Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen

ABSTRACT Multinucleate fungi and oomycetes are phylogenetically distant but structurally similar. To address whether they share similar nuclear dynamics, we carried out time-lapse imaging of fluorescently labeled Phytophthora palmivora nuclei. Nuclei underwent coordinated bidirectional movements dur...

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Autores principales:	Edouard Evangelisti, Liron Shenhav, Temur Yunusov, Marie Le Naour–Vernet, Philipp Rink, Sebastian Schornack
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	oomycetes Phytophthora palmivora nucleus movement centrosome hydrodynamics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/128100fbf47a48d5ac92f29168ea374b
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spelling	oai:doaj.org-article:128100fbf47a48d5ac92f29168ea374b2021-11-15T15:59:41ZHydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen10.1128/mBio.01516-192150-7511https://doaj.org/article/128100fbf47a48d5ac92f29168ea374b2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01516-19https://doaj.org/toc/2150-7511ABSTRACT Multinucleate fungi and oomycetes are phylogenetically distant but structurally similar. To address whether they share similar nuclear dynamics, we carried out time-lapse imaging of fluorescently labeled Phytophthora palmivora nuclei. Nuclei underwent coordinated bidirectional movements during plant infection. Within hyphal networks growing in planta or in axenic culture, nuclei either are dragged passively with the cytoplasm or actively become rerouted toward nucleus-depleted hyphal sections and often display a very stretched shape. Benomyl-induced depolymerization of microtubules reduced active movements and the occurrence of stretched nuclei. A centrosome protein localized at the leading end of stretched nuclei, suggesting that, as in fungi, astral microtubule-guided movements contribute to nuclear distribution within oomycete hyphae. The remarkable hydrodynamic shape adaptations of Phytophthora nuclei contrast with those in fungi and likely enable them to migrate over longer distances. Therefore, our work summarizes mechanisms which enable a near-equal nuclear distribution in an oomycete. We provide a basis for computational modeling of hydrodynamic nuclear deformation within branched tubular networks. IMPORTANCE Despite their fungal morphology, oomycetes constitute a distinct group of protists related to brown algae and diatoms. Many oomycetes are pathogens and cause diseases of plants, insects, mammals, and humans. Extensive efforts have been made to understand the molecular basis of oomycete infection, but durable protection against these pathogens is yet to be achieved. We use a plant-pathogenic oomycete to decipher a key physiological aspect of oomycete growth and infection. We show that oomycete nuclei travel actively and over long distances within hyphae and during infection. Such movements require microtubules anchored on the centrosome. Nuclei hydrodynamically adapt their shape to travel in or against the flow. In contrast, fungi lack a centrosome and have much less flexible nuclei. Our findings provide a basis for modeling of flexible nuclear shapes in branched hyphal networks and may help in finding hard-to-evade targets to develop specific antioomycete strategies and achieve durable crop disease protection.Edouard EvangelistiLiron ShenhavTemur YunusovMarie Le Naour–VernetPhilipp RinkSebastian SchornackAmerican Society for MicrobiologyarticleoomycetesPhytophthora palmivoranucleus movementcentrosomehydrodynamicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	oomycetes Phytophthora palmivora nucleus movement centrosome hydrodynamics Microbiology QR1-502
spellingShingle	oomycetes Phytophthora palmivora nucleus movement centrosome hydrodynamics Microbiology QR1-502 Edouard Evangelisti Liron Shenhav Temur Yunusov Marie Le Naour–Vernet Philipp Rink Sebastian Schornack Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
description	ABSTRACT Multinucleate fungi and oomycetes are phylogenetically distant but structurally similar. To address whether they share similar nuclear dynamics, we carried out time-lapse imaging of fluorescently labeled Phytophthora palmivora nuclei. Nuclei underwent coordinated bidirectional movements during plant infection. Within hyphal networks growing in planta or in axenic culture, nuclei either are dragged passively with the cytoplasm or actively become rerouted toward nucleus-depleted hyphal sections and often display a very stretched shape. Benomyl-induced depolymerization of microtubules reduced active movements and the occurrence of stretched nuclei. A centrosome protein localized at the leading end of stretched nuclei, suggesting that, as in fungi, astral microtubule-guided movements contribute to nuclear distribution within oomycete hyphae. The remarkable hydrodynamic shape adaptations of Phytophthora nuclei contrast with those in fungi and likely enable them to migrate over longer distances. Therefore, our work summarizes mechanisms which enable a near-equal nuclear distribution in an oomycete. We provide a basis for computational modeling of hydrodynamic nuclear deformation within branched tubular networks. IMPORTANCE Despite their fungal morphology, oomycetes constitute a distinct group of protists related to brown algae and diatoms. Many oomycetes are pathogens and cause diseases of plants, insects, mammals, and humans. Extensive efforts have been made to understand the molecular basis of oomycete infection, but durable protection against these pathogens is yet to be achieved. We use a plant-pathogenic oomycete to decipher a key physiological aspect of oomycete growth and infection. We show that oomycete nuclei travel actively and over long distances within hyphae and during infection. Such movements require microtubules anchored on the centrosome. Nuclei hydrodynamically adapt their shape to travel in or against the flow. In contrast, fungi lack a centrosome and have much less flexible nuclei. Our findings provide a basis for modeling of flexible nuclear shapes in branched hyphal networks and may help in finding hard-to-evade targets to develop specific antioomycete strategies and achieve durable crop disease protection.
format	article
author	Edouard Evangelisti Liron Shenhav Temur Yunusov Marie Le Naour–Vernet Philipp Rink Sebastian Schornack
author_facet	Edouard Evangelisti Liron Shenhav Temur Yunusov Marie Le Naour–Vernet Philipp Rink Sebastian Schornack
author_sort	Edouard Evangelisti
title	Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
title_short	Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
title_full	Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
title_fullStr	Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
title_full_unstemmed	Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen
title_sort	hydrodynamic shape changes underpin nuclear rerouting in branched hyphae of an oomycete pathogen
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/128100fbf47a48d5ac92f29168ea374b
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_version_	1718427013568528384

Hydrodynamic Shape Changes Underpin Nuclear Rerouting in Branched Hyphae of an Oomycete Pathogen

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