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Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation

Gall formation on the belowground parts of plants infected with Plasmodiophora brassicae is the result of extensive host cellular reprogramming. The development of these structures is a consequence of increased cell proliferation followed by massive enlargement of cells colonized with the pathogen....

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Autores principales: Stefanowicz, Karolina, Szymanska-Chargot, Monika, Truman, William, Walerowski, Piotr, Olszak, Marcin, Augustyniak, Adam, Kosmala, Arkadiusz, Zdunek, Artur, Malinowski, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359924/
https://www.ncbi.nlm.nih.gov/pubmed/34394168
http://dx.doi.org/10.3389/fpls.2021.711838
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author Stefanowicz, Karolina
Szymanska-Chargot, Monika
Truman, William
Walerowski, Piotr
Olszak, Marcin
Augustyniak, Adam
Kosmala, Arkadiusz
Zdunek, Artur
Malinowski, Robert
author_facet Stefanowicz, Karolina
Szymanska-Chargot, Monika
Truman, William
Walerowski, Piotr
Olszak, Marcin
Augustyniak, Adam
Kosmala, Arkadiusz
Zdunek, Artur
Malinowski, Robert
author_sort Stefanowicz, Karolina
collection PubMed
description Gall formation on the belowground parts of plants infected with Plasmodiophora brassicae is the result of extensive host cellular reprogramming. The development of these structures is a consequence of increased cell proliferation followed by massive enlargement of cells colonized with the pathogen. Drastic changes in cellular growth patterns create local deformities in the roots and hypocotyl giving rise to mechanical tensions within the tissue of these organs. Host cell wall extensibility and recomposition accompany the growth of the gall and influence pathogen spread and also pathogen life cycle progression. Demethylation of pectin within the extracellular matrix may play an important role in P. brassicae-driven hypertrophy of host underground organs. Through proteomic analysis of the cell wall, we identified proteins accumulating in the galls developing on the underground parts of Arabidopsis thaliana plants infected with P. brassicae. One of the key proteins identified was the pectin methylesterase (PME18); we further characterized its expression and conducted functional and anatomic studies in the knockout mutant and used Raman spectroscopy to study the status of pectin in P. brassicae-infected galls. We found that late stages of gall formation are accompanied with increased levels of PME18. We have also shown that the massive enlargement of cells colonized with P. brassicae coincides with decreases in pectin methylation. In pme18-2 knockout mutants, P. brassicae could still induce demethylation; however, the galls in this line were smaller and cellular expansion was less pronounced. Alteration in pectin demethylation in the host resulted in changes in pathogen distribution and slowed down disease progression. To conclude, P. brassicae-driven host organ hypertrophy observed during clubroot disease is accompanied by pectin demethylation in the extracellular matrix. The pathogen hijacks endogenous host mechanisms involved in cell wall loosening to create an optimal cellular environment for completion of its life cycle and eventual release of resting spores facilitated by degradation of demethylated pectin polymers.
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spelling pubmed-83599242021-08-13 Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation Stefanowicz, Karolina Szymanska-Chargot, Monika Truman, William Walerowski, Piotr Olszak, Marcin Augustyniak, Adam Kosmala, Arkadiusz Zdunek, Artur Malinowski, Robert Front Plant Sci Plant Science Gall formation on the belowground parts of plants infected with Plasmodiophora brassicae is the result of extensive host cellular reprogramming. The development of these structures is a consequence of increased cell proliferation followed by massive enlargement of cells colonized with the pathogen. Drastic changes in cellular growth patterns create local deformities in the roots and hypocotyl giving rise to mechanical tensions within the tissue of these organs. Host cell wall extensibility and recomposition accompany the growth of the gall and influence pathogen spread and also pathogen life cycle progression. Demethylation of pectin within the extracellular matrix may play an important role in P. brassicae-driven hypertrophy of host underground organs. Through proteomic analysis of the cell wall, we identified proteins accumulating in the galls developing on the underground parts of Arabidopsis thaliana plants infected with P. brassicae. One of the key proteins identified was the pectin methylesterase (PME18); we further characterized its expression and conducted functional and anatomic studies in the knockout mutant and used Raman spectroscopy to study the status of pectin in P. brassicae-infected galls. We found that late stages of gall formation are accompanied with increased levels of PME18. We have also shown that the massive enlargement of cells colonized with P. brassicae coincides with decreases in pectin methylation. In pme18-2 knockout mutants, P. brassicae could still induce demethylation; however, the galls in this line were smaller and cellular expansion was less pronounced. Alteration in pectin demethylation in the host resulted in changes in pathogen distribution and slowed down disease progression. To conclude, P. brassicae-driven host organ hypertrophy observed during clubroot disease is accompanied by pectin demethylation in the extracellular matrix. The pathogen hijacks endogenous host mechanisms involved in cell wall loosening to create an optimal cellular environment for completion of its life cycle and eventual release of resting spores facilitated by degradation of demethylated pectin polymers. Frontiers Media S.A. 2021-07-29 /pmc/articles/PMC8359924/ /pubmed/34394168 http://dx.doi.org/10.3389/fpls.2021.711838 Text en Copyright © 2021 Stefanowicz, Szymanska-Chargot, Truman, Walerowski, Olszak, Augustyniak, Kosmala, Zdunek and Malinowski. 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
Stefanowicz, Karolina
Szymanska-Chargot, Monika
Truman, William
Walerowski, Piotr
Olszak, Marcin
Augustyniak, Adam
Kosmala, Arkadiusz
Zdunek, Artur
Malinowski, Robert
Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title_full Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title_fullStr Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title_full_unstemmed Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title_short Plasmodiophora brassicae-Triggered Cell Enlargement and Loss of Cellular Integrity in Root Systems Are Mediated by Pectin Demethylation
title_sort plasmodiophora brassicae-triggered cell enlargement and loss of cellular integrity in root systems are mediated by pectin demethylation
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359924/
https://www.ncbi.nlm.nih.gov/pubmed/34394168
http://dx.doi.org/10.3389/fpls.2021.711838
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