Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction

BackgroundEndoreduplication, a modified cell cycle, involves cells duplicating DNA without undergoing mitosis. This phenomenon is frequently observed in plants, algae, and animals. Biotrophic pathogens have been demonstrated to induce endoreduplication in plants to secure more space or nutrients.Met...

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Main Authors: Michaela Hittorf, Andrea Garvetto, Marianne Magauer, Martin Kirchmair, Willibald Salvenmoser, Pedro Murúa, Sigrid Neuhauser
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1494905/full
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author Michaela Hittorf
Andrea Garvetto
Marianne Magauer
Martin Kirchmair
Willibald Salvenmoser
Pedro Murúa
Sigrid Neuhauser
author_facet Michaela Hittorf
Andrea Garvetto
Marianne Magauer
Martin Kirchmair
Willibald Salvenmoser
Pedro Murúa
Sigrid Neuhauser
author_sort Michaela Hittorf
collection DOAJ
description BackgroundEndoreduplication, a modified cell cycle, involves cells duplicating DNA without undergoing mitosis. This phenomenon is frequently observed in plants, algae, and animals. Biotrophic pathogens have been demonstrated to induce endoreduplication in plants to secure more space or nutrients.MethodsIn this study, we investigated the endoreduplication process triggered by two phylogenetically distant Rhizaria organisms—Maullinia spp. (in brown algae) and Plasmodiophora brassicae (in plants)—by combining fluorescent in situ hybridization (FISH) with nuclear area measurements.ResultsWe could confirm that Plasmodiophora brassicae (Plasmodiophorida) triggers endoreduplication in infected plants. For the first time, we also demonstrated pathogen-induced endoreduplication in brown algae infected with Maullinia ectocarpii and Maullinia braseltonii (Phagomyxida). We identified molecular signatures of endoreduplication in RNA-seq datasets of P. brassicae-infected Brassica oleracea and M. ectocarpii-infected Ectocarpus siliculosus.DiscussionCell cycle switch proteins such as CCS52A1 and B in plants, CCS52 in algae, and the protein kinase WEE1 in plants were upregulated in RNA-seq datasets hinting at a potential role in the phytomyxean-induced transition from mitotic cell cycle to endocycle. By demonstrating the consistent induction of endoreduplication in hosts during phytomyxid infections, our study expands our understanding of Phytomyxea–host interaction. The induction of this cellular mechanism by phytomyxid parasites in phylogenetically distant hosts further emphasizes the importance of endoreduplication in these biotrophic interactions.
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spelling doaj-art-1a13d0fd8f9341d7bd47b32bfcf080922025-02-05T07:32:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011510.3389/fmicb.2024.14949051494905Local endoreduplication of the host is a conserved process during Phytomyxea–host interactionMichaela Hittorf0Andrea Garvetto1Marianne Magauer2Martin Kirchmair3Willibald Salvenmoser4Pedro Murúa5Sigrid Neuhauser6Department of Microbiology, Universität Innsbruck, Innsbruck, AustriaDepartment of Microbiology, Universität Innsbruck, Innsbruck, AustriaDepartment of Botany, Universität Innsbruck, Innsbruck, AustriaDepartment of Microbiology, Universität Innsbruck, Innsbruck, AustriaDepartment of Zoology, Universität Innsbruck, Innsbruck, AustriaLaboratorio de Macroalgas y Ficopatología, Instituto de Acuicultura, Universidad Austral de Chile, Puerto Montt, ChileDepartment of Microbiology, Universität Innsbruck, Innsbruck, AustriaBackgroundEndoreduplication, a modified cell cycle, involves cells duplicating DNA without undergoing mitosis. This phenomenon is frequently observed in plants, algae, and animals. Biotrophic pathogens have been demonstrated to induce endoreduplication in plants to secure more space or nutrients.MethodsIn this study, we investigated the endoreduplication process triggered by two phylogenetically distant Rhizaria organisms—Maullinia spp. (in brown algae) and Plasmodiophora brassicae (in plants)—by combining fluorescent in situ hybridization (FISH) with nuclear area measurements.ResultsWe could confirm that Plasmodiophora brassicae (Plasmodiophorida) triggers endoreduplication in infected plants. For the first time, we also demonstrated pathogen-induced endoreduplication in brown algae infected with Maullinia ectocarpii and Maullinia braseltonii (Phagomyxida). We identified molecular signatures of endoreduplication in RNA-seq datasets of P. brassicae-infected Brassica oleracea and M. ectocarpii-infected Ectocarpus siliculosus.DiscussionCell cycle switch proteins such as CCS52A1 and B in plants, CCS52 in algae, and the protein kinase WEE1 in plants were upregulated in RNA-seq datasets hinting at a potential role in the phytomyxean-induced transition from mitotic cell cycle to endocycle. By demonstrating the consistent induction of endoreduplication in hosts during phytomyxid infections, our study expands our understanding of Phytomyxea–host interaction. The induction of this cellular mechanism by phytomyxid parasites in phylogenetically distant hosts further emphasizes the importance of endoreduplication in these biotrophic interactions.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1494905/fullendocyclePlasmodiophora brassicaeMaullinia ectocarpiibiotrophplant pathogen
spellingShingle Michaela Hittorf
Andrea Garvetto
Marianne Magauer
Martin Kirchmair
Willibald Salvenmoser
Pedro Murúa
Sigrid Neuhauser
Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
Frontiers in Microbiology
endocycle
Plasmodiophora brassicae
Maullinia ectocarpii
biotroph
plant pathogen
title Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
title_full Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
title_fullStr Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
title_full_unstemmed Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
title_short Local endoreduplication of the host is a conserved process during Phytomyxea–host interaction
title_sort local endoreduplication of the host is a conserved process during phytomyxea host interaction
topic endocycle
Plasmodiophora brassicae
Maullinia ectocarpii
biotroph
plant pathogen
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1494905/full
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