Genome dynamics of pathogenic organisms are driven by pathogen and host co-evolution, in which pathogen genomes are shaped to overcome stresses imposed by hosts with various genetic backgrounds through generation of a variety of isolates. This same principle applies to the rice blast pathogen Magnaporthe oryzae and the rice host; however, genetic variations among different isolates of M. oryzae remain largely unknown, particularly at genome and transcriptome levels. Here, we applied genomic and transcriptomic analytical tools to investigate M. oryzae isolate 98-06 that is the most aggressive in infection of susceptible rice cultivars. A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15. Genome-wide expression profiling revealed the presence of two critical expression patterns of M. oryzae based on 64 known pathogenicity-related (PaR) genes. In addition, 134 candidate effectors with various segregation patterns were identified. Five tested proteins could suppress BAX-mediated programmed cell death in Nicotiana benthamiana leaves. Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity. Moreover, Iug6 and Iug9 are located exclusively in the biotrophic interfacial complex (BIC) and their overexpression leads to suppression of defense-related gene expression in rice, suggesting that they might participate in biotrophy by inhibiting the SA and ET pathways within the host. Thus, our studies identify novel effector and PaR proteins involved in pathogenicity of the highly aggressive M. oryzae field isolate 98-06, and reveal molecular and genomic dynamics in the evolution of M. oryzae and rice host interactions.

Reactive oxygen species (ROS) play a vital role in plant immune response, but the genes involved in the regulation of ROS are scantily reported. Phytophthora pathogens produce a large number of effectors to promote infection, but the modes of action adopted are largely unknown. Here, we report that RxLR207 could activate ROS-mediated cell death in Nicotiana benthamiana and was essential for virulence of P. capsici. We found that this effector targeted BPA1 (binding partner of ACD11) and four members of BPLs (BPA1-Like proteins) in Arabidopsis, and the bpa1 and bpl mutants had enhanced ROS accumulation and cell death under biotic or abiotic stresses. Furthermore, we showed that BPA1 and several BPLs functioned redundantly in plant immunity to P. capsici. We discovered that BPA1 and all six BPLs interacted with ACD11, and stabilization of ACD11 was impaired in the bpa1, bpl2, bpl3, and bpl4 mutants. RxLR207 could promote the degradation of BPA1, BPL1, BPL2, and BPL4 to disrupt ACD11 stabilization in a 26S proteasome-dependent manner. Taken together, these findings indicate the important roles of Arabidopsis BPA1 and its homologs in ROS homeostasis and defense response, highlighting the usefulness of a pathogen effector-directed approach as a promising strategy for the discovery of novel plant immune regulators.

Phytophthora pathogens secrete an array of specific effector proteins to manipulate host innate immunity to promote pathogen colonization. However, little is known about the host targets of effectors and the specific mechanisms by which effectors increase susceptibility. Here we report that the soybean pathogen Phytophthora sojae uses an essential effector PsAvh262 to stabilize endoplasmic reticulum (ER)-luminal binding immunoglobulin proteins (BiPs), which act as negative regulators of plant resistance to Phytophthora. By stabilizing BiPs, PsAvh262 suppresses ER stress-triggered cell death and facilitates Phytophthora infection. The direct targeting of ER stress regulators may represent a common mechanism of host manipulation by microbes.