Identification of a C2H2 Transcription Factor (PsCZF3) Associated with RxLR Effectors and Carbohydrate-Active Enzymes in Phytophthora sojae Based on WGCNA

Abstract

Phytophthora sojae is a destructive soybean pathogen that orchestrates various secreted proteins (effectors) to modulate plant immunity and facilitate infection. Although a number of effectors have been identified and functionally studied in P. sojae, the way these molecules are regulated is marginally known. In this study, we performed a weighted gene correlation network analysis (WGCNA) based on digital RNA-seq, which enabled the identification of a transcription factor (PsCZF3) in P. sojae. This transcription factor is a C2H2-type zinc finger protein that regulates the transcription of 35 RxLR effectors during the early infection stage. Phylogenetic analysis revealed that PsCZF3 is a highly conserved protein across oomycetes, suggesting that this regulation mechanism may broadly exist in oomycete species. In addition, by building a subnetwork of PsCZF3 and correlated genes, we also found that PsCZF3 contributed to the transcriptional regulation of carbohydrate-active enzymes. Our findings suggest that the activation of PsCZF3 facilitates P. sojae infection by up-regulating RxLR effectors and carbohydrate-active enzymes.

Reference Genome Resource for the Citrus Pathogen Phytophthora citrophthora

“…to play an important role in the disease cycle of many Phytophthora species [20][21][22][23][24][25][26][27][28]. In total, 713 effectors were predicted for P. citrophthora STE-U-9442, of which 420 is cytoplasmic and 293 is apoplastic (File S2).…”

A MYB‐related transcription factor regulates effector gene expression in an oomycete pathogen

“…Other types of TFs were shown to regulate virulence, but whether they are also involved in effector gene expression still remains unknown, such as PsBZP32 (Sheng et al., 2021 ), PsMAD1 (Lin et al., 2018 ), and PsCZF1 (Wang et al., 2009 ). Importantly, a C2H2 TF, PsCZF3, was recently shown to be co‐expressed with 35 RxLR effector genes (Hu et al., 2022 ). It is regrettable that the authors did not further functionally verify the role of PsCZF3 in regulating the expression of effector genes encoding RxLRs.…”

“…These TFs regulate the development and/or pathogenicity of Phytophthora , but none of them have been shown to regulate effector gene expression. Interestingly, a recent weighted gene correlation network analysis (WGCNA) of P. sojae transcriptomes revealed a C2H2 zinc finger TF (PsCZF3) correlated with 35 RxLR effectors (Hu et al., 2022 ). Nevertheless, whether PsCZF3 could regulate the gene expression of these effectors remains to be determined.…”

“…Interestingly, a recent weighted gene correlation network analysis (WGCNA) of P. sojae transcriptomes revealed a C2H2 zinc finger TF (PsCZF3) correlated with 35 RxLR effectors (Hu et al, 2022).…”

An updated assessment of the soybean–Phytophthora sojae pathosystem

“…They identified 25 putative transcription factor (TF) binding sites within promoter regions and reported a positive correlation between transcript level and chromatin accessibility (Zhang, Lin, et al, 2022). Hu et al (2022) used digital RNA‐seq and weighted gene correlation network analysis to identify P . sojae TFs that potentially regulate effector expression during soybean infection.…”