Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density

Abstract Background Commercial cultivars of perennial ryegrass infected with selected Epichloë fungal endophytes are highly desirable in certain pastures as the resulting mutualistic association has the capacity to confer agronomic benefits (such as invertebrate pest deterrence) largely due to funga...

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Main Authors: Kim A. Richardson, Anouck C. M. de Bonth, Zac Beechey-Gradwell, Suhas Kadam, Luke J. Cooney, Kelly A. Nelson, Ruth Cookson, Somrutai Winichayakul, Michele Reid, Philip Anderson, Tracey Crowther, Xiuying Zou, Dorothy Maher, Hong Xue, Richard W. Scott, Anne Allan, Richard D. Johnson, Stuart D. Card, Wade J. Mace, Nicholas J. Roberts, Gregory Bryan
Format: Article
Language:English
Published: BMC 2023-12-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-023-04635-8
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author Kim A. Richardson
Anouck C. M. de Bonth
Zac Beechey-Gradwell
Suhas Kadam
Luke J. Cooney
Kelly A. Nelson
Ruth Cookson
Somrutai Winichayakul
Michele Reid
Philip Anderson
Tracey Crowther
Xiuying Zou
Dorothy Maher
Hong Xue
Richard W. Scott
Anne Allan
Richard D. Johnson
Stuart D. Card
Wade J. Mace
Nicholas J. Roberts
Gregory Bryan
author_facet Kim A. Richardson
Anouck C. M. de Bonth
Zac Beechey-Gradwell
Suhas Kadam
Luke J. Cooney
Kelly A. Nelson
Ruth Cookson
Somrutai Winichayakul
Michele Reid
Philip Anderson
Tracey Crowther
Xiuying Zou
Dorothy Maher
Hong Xue
Richard W. Scott
Anne Allan
Richard D. Johnson
Stuart D. Card
Wade J. Mace
Nicholas J. Roberts
Gregory Bryan
author_sort Kim A. Richardson
collection DOAJ
description Abstract Background Commercial cultivars of perennial ryegrass infected with selected Epichloë fungal endophytes are highly desirable in certain pastures as the resulting mutualistic association has the capacity to confer agronomic benefits (such as invertebrate pest deterrence) largely due to fungal produced secondary metabolites (e.g., alkaloids). In this study, we investigated T2 segregating populations derived from two independent transformation events expressing diacylglycerol acyltransferase (DGAT) and cysteine oleosin (CO) genes designed to increase foliar lipid and biomass accumulation. These populations were either infected with Epichloë festucae var. lolii strain AR1 or Epichloë sp. LpTG-3 strain AR37 to examine relationships between the introduced trait and the endophytic association. Here we report on experiments designed to investigate if expression of the DGAT + CO trait in foliar tissues of perennial ryegrass could negatively impact the grass-endophyte association and vice versa. Both endophyte and plant characters were measured under controlled environment and field conditions. Results Expected relative increases in total fatty acids of 17–58% accrued as a result of DGAT + CO expression with no significant difference between the endophyte-infected and non-infected progeny. Hyphal growth in association with DGAT + CO expression appeared normal when compared to control plants in a growth chamber. There was no significant difference in mycelial biomass for both strains AR1 and AR37, however, Epichloë-derived alkaloid concentrations were significantly lower on some occasions in the DGAT + CO plants compared to the corresponding null-segregant progenies, although these remained within the reported range for bioactivity. Conclusions These results suggest that the mutualistic association formed between perennial ryegrass and selected Epichloë strains does not influence expression of the host DGAT + CO technology, but that endophyte performance may be reduced under some circumstances. Further investigation will now be required to determine the preferred genetic backgrounds for introgression of the DGAT + CO trait in combination with selected endophyte strains, as grass host genetics is a major determinant to the success of the grass-endophyte association in this species.
