Phase-specific transcriptional patterns of the oomycete pathogen Phytophthora sojae unravel genes essential for asexual development and pathogenic processes

Author summaryOomycetes are fungi-like microorganisms with differences in biology and genetics. Using fungicides to control the pathogenic oomycetes has limited effectiveness. Therefore, a detailed understanding of the oomycetes is necessary for identifying potential candidates as fungicide targets. The present study investigated the transcriptional changes in a model oomycete pathogen, Phytophthora sojae, during asexual development and plant infection. The analysis identified various types of genes with differences in expression patterns during development and infection. Further analysis focused on the transcriptome dynamics during asexual stages which exhibited more remarkable plasticity. Detailed analysis of the genes revealed stage-specific responses of a few genes and specifically identified three genes with functional relevance in different developmental stages of P. sojae, including a serine/threonine phosphatase in mycelial and sporangium stages, a histidine kinase in zoospore and cyst stages, and a bZIP transcription factor in cyst germination. Also these three genes function in different participate in multiple layers of the pathogenicity process. Thus, the study provides a reference for further research on the candidate genes, which may be used to defeat the pathogenic oomycetes. Oomycetes are filamentous microorganisms easily mistaken as fungi but vastly differ in physiology, biochemistry, and genetics. This commonly-held misconception lead to a reduced effectiveness by using conventional fungicides to control oomycetes, thus it demands the identification of novel functional genes as target for precisely design oomycetes-specific microbicide. The present study initially analyzed the available transcriptome data of the model oomycete pathogen, Phytophthora sojae, and constructed an expression matrix of 10,953 genes across the stages of asexual development and host infection. Hierarchical clustering, specificity, and diversity analyses revealed a more pronounced transcriptional plasticity during the stages of asexual development than that in host infection, which drew our attention by particularly focusing on transcripts in asexual development stage to eventually clustered them into 6 phase-specific expression modules. Three of which respectively possessing a serine/threonine phosphatase (PP2C) expressed during the mycelial and sporangium stages, a histidine kinase (HK) expressed during the zoospore and cyst stages, and a bZIP transcription factor (bZIP32) exclusive to the cyst germination stage were selected for down-stream functional validation. In this way, we demonstrated that PP2C, HK, and bZIP32 play significant roles in P. sojae asexual development and virulence. Thus, these findings provide a foundation for further gene functional annotation in oomycetes and crop disease management.

Automated summary

This study analyzed the transcriptomic changes in Phytophthora sojae during asexual development and host infection. Various types of genes with expression pattern differences were identified. The transcriptome dynamics during asexual stages showed higher plasticity. Three genes with functional relevance in different developmental stages were identified and shown to play significant roles in pathogenicity. These findings contribute to further gene functional annotation and crop disease management in oomycetes.