Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)

Plant-microbe interactions are a phenomenal display of symbiotic/parasitic relationships between living organisms. Plant growth-promoting rhizobacteria (PGPR) are some of the most widely investigated plant-beneficial microbes due to their capabilities in stimulating plant growth and development and...

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Main Authors: Manamele D. Mashabela, Fidele Tugizimana, Paul A. Steenkamp, Lizelle A. Piater, Ian A. Dubery, Tarekegn Terefe, Msizi I. Mhlongo
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1103413/full
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author Manamele D. Mashabela
Fidele Tugizimana
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
Tarekegn Terefe
Msizi I. Mhlongo
author_facet Manamele D. Mashabela
Fidele Tugizimana
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
Tarekegn Terefe
Msizi I. Mhlongo
author_sort Manamele D. Mashabela
collection DOAJ
description Plant-microbe interactions are a phenomenal display of symbiotic/parasitic relationships between living organisms. Plant growth-promoting rhizobacteria (PGPR) are some of the most widely investigated plant-beneficial microbes due to their capabilities in stimulating plant growth and development and conferring protection to plants against biotic and abiotic stresses. As such, PGPR-mediated plant priming/induced systemic resistance (ISR) has become a hot topic among researchers, particularly with prospects of applications in sustainable agriculture. The current study applies untargeted ultra-high performance liquid chromatography-high-definition mass spectrometry (UHPLC-HDMS) to investigate PGPR-based metabolic reconfigurations in the metabolome of primed wheat plants against Puccinia striiformis f. sp. tricti (Pst). A seed bio-priming approach was adopted, where seeds were coated with two PGPR strains namely Bacillus subtilis and Paenibacillus alvei (T22) and grown under controlled conditions in a glasshouse. The plants were infected with Pst one-week post-germination, followed by weekly harvesting of leaf material. Subsequent metabolite extraction was carried out for analysis on a UHPLC-HDMS system for data acquisition. The data was chemometrically processed to reveal the underlying trends and data structures as well as potential signatory biomarkers for priming against Pst. Results showed notable metabolic reprogramming in primary and secondary metabolism, where the amino acid and organic acid content of primed-control, primed-challenged and non-primed-challenged plants were differentially reprogrammed. Similar trends were observed from the secondary metabolism, in which primed plants (particularly primed-challenged) showed an up-regulation of phenolic compounds (flavonoids, hydroxycinnamic acids-HCAs- and HCA amides) compared to the non-primed plants. The metabolomics-based semi-quantitative and qualitative assessment of the plant metabolomes revealed a time-dependent metabolic reprogramming in primed-challenged and primed-unchallenged plants, indicating the metabolic adaptations of the plants to stripe rust infection over time.
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spelling doaj.art-3938335e87f845db89039c82d5dd1daf2023-04-12T13:40:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-04-011410.3389/fpls.2023.11034131103413Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)Manamele D. Mashabela0Fidele Tugizimana1Fidele Tugizimana2Paul A. Steenkamp3Lizelle A. Piater4Ian A. Dubery5Tarekegn Terefe6Msizi I. Mhlongo7Research Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaInternational Research and Development Division, Omnia Group, Ltd., Johannesburg, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaDivision of Small Grain Diseases and Crop Protection, Agricultural Research Council-Small Grains Institute (ARC-SGI), Private Bag X29 Bethlehem, Free State, Bethlehem, South AfricaResearch Centre for Plant Metabolomics, Department of Biochemistry, University of Johannesburg, Johannesburg, South AfricaPlant-microbe interactions are a phenomenal display of symbiotic/parasitic relationships between living organisms. Plant growth-promoting rhizobacteria (PGPR) are some of the most widely investigated plant-beneficial microbes due to their capabilities in stimulating plant growth and development and conferring protection to plants against biotic and abiotic stresses. As such, PGPR-mediated plant priming/induced systemic resistance (ISR) has become a hot topic among researchers, particularly with prospects of applications in sustainable agriculture. The current study applies untargeted ultra-high performance liquid chromatography-high-definition mass spectrometry (UHPLC-HDMS) to investigate PGPR-based metabolic reconfigurations in the metabolome of primed wheat plants against Puccinia striiformis f. sp. tricti (Pst). A seed bio-priming approach was adopted, where seeds were coated with two PGPR strains namely Bacillus subtilis and Paenibacillus alvei (T22) and grown under controlled conditions in a glasshouse. The plants were infected with Pst one-week post-germination, followed by weekly harvesting of leaf material. Subsequent metabolite extraction was carried out for analysis on a UHPLC-HDMS system for data acquisition. The data was chemometrically processed to reveal the underlying trends and data structures as well as potential signatory biomarkers for priming against Pst. Results showed notable metabolic reprogramming in primary and secondary metabolism, where the amino acid and organic acid content of primed-control, primed-challenged and non-primed-challenged plants were differentially reprogrammed. Similar trends were observed from the secondary metabolism, in which primed plants (particularly primed-challenged) showed an up-regulation of phenolic compounds (flavonoids, hydroxycinnamic acids-HCAs- and HCA amides) compared to the non-primed plants. The metabolomics-based semi-quantitative and qualitative assessment of the plant metabolomes revealed a time-dependent metabolic reprogramming in primed-challenged and primed-unchallenged plants, indicating the metabolic adaptations of the plants to stripe rust infection over time.https://www.frontiersin.org/articles/10.3389/fpls.2023.1103413/fullmetabolic reprogrammingplant primingplant growth promoting rhizobacteriainduced systematic resistanceultra-high performance liquid chromatography-high-definition mass spectrometryPuccinia striiformis f. sp. tricti
spellingShingle Manamele D. Mashabela
Fidele Tugizimana
Fidele Tugizimana
Paul A. Steenkamp
Lizelle A. Piater
Ian A. Dubery
Tarekegn Terefe
Msizi I. Mhlongo
Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
Frontiers in Plant Science
metabolic reprogramming
plant priming
plant growth promoting rhizobacteria
induced systematic resistance
ultra-high performance liquid chromatography-high-definition mass spectrometry
Puccinia striiformis f. sp. tricti
title Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
title_full Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
title_fullStr Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
title_full_unstemmed Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
title_short Metabolomic evaluation of PGPR defence priming in wheat (Triticum aestivum L.) cultivars infected with Puccinia striiformis f. sp. tritici (stripe rust)
title_sort metabolomic evaluation of pgpr defence priming in wheat triticum aestivum l cultivars infected with puccinia striiformis f sp tritici stripe rust
topic metabolic reprogramming
plant priming
plant growth promoting rhizobacteria
induced systematic resistance
ultra-high performance liquid chromatography-high-definition mass spectrometry
Puccinia striiformis f. sp. tricti
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1103413/full
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