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...
Published in: | Frontiers in Marine Science |
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Main Authors: | , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | unknown |
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2022
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Online Access: | https://epic.awi.de/id/eprint/55820/ https://epic.awi.de/id/eprint/55820/1/Liesner_etal_2022_FMarS.pdf https://doi.org/10.3389/fmars.2022.838793 https://hdl.handle.net/10013/epic.30a1798f-4ad9-4a04-9f15-3a554869a492 https://hdl.handle.net/ |
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Open Polar |
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Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) |
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ftawi |
language |
unknown |
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 genes between the reciprocal crosses at 20.5°C indicate that female and male gametophytes may contribute differently to offspring traits. We consider potential inbreeding depression in the Spitsbergen selfing and quantify the better performance of both crosses using heterosis-related parameters. We discuss the potential and risks of outbreeding to produce more resilient crops for mariculture and marine forest restoration. |
format |
Article in Journal/Newspaper |
author |
Liesner, Daniel Pearson, Gareth A. Bartsch, Inka Rana, Shivani Harms, Lars Heinrich, Sandra Bischof, Kai Glöckner, Gernot Valentin, Klaus-Ulrich |
spellingShingle |
Liesner, Daniel Pearson, Gareth A. Bartsch, Inka Rana, Shivani Harms, Lars Heinrich, Sandra Bischof, Kai Glöckner, Gernot Valentin, Klaus-Ulrich Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics |
author_facet |
Liesner, Daniel Pearson, Gareth A. Bartsch, Inka Rana, Shivani Harms, Lars Heinrich, Sandra Bischof, Kai Glöckner, Gernot Valentin, Klaus-Ulrich |
author_sort |
Liesner, Daniel |
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 |
publishDate |
2022 |
url |
https://epic.awi.de/id/eprint/55820/ https://epic.awi.de/id/eprint/55820/1/Liesner_etal_2022_FMarS.pdf https://doi.org/10.3389/fmars.2022.838793 https://hdl.handle.net/10013/epic.30a1798f-4ad9-4a04-9f15-3a554869a492 https://hdl.handle.net/ |
geographic |
Arctic Helgoland |
geographic_facet |
Arctic Helgoland |
genre |
Arctic Spitsbergen |
genre_facet |
Arctic Spitsbergen |
op_source |
EPIC3Frontiers in Marine Science, 9, pp. 838793, ISSN: 2296-7745 |
op_relation |
https://epic.awi.de/id/eprint/55820/1/Liesner_etal_2022_FMarS.pdf https://hdl.handle.net/ Liesner, D. orcid:0000-0002-2125-9498 , Pearson, G. A. orcid:0000-0002-0768-464X , Bartsch, I. orcid:0000-0001-7609-2149 , Rana, S. , Harms, L. orcid:0000-0001-7620-0613 , Heinrich, S. , Bischof, K. , Glöckner, G. orcid:0000-0002-9061-1061 and Valentin, K. U. (2022) Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics , Frontiers in Marine Science, 9 , p. 838793 . doi:10.3389/fmars.2022.838793 <https://doi.org/10.3389/fmars.2022.838793> , hdl:10013/epic.30a1798f-4ad9-4a04-9f15-3a554869a492 |
op_rights |
info:eu-repo/semantics/openAccess |
op_doi |
https://doi.org/10.3389/fmars.2022.838793 |
container_title |
Frontiers in Marine Science |
container_volume |
9 |
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1766331244380946432 |
spelling |
ftawi:oai:epic.awi.de:55820 2023-05-15T14:59:06+02:00 Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics Liesner, Daniel Pearson, Gareth A. Bartsch, Inka Rana, Shivani Harms, Lars Heinrich, Sandra Bischof, Kai Glöckner, Gernot Valentin, Klaus-Ulrich 2022-03-10 application/pdf https://epic.awi.de/id/eprint/55820/ https://epic.awi.de/id/eprint/55820/1/Liesner_etal_2022_FMarS.pdf https://doi.org/10.3389/fmars.2022.838793 https://hdl.handle.net/10013/epic.30a1798f-4ad9-4a04-9f15-3a554869a492 https://hdl.handle.net/ unknown https://epic.awi.de/id/eprint/55820/1/Liesner_etal_2022_FMarS.pdf https://hdl.handle.net/ Liesner, D. orcid:0000-0002-2125-9498 , Pearson, G. A. orcid:0000-0002-0768-464X , Bartsch, I. orcid:0000-0001-7609-2149 , Rana, S. , Harms, L. orcid:0000-0001-7620-0613 , Heinrich, S. , Bischof, K. , Glöckner, G. orcid:0000-0002-9061-1061 and Valentin, K. U. (2022) Increased Heat Resilience of Intraspecific Outbred Compared to Inbred Lineages in the Kelp Laminaria digitata: Physiology and Transcriptomics , Frontiers in Marine Science, 9 , p. 838793 . doi:10.3389/fmars.2022.838793 <https://doi.org/10.3389/fmars.2022.838793> , hdl:10013/epic.30a1798f-4ad9-4a04-9f15-3a554869a492 info:eu-repo/semantics/openAccess EPIC3Frontiers in Marine Science, 9, pp. 838793, ISSN: 2296-7745 Article isiRev info:eu-repo/semantics/article 2022 ftawi https://doi.org/10.3389/fmars.2022.838793 2022-03-21T00:09:29Z 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 genes between the reciprocal crosses at 20.5°C indicate that female and male gametophytes may contribute differently to offspring traits. We consider potential inbreeding depression in the Spitsbergen selfing and quantify the better performance of both crosses using heterosis-related parameters. We discuss the potential and risks of outbreeding to produce more resilient crops for mariculture and marine forest restoration. Article in Journal/Newspaper Arctic Spitsbergen Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) Arctic Helgoland Frontiers in Marine Science 9 |