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Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem

INTRODUCTION: Food security is a major challenge to sustainably supply food to meet the demands of the ever-growing global population. Crop loss due to pathogens is a major concern to overcoming this global food security challenge. Soybean root and stem rot caused by Phytophthora sojae results in ap...

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Autores principales: Adigun, Oludoyin Adeseun, Pham, Thu Huong, Grapov, Dmitry, Nadeem, Muhammad, Jewell, Linda Elizabeth, Cheema, Mumtaz, Galagedara, Lakshman, Thomas, Raymond
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10219219/
https://www.ncbi.nlm.nih.gov/pubmed/37251755
http://dx.doi.org/10.3389/fpls.2023.1141823
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author Adigun, Oludoyin Adeseun
Pham, Thu Huong
Grapov, Dmitry
Nadeem, Muhammad
Jewell, Linda Elizabeth
Cheema, Mumtaz
Galagedara, Lakshman
Thomas, Raymond
author_facet Adigun, Oludoyin Adeseun
Pham, Thu Huong
Grapov, Dmitry
Nadeem, Muhammad
Jewell, Linda Elizabeth
Cheema, Mumtaz
Galagedara, Lakshman
Thomas, Raymond
author_sort Adigun, Oludoyin Adeseun
collection PubMed
description INTRODUCTION: Food security is a major challenge to sustainably supply food to meet the demands of the ever-growing global population. Crop loss due to pathogens is a major concern to overcoming this global food security challenge. Soybean root and stem rot caused by Phytophthora sojae results in approximately 20B $US crop loss annually. Phyto-oxylipins are metabolites biosynthesized in the plants by oxidative transformation of polyunsaturated fatty acids through an array of diverging metabolic pathways and play an important role in plant development and defense against pathogen colonization and infection. Lipid mediated plant immunity is a very attractive target for developing long term resistance in many plants’ disease pathosystem. However, little is known about the phyto-oxylipin’s role in the successful strategies used by tolerant soybean cultivar to mitigate Phytophthora sojae infection. METHODS: We used scanning electron microscopy to observe the alterations in root morphology and a targeted lipidomics approach using high resolution accurate mass tandem mass spectrometry to assess phyto-oxylipin anabolism at 48 h, 72 h and 96 h post infection. RESULTS AND DISCUSSION: We observed the presence of biogenic crystals and reinforced epidermal walls in the tolerant cultivar suggesting a mechanism for disease tolerance when compared with susceptible cultivar. Similarly, the unequivocally unique biomarkers implicated in oxylipin mediated plant immunity [10(E),12(Z)-13S-hydroxy-9(Z),11(E),15(Z)-octadecatrienoic acid, (Z)-12,13-dihydroxyoctadec-9-enoic acid, (9Z,11E)-13-Oxo-9,11-octadecadienoic acid, 15(Z)-9-oxo-octadecatrienoic acid, 10(E),12(E)-9-hydroperoxyoctadeca-10,12-dienoic acid, 12-oxophytodienoic acid and (12Z,15Z)-9, 10-dihydroxyoctadeca-12,15-dienoic acid] generated from intact oxidized lipid precursors were upregulated in tolerant soybean cultivar while downregulated in infected susceptible cultivar relative to non-inoculated controls at 48 h, 72 h and 96 h post infection by Phytophthora sojae, suggesting that these molecules may be a critical component of the defense strategies used in tolerant cultivar against Phytophthora sojae infection. Interestingly, microbial originated oxylipins, 12S-hydroperoxy-5(Z),8(Z),10(E),14(Z)-eicosatetraenoic acid and (4Z,7Z,10Z,13Z)-15-[3-[(Z)-pent-2-enyl]oxiran-2-yl]pentadeca-4,7,10,13-tetraenoic acid were upregulated only in infected susceptible cultivar but downregulated in infected tolerant cultivar. These microbial originated oxylipins are capable of modulating plant immune response to enhance virulence. This study demonstrated novel evidence for phyto-oxylipin metabolism in soybean cultivars during pathogen colonization and infection using the Phytophthora sojae-soybean pathosystem. This evidence may have potential applications in further elucidation and resolution of the role of phyto-oxylipin anabolism in soybean tolerance to Phytophthora sojae colonization and infection.
