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Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii

Kelps are key primary producers of cold and temperate marine coastal ecosystems and exhibit systemic defences against pathogens. Yet, the cellular mechanisms underpinning their immunity remain to be elucidated. We investigated the time course of infection of the kelp Macrocystis pyrifera by the oomy...

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Autores principales: Murúa, Pedro, Müller, Dieter G., Etemadi, Mohammad, van West, Pieter, Gachon, Claire M. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7317505/
https://www.ncbi.nlm.nih.gov/pubmed/31955420
http://dx.doi.org/10.1111/nph.16438
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author Murúa, Pedro
Müller, Dieter G.
Etemadi, Mohammad
van West, Pieter
Gachon, Claire M. M.
author_facet Murúa, Pedro
Müller, Dieter G.
Etemadi, Mohammad
van West, Pieter
Gachon, Claire M. M.
author_sort Murúa, Pedro
collection PubMed
description Kelps are key primary producers of cold and temperate marine coastal ecosystems and exhibit systemic defences against pathogens. Yet, the cellular mechanisms underpinning their immunity remain to be elucidated. We investigated the time course of infection of the kelp Macrocystis pyrifera by the oomycete Anisolpidium ectocarpii using TEM, in vivo autophagy markers and autophagy inhibitors. Over several infection cycles, A. ectocarpii undergoes sequential physiological shifts sensitive to autophagy inhibitors. Initially lipid‐rich, pathogen thalli become increasingly lipid‐depleted; they subsequently tend to become entirely abortive, irrespective of their lipid content. Moreover, infected algal cells mount local defences and can directly eliminate the pathogen by xenophagy. Finally, autophagy‐dependent plastid recycling is induced in uninfected host cells. We demonstrate the existence of local, inducible autophagic processes both in the pathogen and infected host cells, which result in the restriction of pathogen propagation. We also show the existence of a systemic algal response mediated by autophagy. We propose a working model accounting for all our observations, whereby the outcome of the algal–pathogen interaction (i.e. completion or not of the pathogen life cycle) is dictated by the induction, and possibly the mutual hijacking, of the host and pathogen autophagy machineries.
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spelling pubmed-73175052020-06-30 Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii Murúa, Pedro Müller, Dieter G. Etemadi, Mohammad van West, Pieter Gachon, Claire M. M. New Phytol Research Kelps are key primary producers of cold and temperate marine coastal ecosystems and exhibit systemic defences against pathogens. Yet, the cellular mechanisms underpinning their immunity remain to be elucidated. We investigated the time course of infection of the kelp Macrocystis pyrifera by the oomycete Anisolpidium ectocarpii using TEM, in vivo autophagy markers and autophagy inhibitors. Over several infection cycles, A. ectocarpii undergoes sequential physiological shifts sensitive to autophagy inhibitors. Initially lipid‐rich, pathogen thalli become increasingly lipid‐depleted; they subsequently tend to become entirely abortive, irrespective of their lipid content. Moreover, infected algal cells mount local defences and can directly eliminate the pathogen by xenophagy. Finally, autophagy‐dependent plastid recycling is induced in uninfected host cells. We demonstrate the existence of local, inducible autophagic processes both in the pathogen and infected host cells, which result in the restriction of pathogen propagation. We also show the existence of a systemic algal response mediated by autophagy. We propose a working model accounting for all our observations, whereby the outcome of the algal–pathogen interaction (i.e. completion or not of the pathogen life cycle) is dictated by the induction, and possibly the mutual hijacking, of the host and pathogen autophagy machineries. John Wiley and Sons Inc. 2020-02-29 2020-06 /pmc/articles/PMC7317505/ /pubmed/31955420 http://dx.doi.org/10.1111/nph.16438 Text en © 2020 The Authors. New Phytologist © 2020 New Phytologist Trust This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Murúa, Pedro
Müller, Dieter G.
Etemadi, Mohammad
van West, Pieter
Gachon, Claire M. M.
Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title_full Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title_fullStr Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title_full_unstemmed Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title_short Host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp Macrocystis pyrifera against the oomycete pathogen Anisolpidium ectocarpii
title_sort host and pathogen autophagy are central to the inducible local defences and systemic response of the giant kelp macrocystis pyrifera against the oomycete pathogen anisolpidium ectocarpii
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7317505/
https://www.ncbi.nlm.nih.gov/pubmed/31955420
http://dx.doi.org/10.1111/nph.16438
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