Abstract
Most pathogenic oomycetes of the genus Phytophthora 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 Phytophthora parasitica, the perception of a K+ 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+ 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.
Highlights
Oomycetes constitute a diverse group of eukaryotic microorganisms growing as filamentous coenocytic hyphae, reproducing both sexually and asexually and belonging, together with diatoms and brown algae, to the Stramenopiles [1]
To further define cellular and molecular mechanisms implied in aggregation, K+ gradients were applied in vitro to freely swimming P. parasitica zoospores
As previously observed by Galiana et al (2019) [7], most of cells showed anticlockwise rotation movement or a short and erratic displacement indicative of the presence of flagella at that time point (Figure S1B and Video S2)
Summary
Oomycetes constitute a diverse group of eukaryotic microorganisms growing as filamentous coenocytic hyphae, reproducing both sexually and asexually and belonging, together with diatoms and brown algae, to the Stramenopiles [1]. Unicellular, biflagellate zoospores explore their environment and use sensory systems for the detection of stimuli such as chemical gradients (chemotaxis) and ionic fields (electrotaxis) [4]. They move towards the host plant and adhere to its surface to initiate infection. Once a small number of zoospores has reached the host surface, they produce signals that attract hundreds of individuals, resulting in biofilm formation of encysted spores [5,7]. Little is known about how zoospores communicate, coordinate their behavior and constitute an inoculum on the host, as studies have investigated this process at the multicellular level only recently [10,11]
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