An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity
Citation
Huang, J., Gu, L., Zhang, Y., Yan, T., Kong, G., Kong, L., Guo, B., Qiu, M., Wang, Y., Jing, M., Xing, W., Ye, W., Wu, Z., Zhang, Z., Zheng, X., Gijzen, M., Wang, Y., Dong, S. (2017). An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nature Communications, [online] 8(1), http://dx.doi.org/10.1038/s41467-017-02233-5
Plain language summary
The plant pathogen Phytophthora sojae causes root and stem rot of soybean. Resistance to Phytophthora sojae in soybean is controlled by Rps genes. Soybean Rps genes encode for products that interact with pathogen virulence factors (encoded by Avr genes) and trigger immune responses that stop pathogen growth. However, new strains of the pathogen that escape Rps mediated immunity and cause disease arise over time. Our past work showed that the P. sojae gene Avr3a encodes a small secreted protein that triggers immunity on soybean plants carrying the Rps3a gene. We now show that Avr3a works as a virulence factor by interfering with soybean RNA processing systems. When DNA is transcribed into mRNA, the initial mRNA molecule (called the pre-mRNA) must often be spliced into new forms by protein complexes. Our experiments suggest that the pathogen Avr3a protein targets these host pre-mRNA splicing complexes and alters the processing outcomes. Specifically, we have identified a new soybean protein, GmSKRP (Glycine max serine, lysine, and arginine rich protein) that interacts with Avr3a and is important for proper pre-mRNA splicing in soybean. The results illustrate how a pathogen virulence factor can upset basic host operating systems.
Abstract
The process of RNA splicing influences many physiological processes, including plant immunity. However, how plant parasites manipulate host RNA splicing process remains unknown. Here we demonstrate that PsAvr3c, an avirulence effector from oomycete plant pathogen Phytophthora sojae, physically binds to and stabilizes soybean serine/lysine/arginine-rich proteins GmSKRPs. The SKRPs are novel proteins that associate with a complex that contains plant spliceosome components, and are negative regulators of plant immunity. Analysis by RNA-seq data indicates that alternative splicing of pre-mRNAs from 401 soybean genes, including defense-related genes, is altered in GmSKRP1 and PsAvr3c overexpressing lines compared to control plants. Representative splicing events mediated by GmSKRP1 and PsAvr3c are tested by infection assays or by transient expression in soybean plants. Our results show that plant pathogen effectors can reprogram host pre-mRNA splicing to promote disease, and we propose that pathogens evolved such strategies to defeat host immune systems.