying sublethal to lethal 20–23°C. The upper survival temperature of microscopic sporophytes was lower for the inbred Arctic selfing (21°C) than for the temperate selfing and the reciprocal crosses (22°C). Only in the temperate selfing, 4.5% of sporophytes survived 23°C. We then subjected 4–7 cm long sporophytes to a control temperature (10°C), moderate (19°C) and sublethal to lethal heat stress (20.5°C) for 18 days to assess gene expression in addition to physiological parameters. Growth and optimum quantum yield decreased similarly in the reciprocal crosses and the temperate selfing at 19 and 20.5°C, while inbred Arctic sporophytes died within seven days at both 19 and 20.5°C. In response to 20.5°C, 252 genes were constitutively regulated across all surviving lineages, which we use to describe metabolic regulation patterns in response to heat stress in kelp. At sublethal 20.5°C, ca. 150 genes were differentially expressed by either crossed lineage in comparison to the temperate selfing, indicating that they maintained a growth response similar to the temperate selfing with differential metabolic regulation during sublethal heat stress. Subtle differences in physiology and the differential expression of nine ... Article in Journal/Newspaper Arctic Spitsbergen Directory of Open Access Journals: DOAJ Articles Arctic Helgoland Frontiers in Marine Science 9
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic temperature performance
marine forest
genotype
inbreeding
outbreeding
gene expression
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
spellingShingle temperature performance
marine forest
genotype
inbreeding
outbreeding
gene expression
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
Daniel Liesner
Gareth A. Pearson
Inka Bartsch
Shivani Rana
Lars Harms
Sandra Heinrich
Kai Bischof
Gernot Glöckner
Klaus Valentin
Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
topic_facet temperature performance
marine forest
genotype
inbreeding
outbreeding
gene expression
Science
Q
General. Including nature conservation
geographical distribution
QH1-199.5
description Marine forests and kelps as their foundation species are threatened by ocean warming especially at the warm distributional edges. Previously identified genetic divergence and ecotypic differentiation within kelp species may allow to produce more resilient lineages by intraspecific outbreeding among populations. In a mechanistic investigation of heat stress, heterosis (hybrid vigour), and underlying gene expression patterns, we assessed the thermal performance of inbred (selfings) and outbred (reciprocal crosses) sporophytes of the N-Atlantic kelp Laminaria digitata among clonal isolates from two divergent populations; one from the temperate North Sea (Helgoland) and one from the Arctic (Spitsbergen). First, we investigated the upper thermal tolerance of microscopic sporophytes in a 14-day experiment applying sublethal to lethal 20–23°C. The upper survival temperature of microscopic sporophytes was lower for the inbred Arctic selfing (21°C) than for the temperate selfing and the reciprocal crosses (22°C). Only in the temperate selfing, 4.5% of sporophytes survived 23°C. We then subjected 4–7 cm long sporophytes to a control temperature (10°C), moderate (19°C) and sublethal to lethal heat stress (20.5°C) for 18 days to assess gene expression in addition to physiological parameters. Growth and optimum quantum yield decreased similarly in the reciprocal crosses and the temperate selfing at 19 and 20.5°C, while inbred Arctic sporophytes died within seven days at both 19 and 20.5°C. In response to 20.5°C, 252 genes were constitutively regulated across all surviving lineages, which we use to describe metabolic regulation patterns in response to heat stress in kelp. At sublethal 20.5°C, ca. 150 genes were differentially expressed by either crossed lineage in comparison to the temperate selfing, indicating that they maintained a growth response similar to the temperate selfing with differential metabolic regulation during sublethal heat stress. Subtle differences in physiology and the differential expression of nine ...
format Article in Journal/Newspaper
author Daniel Liesner
Gareth A. Pearson
Inka Bartsch
Shivani Rana
Lars Harms
Sandra Heinrich
Kai Bischof
Gernot Glöckner
Klaus Valentin
author_facet Daniel Liesner
Gareth A. Pearson
Inka Bartsch
Shivani Rana
Lars Harms
Sandra Heinrich
Kai Bischof
Gernot Glöckner
Klaus Valentin
author_sort Daniel Liesner
title Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
title_short Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
title_full Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
title_fullStr Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
title_full_unstemmed Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics
title_sort increased heat resilience of intraspecific outbred compared to inbred lineages in the kelp laminaria digitata: physiology and transcriptomics
publisher Frontiers Media S.A.
publishDate 2022
url https://doi.org/10.3389/fmars.2022.838793
https://doaj.org/article/49dd08c2b7ca4804875f6a706b63695c
geographic Arctic
Helgoland
geographic_facet Arctic
Helgoland
genre Arctic
Spitsbergen
genre_facet Arctic
Spitsbergen
op_source Frontiers in Marine Science, Vol 9 (2022)
op_relation https://www.frontiersin.org/articles/10.3389/fmars.2022.838793/full
https://doaj.org/toc/2296-7745
2296-7745
doi:10.3389/fmars.2022.838793
https://doaj.org/article/49dd08c2b7ca4804875f6a706b63695c
op_doi https://doi.org/10.3389/fmars.2022.838793
container_title Frontiers in Marine Science
container_volume 9
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