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spelling pubmed-102192192023-05-27 Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem Adigun, Oludoyin Adeseun Pham, Thu Huong Grapov, Dmitry Nadeem, Muhammad Jewell, Linda Elizabeth Cheema, Mumtaz Galagedara, Lakshman Thomas, Raymond Front Plant Sci Plant Science INTRODUCTION: Food security is a major challenge to sustainably supply food to meet the demands of the ever-growing global population. Crop loss due to pathogens is a major concern to overcoming this global food security challenge. Soybean root and stem rot caused by Phytophthora sojae results in approximately 20B $US crop loss annually. Phyto-oxylipins are metabolites biosynthesized in the plants by oxidative transformation of polyunsaturated fatty acids through an array of diverging metabolic pathways and play an important role in plant development and defense against pathogen colonization and infection. Lipid mediated plant immunity is a very attractive target for developing long term resistance in many plants’ disease pathosystem. However, little is known about the phyto-oxylipin’s role in the successful strategies used by tolerant soybean cultivar to mitigate Phytophthora sojae infection. METHODS: We used scanning electron microscopy to observe the alterations in root morphology and a targeted lipidomics approach using high resolution accurate mass tandem mass spectrometry to assess phyto-oxylipin anabolism at 48 h, 72 h and 96 h post infection. RESULTS AND DISCUSSION: We observed the presence of biogenic crystals and reinforced epidermal walls in the tolerant cultivar suggesting a mechanism for disease tolerance when compared with susceptible cultivar. Similarly, the unequivocally unique biomarkers implicated in oxylipin mediated plant immunity [10(E),12(Z)-13S-hydroxy-9(Z),11(E),15(Z)-octadecatrienoic acid, (Z)-12,13-dihydroxyoctadec-9-enoic acid, (9Z,11E)-13-Oxo-9,11-octadecadienoic acid, 15(Z)-9-oxo-octadecatrienoic acid, 10(E),12(E)-9-hydroperoxyoctadeca-10,12-dienoic acid, 12-oxophytodienoic acid and (12Z,15Z)-9, 10-dihydroxyoctadeca-12,15-dienoic acid] generated from intact oxidized lipid precursors were upregulated in tolerant soybean cultivar while downregulated in infected susceptible cultivar relative to non-inoculated controls at 48 h, 72 h and 96 h post infection by Phytophthora sojae, suggesting that these molecules may be a critical component of the defense strategies used in tolerant cultivar against Phytophthora sojae infection. Interestingly, microbial originated oxylipins, 12S-hydroperoxy-5(Z),8(Z),10(E),14(Z)-eicosatetraenoic acid and (4Z,7Z,10Z,13Z)-15-[3-[(Z)-pent-2-enyl]oxiran-2-yl]pentadeca-4,7,10,13-tetraenoic acid were upregulated only in infected susceptible cultivar but downregulated in infected tolerant cultivar. These microbial originated oxylipins are capable of modulating plant immune response to enhance virulence. This study demonstrated novel evidence for phyto-oxylipin metabolism in soybean cultivars during pathogen colonization and infection using the Phytophthora sojae-soybean pathosystem. This evidence may have potential applications in further elucidation and resolution of the role of phyto-oxylipin anabolism in soybean tolerance to Phytophthora sojae colonization and infection. Frontiers Media S.A. 2023-05-12 /pmc/articles/PMC10219219/ /pubmed/37251755 http://dx.doi.org/10.3389/fpls.2023.1141823 Text en Copyright © 2023 Adigun, Pham, Grapov, Nadeem, Jewell, Cheema, Galagedara and Thomas https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Adigun, Oludoyin Adeseun
Pham, Thu Huong
Grapov, Dmitry
Nadeem, Muhammad
Jewell, Linda Elizabeth
Cheema, Mumtaz
Galagedara, Lakshman
Thomas, Raymond
Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title_full Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title_fullStr Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title_full_unstemmed Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title_short Phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-Phytophthora sojae pathosystem
title_sort phyto-oxylipin mediated plant immune response to colonization and infection in the soybean-phytophthora sojae pathosystem
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10219219/
https://www.ncbi.nlm.nih.gov/pubmed/37251755
http://dx.doi.org/10.3389/fpls.2023.1141823
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