Global Expression Profiling of Transcription Factor Genes Provides New Insights into Pathogenicity and Stress Responses in the Rice Blast Fungus

Abstract

Because most efforts to understand the molecular mechanisms underpinning fungal pathogenicity have focused on studying the function and role of individual genes, relatively little is known about how transcriptional machineries globally regulate and coordinate the expression of a large group of genes involved in pathogenesis. Using quantitative real-time PCR, we analyzed the expression patterns of 206 transcription factor (TF) genes in the rice blast fungus Magnaporthe oryzae under 32 conditions, including multiple infection-related developmental stages and various abiotic stresses. The resulting data, which are publicly available via an online platform, provided new insights into how these TFs are regulated and potentially work together to control cellular responses to a diverse array of stimuli. High degrees of differential TF expression were observed under the conditions tested. More than 50% of the 206 TF genes were up-regulated during conidiation and/or in conidia. Mutations in ten conidiation-specific TF genes caused defects in conidiation. Expression patterns in planta were similar to those under oxidative stress conditions. Mutants of in planta inducible genes not only exhibited sensitive to oxidative stress but also failed to infect rice. These experimental validations clearly demonstrated the value of TF expression patterns in predicting the function of individual TF genes. The regulatory network of TF genes revealed by this study provides a solid foundation for elucidating how M. oryzae regulates its pathogenesis, development, and stress responses.

Author Summary

Rice blast disease, caused by Magnaporthe oryzae, destroys rice crop enough to feed 60 million people every year and has served as a model pathosystem for understanding host-parasite interactions. However, little is known about how M. oryzae globally regulates and coordinates its gene expression at the whole-genome scale. We analyzed the expression patterns of 206 M. oryzae genes encoding transcription factors (TFs) under 32 conditions, including infection-related developmental stages and various abiotic stresses, using quantitative real-time PCR. We focused on identifying the TF genes that are induced during the two most important infection-related morphogenetic changes; conidiation and infectious growth in rice. We identified 57 conidiation-specific TF genes and functionally characterized ten of them. Our data also showed that infectious growth in planta and oxidative stress responses in vitro involve largely overlapping groups of TFs. Comprehensive TF expression data and functional validation provided new insights into the regulatory mechanism underpinning pathogenicity and stress responses in M. oryzae. These data will also serve as a guide in studying the role of individual TF genes and the coordination of their expression in controlling development, pathogenicity, and abiotic stress responses in M. oryzae.