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Sterol-Sensing Domain (SSD)-Containing Proteins in Sterol Auxotrophic Phytophthora capsici Mediate Sterol Signaling and Play a Role in Asexual Reproduction and Pathogenicity

Authors :
Weizhen Wang
Zhaolin Xue
Linfang Xie
Xin Zhou
Fan Zhang
Sicong Zhang
Francine Govers
Xili Liu
Source :
Microbiology Spectrum 11 (2023) 1, Microbiology Spectrum, 11(1)
Publication Year :
2023
Publisher :
American Society for Microbiology, 2023.

Abstract

Phytophthora species are devastating filamentous plant pathogens that belong to oomycetes, a group of microorganisms similar to fungi in morphology but phylogenetically distinct. They are sterol auxotrophic, but nevertheless exploit exogenous sterols for growth and development. However, as for now the mechanisms underlying sterol utilization in Phytophthora are unknown. In this study, we identified four genes in Phytophthora capsici that encode proteins containing a sterol-sensing domain (SSD), a protein domain of around 180 amino acids comprising five transmembrane segments and known to feature in sterol signaling in animals. Using a modified CRISPR/Cas9 system, we successfully knocked out the four genes named PcSCP1 to PcSCP4 (for P. capsici SSD-containing protein 1 to 4), either individually or sequentially, thereby creating single, double, triple, and quadruple knockout transformants. Results showed that knocking out just one of the four PcSCPs was not sufficient to block sterol signaling. However, the quadruple “all-four” PcSCPs knockout transformants no longer responded to sterol treatment in asexual reproduction, in contrast to wild-type P. capsici that produced zoospores under sterol treatment. Apparently, the four PcSCPs play a key role in sterol signaling in P. capsici with functional redundancy. Transcriptome analysis indicated that the expression of a subset of genes is regulated by exogenous sterols via PcSCPs. Further investigations showed that sterols could stimulate zoospore differentiation via PcSCPs by controlling actin-mediated membrane trafficking. Moreover, the pathogenicity of the “all-four” PcSCPs knockout transformants was significantly decreased and many pathogenicity related genes were downregulated, implying that PcSCPs also contribute to plant-pathogen interaction.

Details

ISSN :
21650497
Volume :
11
Database :
OpenAIRE
Journal :
Microbiology Spectrum
Accession number :
edsair.doi.dedup.....1e67277ade480e19ddac4afe65433e66
Full Text :
https://doi.org/10.1128/spectrum.03797-22