The Basic Leucine Zipper Transcription Factor PlBZP32 Associated with the Oxidative Stress Response Is Critical for Pathogenicity of the Lychee Downy Blight Oomycete Peronophythora litchii

Abstract

Basic leucine zipper (bZIP) transcription factors are widespread in eukaryotes, including plants, animals, fungi, and oomycetes. However, the functions of bZIPs in oomycetes are rarely known. In this study, we identified a bZIP protein possessing a special bZIP-PAS structure in Peronophythora litchii, named PlBZP32. We found that PlBZP32 is upregulated in zoospores, in cysts, and during invasive hyphal growth. We studied the functions of PlBZP32 using the RNAi technique to suppress the expression of this gene. PlBZP32-silenced mutants were more sensitive to oxidative stress, showed a lower cyst germination rate, and produced more sporangia than the wild-type strain SHS3. The PlBZP32-silenced mutants were also less invasive on the host plant. Furthermore, we analyzed the activities of extracellular peroxidases and laccases and found that silencing PlBZP32 decreased the activities of P. litchii peroxidase and laccase. To our knowledge, this is the first report that the functions of a bZIP-PAS protein are associated with oxidative stress, asexual development, and pathogenicity in oomycetes. IMPORTANCE In this study, we utilized the RNAi technique to investigate the functions of PlBZP32, which possesses a basic leucine zipper (bZIP)-PAS structure, and provided insights into the contributions of bZIP transcription factors to oxidative stress, the production of sporangia, the germination of cysts, and the pathogenicity of Peronophythora litchii. This study also revealed the role of PlBZP32 in regulating the enzymatic activities of extracellular peroxidases and laccases in the plant-pathogenic oomycete.

The bZIP transcription factor PsBZP32 is involved in cyst germination, oxidative stress response, and pathogenicity of Phytophthora sojae

“…According to our bioinformatics analysis, this bZIP-PAS protein is conserved and specific to Stramenopila. In this study and a recent study, the gene silencing assays indicated that the bZIP-PAS protein PsBZP32 plays a key role in the cyst germination, oxidative stress response, and pathogenicity of P. sojae, while PlBZP32 in Peronophythora litchii has similar biological functions (Kong et al 2020). Therefore, the bZIP-PAS proteins may have conserved functions in oomycete plant pathogens.…”

“…In Pe. litchii, PlBZP32 can regulate the activities of extracellular peroxidases and laccases (Kong et al 2020), and the heat shock TF PsHSF1 in P. sojae also has these functions (Sheng et al 2015). However, silencing of PsBZP32 did not attenuate extracellular peroxidase and laccase activities.…”

“…In Pe. litchii, the researchers also failed to knock out PlBZP32 (Kong et al 2020). In addition, we generated PsBZP32-overexpressing transformants, but they showed only 1.5-to-3-fold expression levels and no different phenotype compared with WT.…”

“…Considering that gene silencing might cause off-target effects, we confirmed that the transformed antisense sequence of PsBZP32 had no potential target (> 21 bp identical sequence) in P. sojae genome based on bioinformatics analysis, and in Pe. litchii, PlBZP32-silencing did not affect the expression of the neighboring gene Pl105397 (Kong et al 2020). However, due to the technical limitations on BZP32 knockout (and complementation), the accurate biological functions of these proteins still demand further investigation.…”

The Mitogen-Activated Protein Kinase PlMAPK2 Is Involved in Zoosporogenesis and Pathogenicity of Peronophythoralitchii

“…For example, Phytophthora infestans, Phytophthora capsici, Phytophthora sojae and Peronophythora litchii severely damage potato, soybean, cucurbits and lychee, respectively [3,4]. Among them, lychee downy blight caused by P. litchii is the most destructive disease of lychee and results in crop losses ranging from 30% to 80% annually [5].…”