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The methylome is altered for plants in a high CO2 world: Insights into the response of a wild plant population to multigenerational exposure to elevated atmospheric [CO2]

The methylome is altered for plants in a high CO2 world: Insights into the response of a wild plant population to multigenerational exposure to elevated atmospheric [CO2]
The methylome is altered for plants in a high CO2 world: Insights into the response of a wild plant population to multigenerational exposure to elevated atmospheric [CO2]
Unravelling plant responses to rising atmospheric CO2 concentration ([CO2]) has largely focussed on plastic functional attributes to single generation [CO2] exposure. Quantifying the consequences of long‐term, decadal multigenerational exposure to elevated [CO2] and the genetic changes that may underpin evolutionary mechanisms with [CO2] as a driver remain largely unexplored. Here, we investigated both plastic and evolutionary plant responses to elevated [CO2] by applying multi‐omic technologies using populations of Plantago lanceolata L., grown in naturally high [CO2] for many generations in a CO2 spring. Seed from populations at the CO2 spring and an adjacent control site (ambient [CO2]) were grown in a common environment for one generation, and then offspring were grown in ambient or elevated [CO2] growth chambers. Low overall genetic differentiation between the CO2 spring and control site populations was found, with evidence of weak selection in exons. We identified evolutionary divergence in the DNA methylation profiles of populations derived from the spring relative to the control population, providing the first evidence that plant methylomes may respond to elevated [CO2] over multiple generations. In contrast, growth at elevated [CO2] for a single generation induced limited methylome remodelling (an order of magnitude fewer differential methylation events than observed between populations), although some of this appeared to be stably transgenerationally inherited. In all, 59 regions of the genome were identified where transcripts exhibiting differential expression (associated with single generation or long‐term natural exposure to elevated [CO2]) co‐located with sites of differential methylation or with single nucleotide polymorphisms exhibiting significant inter‐population divergence. This included genes in pathways known to respond to elevated [CO2], such as nitrogen use efficiency and stomatal patterning. This study provides the first indication that DNA methylation may contribute to plant adaptation to future atmospheric [CO2] and identifies several areas of the genome that are targets for future study.
1354-1013
Saban, Jasmine
a43e61ec-d1a7-4719-b0a3-4226c61d1f4e
Watson-Lazowski, Alex James
52ab3b08-daf3-4ff5-bd1e-a839dcf89705
Chapman, Mark
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Taylor, Gail
f3851db9-d37c-4c36-8663-e5c2cb03e171
Saban, Jasmine
a43e61ec-d1a7-4719-b0a3-4226c61d1f4e
Watson-Lazowski, Alex James
52ab3b08-daf3-4ff5-bd1e-a839dcf89705
Chapman, Mark
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Taylor, Gail
f3851db9-d37c-4c36-8663-e5c2cb03e171

Saban, Jasmine, Watson-Lazowski, Alex James, Chapman, Mark and Taylor, Gail (2020) The methylome is altered for plants in a high CO2 world: Insights into the response of a wild plant population to multigenerational exposure to elevated atmospheric [CO2]. Global Change Biology. (doi:10.1111/gcb.15249).

Record type: Article

Abstract

Unravelling plant responses to rising atmospheric CO2 concentration ([CO2]) has largely focussed on plastic functional attributes to single generation [CO2] exposure. Quantifying the consequences of long‐term, decadal multigenerational exposure to elevated [CO2] and the genetic changes that may underpin evolutionary mechanisms with [CO2] as a driver remain largely unexplored. Here, we investigated both plastic and evolutionary plant responses to elevated [CO2] by applying multi‐omic technologies using populations of Plantago lanceolata L., grown in naturally high [CO2] for many generations in a CO2 spring. Seed from populations at the CO2 spring and an adjacent control site (ambient [CO2]) were grown in a common environment for one generation, and then offspring were grown in ambient or elevated [CO2] growth chambers. Low overall genetic differentiation between the CO2 spring and control site populations was found, with evidence of weak selection in exons. We identified evolutionary divergence in the DNA methylation profiles of populations derived from the spring relative to the control population, providing the first evidence that plant methylomes may respond to elevated [CO2] over multiple generations. In contrast, growth at elevated [CO2] for a single generation induced limited methylome remodelling (an order of magnitude fewer differential methylation events than observed between populations), although some of this appeared to be stably transgenerationally inherited. In all, 59 regions of the genome were identified where transcripts exhibiting differential expression (associated with single generation or long‐term natural exposure to elevated [CO2]) co‐located with sites of differential methylation or with single nucleotide polymorphisms exhibiting significant inter‐population divergence. This included genes in pathways known to respond to elevated [CO2], such as nitrogen use efficiency and stomatal patterning. This study provides the first indication that DNA methylation may contribute to plant adaptation to future atmospheric [CO2] and identifies several areas of the genome that are targets for future study.

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Accepted/In Press date: 18 May 2020
Published date: 9 September 2020

Identifiers

Local EPrints ID: 443860
URI: http://eprints.soton.ac.uk/id/eprint/443860
ISSN: 1354-1013
PURE UUID: 278666b5-3ad4-42a8-a459-c5a9b257b929
ORCID for Mark Chapman: ORCID iD orcid.org/0000-0002-7151-723X
ORCID for Gail Taylor: ORCID iD orcid.org/0000-0001-8470-6390

Catalogue record

Date deposited: 15 Sep 2020 16:32
Last modified: 18 Feb 2021 17:21

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Contributors

Author: Jasmine Saban
Author: Alex James Watson-Lazowski
Author: Mark Chapman ORCID iD
Author: Gail Taylor ORCID iD

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