Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection

Necrotrophic fungi affect a wide range of plants and cause significant crop losses. For the activation of multi-layered innate immune defences, plants can be primed or pre-conditioned to rapidly and more efficiently counteract this pathogen. Untargeted and targeted metabolomics analyses were applied...

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Main Authors: Claude Y. Hamany Djande, Fidele Tugizimana, Paul A. Steenkamp, Lizelle A. Piater, Ian A. Dubery
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/13/9/997
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author Claude Y. Hamany Djande
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
author_facet Claude Y. Hamany Djande
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
author_sort Claude Y. Hamany Djande
collection DOAJ
description Necrotrophic fungi affect a wide range of plants and cause significant crop losses. For the activation of multi-layered innate immune defences, plants can be primed or pre-conditioned to rapidly and more efficiently counteract this pathogen. Untargeted and targeted metabolomics analyses were applied to elucidate the biochemical processes involved in the response of 3,5-dichloroanthranilic acid (3,5-DCAA) primed barley plants to <i>Pyrenophora teres</i> f. <i>teres</i> (<i>Ptt</i>). A susceptible barley cultivar (‘Hessekwa’) at the third leaf growth stage was treated with 3,5-DCAA 24 h prior to infection using a <i>Ptt</i> conidia suspension. The infection was monitored over 2, 4, and 6 days post-inoculation. For untargeted studies, ultra-high performance liquid chromatography coupled with high-resolution mass spectrometry (UHPLC–MS) was used to analyse methanolic plant extracts. Acquired data were processed to generate the data matrices utilised in chemometric modelling and multi-dimensional data mining. For targeted studies, selected metabolites from the amino acids, phenolic acids, and alkaloids classes were quantified using multiple reaction monitoring (MRM) mass spectrometry. 3,5-DCAA was effective as a priming agent in delaying the onset and intensity of symptoms but could not prevent the progression of the disease. Unsupervised learning methods revealed clear differences between the sample extracts from the control plants and the infected plants. Both orthogonal projection to latent structure-discriminant analysis (OPLS-DA) and ‘shared and unique structures’ (SUS) plots allowed for the extraction of potential markers of the primed and naïve plant responses to <i>Ptt</i>. These include classes of organic acids, fatty acids, amino acids, phenolic acids, and derivatives and flavonoids. Among these, 5-oxo-proline and citric acid were notable as priming response-related metabolites. Metabolites from the tricarboxylic acid pathway were only discriminant in the primed plant infected with <i>Ptt</i>. Furthermore, the quantification of targeted metabolites revealed that hydroxycinnamic acids were significantly more prominent in the primed infected plants, especially at 2 d.p.i. Our research advances efforts to better understand regulated and reprogrammed metabolic responses that constitute defence priming in barley against <i>Ptt</i>.
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spelling doaj.art-e157e64e61ac43d6a5979d1a35b992082023-11-19T11:55:19ZengMDPI AGMetabolites2218-19892023-09-0113999710.3390/metabo13090997Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> InfectionClaude Y. Hamany Djande0Fidele Tugizimana1Paul A. Steenkamp2Lizelle A. Piater3Ian A. Dubery4Research Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, P.O. Box 524, Auckland Park, Johannesburg 2006, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, P.O. Box 524, Auckland Park, Johannesburg 2006, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, P.O. Box 524, Auckland Park, Johannesburg 2006, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, P.O. Box 524, Auckland Park, Johannesburg 2006, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, P.O. Box 524, Auckland Park, Johannesburg 2006, South AfricaNecrotrophic fungi affect a wide range of plants and cause significant crop losses. For the activation of multi-layered innate immune defences, plants can be primed or pre-conditioned to rapidly and more efficiently counteract this pathogen. Untargeted and targeted metabolomics analyses were applied to elucidate the biochemical processes involved in the response of 3,5-dichloroanthranilic acid (3,5-DCAA) primed barley plants to <i>Pyrenophora teres</i> f. <i>teres</i> (<i>Ptt</i>). A susceptible barley cultivar (‘Hessekwa’) at the third leaf growth stage was treated with 3,5-DCAA 24 h prior to infection using a <i>Ptt</i> conidia suspension. The infection was monitored over 2, 4, and 6 days post-inoculation. For untargeted studies, ultra-high performance liquid chromatography coupled with high-resolution mass spectrometry (UHPLC–MS) was used to analyse methanolic plant extracts. Acquired data were processed to generate the data matrices utilised in chemometric modelling and multi-dimensional data mining. For targeted studies, selected metabolites from the amino acids, phenolic acids, and alkaloids classes were quantified using multiple reaction monitoring (MRM) mass spectrometry. 3,5-DCAA was effective as a priming agent in delaying the onset and intensity of symptoms but could not prevent the progression of the disease. Unsupervised learning methods revealed clear differences between the sample extracts from the control plants and the infected plants. Both orthogonal projection to latent structure-discriminant analysis (OPLS-DA) and ‘shared and unique structures’ (SUS) plots allowed for the extraction of potential markers of the primed and naïve plant responses to <i>Ptt</i>. These include classes of organic acids, fatty acids, amino acids, phenolic acids, and derivatives and flavonoids. Among these, 5-oxo-proline and citric acid were notable as priming response-related metabolites. Metabolites from the tricarboxylic acid pathway were only discriminant in the primed plant infected with <i>Ptt</i>. Furthermore, the quantification of targeted metabolites revealed that hydroxycinnamic acids were significantly more prominent in the primed infected plants, especially at 2 d.p.i. Our research advances efforts to better understand regulated and reprogrammed metabolic responses that constitute defence priming in barley against <i>Ptt</i>.https://www.mdpi.com/2218-1989/13/9/997barley<i>Pyrenophora teres</i>dichloroanthranilic acidhydroxycinnamic acidsmetabolomicsnet-blotch disease
spellingShingle Claude Y. Hamany Djande
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
Metabolites
barley
<i>Pyrenophora teres</i>
dichloroanthranilic acid
hydroxycinnamic acids
metabolomics
net-blotch disease
title Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
title_full Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
title_fullStr Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
title_full_unstemmed Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
title_short Metabolomic Reconfiguration in Primed Barley (<i>Hordeum vulgare</i>) Plants in Response to <i>Pyrenophora teres</i> f. <i>teres</i> Infection
title_sort metabolomic reconfiguration in primed barley i hordeum vulgare i plants in response to i pyrenophora teres i f i teres i infection
topic barley
<i>Pyrenophora teres</i>
dichloroanthranilic acid
hydroxycinnamic acids
metabolomics
net-blotch disease
url https://www.mdpi.com/2218-1989/13/9/997
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