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Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes

Anticipating an increased ecological awareness, scientists have been exploring new strategies to reduce the use of chemical pesticides to control pests and diseases. Triggering the intrinsic plant defense system is one of the promising strategies to reduce yield loss by pathogenic organisms, such as...

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Autores principales: Singh, Richard Raj, Pajar, Jessil Ann, Audenaert, Kris, Kyndt, Tina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8386471/
https://www.ncbi.nlm.nih.gov/pubmed/34456953
http://dx.doi.org/10.3389/fpls.2021.713870
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author Singh, Richard Raj
Pajar, Jessil Ann
Audenaert, Kris
Kyndt, Tina
author_facet Singh, Richard Raj
Pajar, Jessil Ann
Audenaert, Kris
Kyndt, Tina
author_sort Singh, Richard Raj
collection PubMed
description Anticipating an increased ecological awareness, scientists have been exploring new strategies to reduce the use of chemical pesticides to control pests and diseases. Triggering the intrinsic plant defense system is one of the promising strategies to reduce yield loss by pathogenic organisms, such as nematodes. Ascorbate oxidase (AO) enzyme plays an important role in plant defense by regulating the apoplastic ascorbate/dehydroascorbate (DHA) ratio via the ascorbate oxidation process. Ascorbate oxidation is known to induce systemic resistance in rice against parasitic root-knot nematodes (RKN). Here, we sought to evaluate if AO- or DHA-induced resistance (IR) against RKN M. graminicola involves activation of the phenylpropanoid pathway and whether this IR phenotype has potential effects on growth of rice seedlings under stressed and unstressed conditions. Our results show that AO/DHA-IR against these parasitic nematodes is dependent on activation of phenylalanine ammonia lyase (PAL). However, application of reduced ascorbic acid (AA) did not induce this response. Gene expression analysis via qRT-PCR showed that OsPAL2 and OsPAL4 are highly expressed in AO/DHA-sprayed nematode-infected roots and PAL-activity measurements confirmed that AO/DHA spraying triggers the plants for primed activation of this enzyme upon nematode infection. AO/DHA-IR is not effective in plants sprayed with a chemical PAL inhibitor confirming that AO/DHA-induced resistance is dependent on PAL activity. Improved plant growth and low nematode infection in AO/DHA-sprayed plants was found to be correlated with an increase in shoot chlorophyll fluorescence (Fv/Fm), chlorophyll index (ChlIdx), and modified anthocyanin reflection index which were proven to be good above-ground parameters for nematode infestation. A detailed growth analysis confirmed the improved growth of AO/DHA-treated plants under nematode-infected conditions. Taken together, our results indicate that ascorbate oxidation enhances the phenylpropanoid-based response to nematode infection and leads to a tolerance phenotype in treated rice plants.
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spelling pubmed-83864712021-08-26 Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes Singh, Richard Raj Pajar, Jessil Ann Audenaert, Kris Kyndt, Tina Front Plant Sci Plant Science Anticipating an increased ecological awareness, scientists have been exploring new strategies to reduce the use of chemical pesticides to control pests and diseases. Triggering the intrinsic plant defense system is one of the promising strategies to reduce yield loss by pathogenic organisms, such as nematodes. Ascorbate oxidase (AO) enzyme plays an important role in plant defense by regulating the apoplastic ascorbate/dehydroascorbate (DHA) ratio via the ascorbate oxidation process. Ascorbate oxidation is known to induce systemic resistance in rice against parasitic root-knot nematodes (RKN). Here, we sought to evaluate if AO- or DHA-induced resistance (IR) against RKN M. graminicola involves activation of the phenylpropanoid pathway and whether this IR phenotype has potential effects on growth of rice seedlings under stressed and unstressed conditions. Our results show that AO/DHA-IR against these parasitic nematodes is dependent on activation of phenylalanine ammonia lyase (PAL). However, application of reduced ascorbic acid (AA) did not induce this response. Gene expression analysis via qRT-PCR showed that OsPAL2 and OsPAL4 are highly expressed in AO/DHA-sprayed nematode-infected roots and PAL-activity measurements confirmed that AO/DHA spraying triggers the plants for primed activation of this enzyme upon nematode infection. AO/DHA-IR is not effective in plants sprayed with a chemical PAL inhibitor confirming that AO/DHA-induced resistance is dependent on PAL activity. Improved plant growth and low nematode infection in AO/DHA-sprayed plants was found to be correlated with an increase in shoot chlorophyll fluorescence (Fv/Fm), chlorophyll index (ChlIdx), and modified anthocyanin reflection index which were proven to be good above-ground parameters for nematode infestation. A detailed growth analysis confirmed the improved growth of AO/DHA-treated plants under nematode-infected conditions. Taken together, our results indicate that ascorbate oxidation enhances the phenylpropanoid-based response to nematode infection and leads to a tolerance phenotype in treated rice plants. Frontiers Media S.A. 2021-08-11 /pmc/articles/PMC8386471/ /pubmed/34456953 http://dx.doi.org/10.3389/fpls.2021.713870 Text en Copyright © 2021 Singh, Pajar, Audenaert and Kyndt. 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
Singh, Richard Raj
Pajar, Jessil Ann
Audenaert, Kris
Kyndt, Tina
Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title_full Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title_fullStr Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title_full_unstemmed Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title_short Induced Resistance by Ascorbate Oxidation Involves Potentiating of the Phenylpropanoid Pathway and Improved Rice Tolerance to Parasitic Nematodes
title_sort induced resistance by ascorbate oxidation involves potentiating of the phenylpropanoid pathway and improved rice tolerance to parasitic nematodes
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8386471/
https://www.ncbi.nlm.nih.gov/pubmed/34456953
http://dx.doi.org/10.3389/fpls.2021.713870
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