Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression

Foliar fungal endophytes are known to alter plant physiology but the mechanisms by which they do so remain poorly understood. We focused on how plant gene expression was altered by six fungal strains that generated “water-saver” and “water-spender” drought physiologies in a C4 grass, Panicum hallii....

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Main Authors: Catherine D. Aimone, Hannah Giauque, Christine V. Hawkes
Format: Article
Language:English
Published: The American Phytopathological Society 2023-09-01
Series:Phytobiomes Journal
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-01-22-0006-FI
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author Catherine D. Aimone
Hannah Giauque
Christine V. Hawkes
author_facet Catherine D. Aimone
Hannah Giauque
Christine V. Hawkes
author_sort Catherine D. Aimone
collection DOAJ
description Foliar fungal endophytes are known to alter plant physiology but the mechanisms by which they do so remain poorly understood. We focused on how plant gene expression was altered by six fungal strains that generated “water-saver” and “water-spender” drought physiologies in a C4 grass, Panicum hallii. Water-saver physiologies have lower plant water loss, improved wilt resistance, and higher survival compared with water-spender strategies. We expected that fungi within each functional group would have similar effects on P. hallii, and this was largely true for plant physiology but not for plant gene expression. When we focused only on genes that were differentially expressed relative to fungus-free controls, we found surprisingly little overlap in plant differentially expressed genes or gene regulatory pathways across the fungal treatments, including within and between the water-saver and water-spender strategies. Nevertheless, using lasso regression, we identified a small subset of genes that predicted 39 and 53% of the variation in plant wilt resistance and water loss, respectively. These results suggest that fungal effects on plant transcription may identify how they extend the plant phenotype, and the comparison across multiple fungi allows us to differentiate broadly fungal-responsive plant genes versus those plant genes that respond only to single fungal taxa. The genes identified here could be targeted for future study to understand their function and, ultimately, represent candidates for precision breeding efforts to increase plant drought tolerance. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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spelling doaj.art-288ab6f6f6044b7bb6a3e3421e4621422023-09-22T23:26:54ZengThe American Phytopathological SocietyPhytobiomes Journal2471-29062023-09-017217218310.1094/PBIOMES-01-22-0006-FIFungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene ExpressionCatherine D. Aimone0Hannah Giauque1Christine V. Hawkes2Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NCDepartment of Integrative Biology, University of Texas at Austin, Austin, TXDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NCFoliar fungal endophytes are known to alter plant physiology but the mechanisms by which they do so remain poorly understood. We focused on how plant gene expression was altered by six fungal strains that generated “water-saver” and “water-spender” drought physiologies in a C4 grass, Panicum hallii. Water-saver physiologies have lower plant water loss, improved wilt resistance, and higher survival compared with water-spender strategies. We expected that fungi within each functional group would have similar effects on P. hallii, and this was largely true for plant physiology but not for plant gene expression. When we focused only on genes that were differentially expressed relative to fungus-free controls, we found surprisingly little overlap in plant differentially expressed genes or gene regulatory pathways across the fungal treatments, including within and between the water-saver and water-spender strategies. Nevertheless, using lasso regression, we identified a small subset of genes that predicted 39 and 53% of the variation in plant wilt resistance and water loss, respectively. These results suggest that fungal effects on plant transcription may identify how they extend the plant phenotype, and the comparison across multiple fungi allows us to differentiate broadly fungal-responsive plant genes versus those plant genes that respond only to single fungal taxa. The genes identified here could be targeted for future study to understand their function and, ultimately, represent candidates for precision breeding efforts to increase plant drought tolerance. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-01-22-0006-FIAscomycotamicrobiomePanicum halliiRNA-seqstress tolerance
spellingShingle Catherine D. Aimone
Hannah Giauque
Christine V. Hawkes
Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
Phytobiomes Journal
Ascomycota
microbiome
Panicum hallii
RNA-seq
stress tolerance
title Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
title_full Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
title_fullStr Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
title_full_unstemmed Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
title_short Fungal Symbionts Generate Water-Saver and Water-Spender Plant Drought Strategies via Diverse Effects on Host Gene Expression
title_sort fungal symbionts generate water saver and water spender plant drought strategies via diverse effects on host gene expression
topic Ascomycota
microbiome
Panicum hallii
RNA-seq
stress tolerance
url https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-01-22-0006-FI
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AT christinevhawkes fungalsymbiontsgeneratewatersaverandwaterspenderplantdroughtstrategiesviadiverseeffectsonhostgeneexpression