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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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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