Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores

Most pathogenic oomycetes of the genus <i>Phytophthora</i> spread in water films as flagellated zoospores. Zoospores perceive and produce signals attracting other zoospores, resulting in autoaggregation in vitro or biofilm formation on plant surface. The mechanisms underlying intercellul...

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Main Authors: Ilaria Bassani, Corinne Rancurel, Sophie Pagnotta, François Orange, Nicolas Pons, Kevin Lebrigand, Franck Panabières, Laurent Counillon, Xavier Noblin, Eric Galiana
Format: Article
Language:English
Published: MDPI AG 2020-07-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/7/1012
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spelling doaj-53f581f0e661459583e5471b9c6b5cf22020-11-25T03:12:41ZengMDPI AGMicroorganisms2076-26072020-07-0181012101210.3390/microorganisms8071012Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>ZoosporesIlaria Bassani0Corinne Rancurel1Sophie Pagnotta2François Orange3Nicolas Pons4Kevin Lebrigand5Franck Panabières6Laurent Counillon7Xavier Noblin8Eric Galiana9Université Côte d’Azur, INRAE, CNRS, ISA, 06903 Sophia Antipolis, FranceUniversité Côte d’Azur, INRAE, CNRS, ISA, 06903 Sophia Antipolis, FranceUniversité Côte d’Azur, Centre Commun de Microscopie Appliquée, 06108 Nice, FranceUniversité Côte d’Azur, Centre Commun de Microscopie Appliquée, 06108 Nice, FranceUniversité Côte d’Azur, CNRS, IPMC, 06560 Sophia Antipolis, FranceUniversité Côte d’Azur, CNRS, IPMC, 06560 Sophia Antipolis, FranceUniversité Côte d’Azur, INRAE, CNRS, ISA, 06903 Sophia Antipolis, FranceUniversité Côte d’Azur, CNRS, LP2M ,06107 Nice, FranceUniversité Côte d’Azur, CNRS UMR 7010, Institut de Physique de Nice, 06108 Nice, FranceUniversité Côte d’Azur, INRAE, CNRS, ISA, 06903 Sophia Antipolis, FranceMost pathogenic oomycetes of the genus <i>Phytophthora</i> spread in water films as flagellated zoospores. Zoospores perceive and produce signals attracting other zoospores, resulting in autoaggregation in vitro or biofilm formation on plant surface. The mechanisms underlying intercellular communication and consequent attraction, adhesion and aggregation are largely unknown. In <i>Phytophthora</i> <i>parasitica,</i> the perception of a K<sup>+</sup> gradient induces coordinated motion and aggregation. To define cellular and molecular events associated with oomycete aggregation, we combined transcriptomic and ultrastructural analyses. Results indicate involvement of electroception in K<sup>+</sup> sensing. They establish that the transcriptome repertoire required for swimming and aggregation is already fully functional at zoospore release. At the time points analyzed, aggregates are mainly constituted of zoospores. They produce vesicular and fibrillary material discharged at cell-to-cell contacts. Consistently, the signature of transcriptome dynamics during transition to aggregates is an upregulation of genes potentially related to vesicular trafficking. Moreover, transcriptomic and functional analyses show a strong enhancement of carbonic anhydrase activity, indicating that pH homeostasis may contribute to aggregation by acting on both zoospore movement and adhesion. This study poses the molecular and cellular bases of aggregative behavior within oomycetes and expands the current knowledge of ion perception-mediated dissemination of propagules in the rhizosphere.https://www.mdpi.com/2076-2607/8/7/1012aggregationoomycete<i>Phytophthora</i> zoosporespotassiumcarbonic anhydrase
collection DOAJ
language English
format Article
sources DOAJ
author Ilaria Bassani
Corinne Rancurel
Sophie Pagnotta
François Orange
Nicolas Pons
Kevin Lebrigand
Franck Panabières
Laurent Counillon
Xavier Noblin
Eric Galiana
spellingShingle Ilaria Bassani
Corinne Rancurel
Sophie Pagnotta
François Orange
Nicolas Pons
Kevin Lebrigand
Franck Panabières
Laurent Counillon
Xavier Noblin
Eric Galiana
Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
Microorganisms
aggregation
oomycete
<i>Phytophthora</i> zoospores
potassium
carbonic anhydrase
author_facet Ilaria Bassani
Corinne Rancurel
Sophie Pagnotta
François Orange
Nicolas Pons
Kevin Lebrigand
Franck Panabières
Laurent Counillon
Xavier Noblin
Eric Galiana
author_sort Ilaria Bassani
title Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
title_short Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
title_full Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
title_fullStr Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
title_full_unstemmed Transcriptomic and Ultrastructural Signatures of K<sup>+</sup>-Induced Aggregation in <i>Phytophthora parasitica </i>Zoospores
title_sort transcriptomic and ultrastructural signatures of k<sup>+</sup>-induced aggregation in <i>phytophthora parasitica </i>zoospores
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2020-07-01
description Most pathogenic oomycetes of the genus <i>Phytophthora</i> spread in water films as flagellated zoospores. Zoospores perceive and produce signals attracting other zoospores, resulting in autoaggregation in vitro or biofilm formation on plant surface. The mechanisms underlying intercellular communication and consequent attraction, adhesion and aggregation are largely unknown. In <i>Phytophthora</i> <i>parasitica,</i> the perception of a K<sup>+</sup> gradient induces coordinated motion and aggregation. To define cellular and molecular events associated with oomycete aggregation, we combined transcriptomic and ultrastructural analyses. Results indicate involvement of electroception in K<sup>+</sup> sensing. They establish that the transcriptome repertoire required for swimming and aggregation is already fully functional at zoospore release. At the time points analyzed, aggregates are mainly constituted of zoospores. They produce vesicular and fibrillary material discharged at cell-to-cell contacts. Consistently, the signature of transcriptome dynamics during transition to aggregates is an upregulation of genes potentially related to vesicular trafficking. Moreover, transcriptomic and functional analyses show a strong enhancement of carbonic anhydrase activity, indicating that pH homeostasis may contribute to aggregation by acting on both zoospore movement and adhesion. This study poses the molecular and cellular bases of aggregative behavior within oomycetes and expands the current knowledge of ion perception-mediated dissemination of propagules in the rhizosphere.
topic aggregation
oomycete
<i>Phytophthora</i> zoospores
potassium
carbonic anhydrase
url https://www.mdpi.com/2076-2607/8/7/1012
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