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spelling doaj.art-a43ddee66a7c4d958b6c8968ded59bbd2023-12-17T12:11:54ZengBMCBMC Plant Biology1471-22292023-12-0123111410.1186/s12870-023-04635-8Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy densityKim A. Richardson0Anouck C. M. de Bonth1Zac Beechey-Gradwell2Suhas Kadam3Luke J. Cooney4Kelly A. Nelson5Ruth Cookson6Somrutai Winichayakul7Michele Reid8Philip Anderson9Tracey Crowther10Xiuying Zou11Dorothy Maher12Hong Xue13Richard W. Scott14Anne Allan15Richard D. Johnson16Stuart D. Card17Wade J. Mace18Nicholas J. Roberts19Gregory Bryan20Resilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdDivision of Plant Sciences & Technology, University of MissouriResilient Agriculture, AgResearch LtdDivision of Plant Sciences & Technology, University of MissouriResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdResilient Agriculture, AgResearch LtdAbstract Background Commercial cultivars of perennial ryegrass infected with selected Epichloë fungal endophytes are highly desirable in certain pastures as the resulting mutualistic association has the capacity to confer agronomic benefits (such as invertebrate pest deterrence) largely due to fungal produced secondary metabolites (e.g., alkaloids). In this study, we investigated T2 segregating populations derived from two independent transformation events expressing diacylglycerol acyltransferase (DGAT) and cysteine oleosin (CO) genes designed to increase foliar lipid and biomass accumulation. These populations were either infected with Epichloë festucae var. lolii strain AR1 or Epichloë sp. LpTG-3 strain AR37 to examine relationships between the introduced trait and the endophytic association. Here we report on experiments designed to investigate if expression of the DGAT + CO trait in foliar tissues of perennial ryegrass could negatively impact the grass-endophyte association and vice versa. Both endophyte and plant characters were measured under controlled environment and field conditions. Results Expected relative increases in total fatty acids of 17–58% accrued as a result of DGAT + CO expression with no significant difference between the endophyte-infected and non-infected progeny. Hyphal growth in association with DGAT + CO expression appeared normal when compared to control plants in a growth chamber. There was no significant difference in mycelial biomass for both strains AR1 and AR37, however, Epichloë-derived alkaloid concentrations were significantly lower on some occasions in the DGAT + CO plants compared to the corresponding null-segregant progenies, although these remained within the reported range for bioactivity. Conclusions These results suggest that the mutualistic association formed between perennial ryegrass and selected Epichloë strains does not influence expression of the host DGAT + CO technology, but that endophyte performance may be reduced under some circumstances. Further investigation will now be required to determine the preferred genetic backgrounds for introgression of the DGAT + CO trait in combination with selected endophyte strains, as grass host genetics is a major determinant to the success of the grass-endophyte association in this species.https://doi.org/10.1186/s12870-023-04635-8Lolium perenneEpichloëLipidsMetabolizable energy
spellingShingle Kim A. Richardson
Anouck C. M. de Bonth
Zac Beechey-Gradwell
Suhas Kadam
Luke J. Cooney
Kelly A. Nelson
Ruth Cookson
Somrutai Winichayakul
Michele Reid
Philip Anderson
Tracey Crowther
Xiuying Zou
Dorothy Maher
Hong Xue
Richard W. Scott
Anne Allan
Richard D. Johnson
Stuart D. Card
Wade J. Mace
Nicholas J. Roberts
Gregory Bryan
Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
BMC Plant Biology
Lolium perenne
Epichloë
Lipids
Metabolizable energy
title Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
title_full Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
title_fullStr Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
title_full_unstemmed Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
title_short Epichloë fungal endophyte interactions in perennial ryegrass (Lolium perenne L.) modified to accumulate foliar lipids for increased energy density
title_sort epichloe fungal endophyte interactions in perennial ryegrass lolium perenne l modified to accumulate foliar lipids for increased energy density
topic Lolium perenne
Epichloë
Lipids
Metabolizable energy
url https://doi.org/10.1186/s12870-023-04635-8
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