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Soil salinization accelerates microbiome stabilization in iterative selections for plant performance

Soil salinization accelerates microbiome stabilization in iterative selections for plant performance
Soil salinization accelerates microbiome stabilization in iterative selections for plant performance

Climate change-related soil salinization increases plant stress and decreases productivity. Soil microorganisms are thought to reduce salt stress through multiple mechanisms, so diverse assemblages could improve plant growth under such conditions. Previous studies have shown that microbiome selection can promote desired plant phenotypes, but with high variability. We hypothesized that microbiome selection would be more consistent in saline soils by increasing potential benefits to the plants. In both salt-amended and untreated soils, we transferred forward Brassica rapa root microbiomes (from high-biomass or randomly selected pots) across six planting generations while assessing bacterial (16S rRNA) and fungal (ITS) composition in detail. Uniquely, we included an add-back control (re-adding initial frozen soil microbiome) as a within-generation reference for microbiome and plant phenotype selection. We observed inconsistent effects of microbiome selection on plant biomass across generations, but microbial composition consistently diverged from the add-back control. Although salt amendment strongly impacted microbial composition, it did not increase the predictability of microbiome effects on plant phenotype, but it did increase the rate at which microbiome selection plateaued. These data highlight a disconnect in the trajectories of microbiomes and plant phenotypes during microbiome selection, emphasizing the role of standard controls to explain microbiome selection outcomes.

artificial selection, microbiome breeding, phenotype selection, rhizosphere, root microbiome, soil salinity
0028-646X
2101-2110
King, William L.
0bd4328a-34ba-4b9a-bf4e-1442c18c43fc
Kaminsky, Laura M.
cdd71929-138a-4719-875f-972240a3f79e
Gannett, Maria
0cc08685-8775-4c2d-bed9-16d50bf0cccd
Thompson, Grant L.
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Kao-Kniffin, Jenny
a2d648ed-576c-45e7-ab2f-348b3366aabd
Bell, Terrence H.
29863b8c-a89c-4077-b22d-62052cfb7225
King, William L.
0bd4328a-34ba-4b9a-bf4e-1442c18c43fc
Kaminsky, Laura M.
cdd71929-138a-4719-875f-972240a3f79e
Gannett, Maria
0cc08685-8775-4c2d-bed9-16d50bf0cccd
Thompson, Grant L.
9abd966b-6495-47eb-9982-8127aa687640
Kao-Kniffin, Jenny
a2d648ed-576c-45e7-ab2f-348b3366aabd
Bell, Terrence H.
29863b8c-a89c-4077-b22d-62052cfb7225

King, William L., Kaminsky, Laura M., Gannett, Maria, Thompson, Grant L., Kao-Kniffin, Jenny and Bell, Terrence H. (2022) Soil salinization accelerates microbiome stabilization in iterative selections for plant performance. New Phytologist, 234 (6), 2101-2110. (doi:10.1111/nph.17774).

Record type: Article

Abstract

Climate change-related soil salinization increases plant stress and decreases productivity. Soil microorganisms are thought to reduce salt stress through multiple mechanisms, so diverse assemblages could improve plant growth under such conditions. Previous studies have shown that microbiome selection can promote desired plant phenotypes, but with high variability. We hypothesized that microbiome selection would be more consistent in saline soils by increasing potential benefits to the plants. In both salt-amended and untreated soils, we transferred forward Brassica rapa root microbiomes (from high-biomass or randomly selected pots) across six planting generations while assessing bacterial (16S rRNA) and fungal (ITS) composition in detail. Uniquely, we included an add-back control (re-adding initial frozen soil microbiome) as a within-generation reference for microbiome and plant phenotype selection. We observed inconsistent effects of microbiome selection on plant biomass across generations, but microbial composition consistently diverged from the add-back control. Although salt amendment strongly impacted microbial composition, it did not increase the predictability of microbiome effects on plant phenotype, but it did increase the rate at which microbiome selection plateaued. These data highlight a disconnect in the trajectories of microbiomes and plant phenotypes during microbiome selection, emphasizing the role of standard controls to explain microbiome selection outcomes.

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More information

Published date: 2022
Additional Information: Funding Information: Work by THB was supported by a postdoctoral fellowship from the Atkinson Center for a Sustainable Future and by the USDA National Institute of Food and Hatch Appropriations under Project #PEN04651 and Accession no. 1016233. Analysis and writing were partly supported by USDA ORG Project PENW-2019-03513. We thank Mia Howard, Sarah Ditton, Marcel Ramos, Olivia McCandless, Ololade Olawade, Emaleigh Perry, Liang Cheng, and LiPing Wei for technical assistance. Lynn Johnson provided helpful advice on the experimental design. We also greatly thank the Weill Hall Growth Facility staff for their assistance with plant maintenance, particularly Janet Myrick, Nick Van Eck, and Scott Anthony. This work was also supported by an Agriculture and Food Research Initiative Grant (2016-67013-24414) from the United States Department of Agriculture National Institute of Food and Agriculture. The authors declare no conflicts of interest. Funding Information: Work by THB was supported by a postdoctoral fellowship from the Atkinson Center for a Sustainable Future and by the USDA National Institute of Food and Hatch Appropriations under Project #PEN04651 and Accession no. 1016233. Analysis and writing were partly supported by USDA ORG Project PENW‐2019‐03513. We thank Mia Howard, Sarah Ditton, Marcel Ramos, Olivia McCandless, Ololade Olawade, Emaleigh Perry, Liang Cheng, and LiPing Wei for technical assistance. Lynn Johnson provided helpful advice on the experimental design. We also greatly thank the Weill Hall Growth Facility staff for their assistance with plant maintenance, particularly Janet Myrick, Nick Van Eck, and Scott Anthony. This work was also supported by an Agriculture and Food Research Initiative Grant (2016‐67013‐24414) from the United States Department of Agriculture National Institute of Food and Agriculture. The authors declare no conflicts of interest. Publisher Copyright: © 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
Keywords: artificial selection, microbiome breeding, phenotype selection, rhizosphere, root microbiome, soil salinity

Identifiers

Local EPrints ID: 486652
URI: http://eprints.soton.ac.uk/id/eprint/486652
ISSN: 0028-646X
PURE UUID: 34b7c4c0-d67d-4684-8729-4d0b80c77c0a
ORCID for William L. King: ORCID iD orcid.org/0000-0001-7272-8242

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Date deposited: 30 Jan 2024 17:56
Last modified: 18 Mar 2024 04:18

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Contributors

Author: William L. King ORCID iD
Author: Laura M. Kaminsky
Author: Maria Gannett
Author: Grant L. Thompson
Author: Jenny Kao-Kniffin
Author: Terrence H. Bell

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