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Plant adaptation or acclimation to rising CO2? Insight from first multigenerational RNA-Seq transcriptome

Plant adaptation or acclimation to rising CO2? Insight from first multigenerational RNA-Seq transcriptome
Plant adaptation or acclimation to rising CO2? Insight from first multigenerational RNA-Seq transcriptome
Atmospheric carbon dioxide (CO2) directly determines the rate of plant photosynthesis and indirectly effects plant productivity and fitness and may therefore act as a selective pressure driving evolution, but evidence to support this contention is sparse. Using Plantago lanceolata L. seed collected from a naturally high CO2 spring and adjacent ambient CO2 control site, we investigated multigenerational response to future, elevated atmospheric CO2. Plants were grown in either ambient or elevated CO2 (700 ?mol mol?1), enabling for the first time, characterization of the functional and population genomics of plant acclimation and adaptation to elevated CO2. This revealed that spring and control plants differed significantly in phenotypic plasticity for traits underpinning fitness including above-ground biomass, leaf size, epidermal cell size and number and stomatal density and index. Gene expression responses to elevated CO2 (acclimation) were modest [33–131 genes differentially expressed (DE)], whilst those between control and spring plants (adaptation) were considerably larger (689–853 DE genes). In contrast, population genomic analysis showed that genetic differentiation between spring and control plants was close to zero, with no fixed differences, suggesting that plants are adapted to their native CO2 environment at the level of gene expression. An unusual phenotype of increased stomatal index in spring but not control plants in elevated CO2 correlated with altered expression of stomatal patterning genes between spring and control plants for three loci (YODA, CDKB1;1 and SCRM2) and between ambient and elevated CO2 for four loci (ER, YODA, MYB88 and BCA1). We propose that the two positive regulators of stomatal number (SCRM2) and CDKB1;1 when upregulated act as key controllers of stomatal adaptation to elevated CO2. Combined with significant transcriptome reprogramming of photosynthetic and dark respiration and enhanced growth in spring plants, we have identified the potential basis of plant adaptation to high CO2 likely to occur over coming decades.
1354-1013
3760-3773
Watson-Lazowski, Alexander
5028e97f-95f7-4871-a10c-5ce50cb1d1a7
Lin, Yun
3cbd9eaf-53ac-4bea-9f83-91b5870b52f4
Miglietta, Franco
efe1ee52-c4f4-475b-8386-3550508e2d59
Edwards, Richard J.
9d25e74f-dc0d-455a-832c-5f363d864c43
Chapman, Mark A.
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Taylor, Gail
Watson-Lazowski, Alexander
5028e97f-95f7-4871-a10c-5ce50cb1d1a7
Lin, Yun
3cbd9eaf-53ac-4bea-9f83-91b5870b52f4
Miglietta, Franco
efe1ee52-c4f4-475b-8386-3550508e2d59
Edwards, Richard J.
9d25e74f-dc0d-455a-832c-5f363d864c43
Chapman, Mark A.
8bac4a92-bfa7-4c3c-af29-9af852ef6383
Taylor, Gail

Watson-Lazowski, Alexander, Lin, Yun, Miglietta, Franco, Edwards, Richard J., Chapman, Mark A. and Taylor, Gail (2016) Plant adaptation or acclimation to rising CO2? Insight from first multigenerational RNA-Seq transcriptome. Global Change Biology, 22 (11), 3760-3773. (doi:10.1111/gcb.13322).

Record type: Article

Abstract

Atmospheric carbon dioxide (CO2) directly determines the rate of plant photosynthesis and indirectly effects plant productivity and fitness and may therefore act as a selective pressure driving evolution, but evidence to support this contention is sparse. Using Plantago lanceolata L. seed collected from a naturally high CO2 spring and adjacent ambient CO2 control site, we investigated multigenerational response to future, elevated atmospheric CO2. Plants were grown in either ambient or elevated CO2 (700 ?mol mol?1), enabling for the first time, characterization of the functional and population genomics of plant acclimation and adaptation to elevated CO2. This revealed that spring and control plants differed significantly in phenotypic plasticity for traits underpinning fitness including above-ground biomass, leaf size, epidermal cell size and number and stomatal density and index. Gene expression responses to elevated CO2 (acclimation) were modest [33–131 genes differentially expressed (DE)], whilst those between control and spring plants (adaptation) were considerably larger (689–853 DE genes). In contrast, population genomic analysis showed that genetic differentiation between spring and control plants was close to zero, with no fixed differences, suggesting that plants are adapted to their native CO2 environment at the level of gene expression. An unusual phenotype of increased stomatal index in spring but not control plants in elevated CO2 correlated with altered expression of stomatal patterning genes between spring and control plants for three loci (YODA, CDKB1;1 and SCRM2) and between ambient and elevated CO2 for four loci (ER, YODA, MYB88 and BCA1). We propose that the two positive regulators of stomatal number (SCRM2) and CDKB1;1 when upregulated act as key controllers of stomatal adaptation to elevated CO2. Combined with significant transcriptome reprogramming of photosynthetic and dark respiration and enhanced growth in spring plants, we have identified the potential basis of plant adaptation to high CO2 likely to occur over coming decades.

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Accepted/In Press date: 18 March 2016
e-pub ahead of print date: 19 August 2016
Published date: November 2016
Organisations: Centre for Biological Sciences

Identifiers

Local EPrints ID: 404634
URI: http://eprints.soton.ac.uk/id/eprint/404634
ISSN: 1354-1013
PURE UUID: 63fdca64-3bfd-4a22-b866-5e1cef097048
ORCID for Mark A. Chapman: ORCID iD orcid.org/0000-0002-7151-723X

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Date deposited: 13 Jan 2017 15:11
Last modified: 16 Mar 2024 04:14

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Contributors

Author: Alexander Watson-Lazowski
Author: Yun Lin
Author: Franco Miglietta
Author: Richard J. Edwards
Author: Mark A. Chapman ORCID iD
Author: Gail Taylor

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