Oomycete pathogens secrete host cell-entering effector proteins to manipulate host immunity during infection. We previously showed that PsAvh52, an early-induced RxLR effector secreted from the soybean root rot pathogen, Phytophthora sojae, could suppress plant immunity. Here, we found that PsAvh52 is required for full virulence on soybean and binds to a novel soybean transacetylase, GmTAP1, in vivo and in vitro. PsAvh52 could cause GmTAP1 to relocate into the nucleus where GmTAP1 could acetylate histones H2A and H3 during early infection, thereby promoting susceptibility to P. sojae. In the absence of PsAvh52, GmTAP1 remained confined to the cytoplasm and did not modify plant susceptibility. These results demonstrate that GmTAP1 is a susceptibility factor that is hijacked by PsAvh52 in order to promote epigenetic modifications that enhance the susceptibility of soybean to P. sojae infection.

RXLR effectors, a class of secreted proteins that are transferred into host cells to manipulate host immunity, have been reported to widely exist in oomycetes, including those from genera Phytophthora, Hyaloperonospora, Albugo, and Saprolegnia. However, in Pythium species, no RXLR effector has yet been characterized, and the origin and evolution of such virulent effectors are still unknown. Here, we developed a modified regular expression method for de novo identification of RXLRs and characterized 359 putative RXLR effectors in nine Pythium species. Phylogenetic analysis revealed that all oomycetous RXLRs formed a single superfamily, suggesting that they might have a common ancestor. RXLR effectors from Pythium and Phytophthora species exhibited similar sequence features, protein structures, and genome locations. In particular, there were significantly more RXLR proteins in the mosquito biological control agent P. guiyangense than in the other eight Pythium species, and P. guiyangense RXLRs might be the result of gene duplication and genome rearrangement events, as indicated by synteny analysis. Expression pattern analysis of RXLR-encoding genes in the plant pathogen P. ultimum detected transcripts of the majority of the predicted RXLR genes, with some RXLR effectors induced in infection stages and one RXLR showing necrosis-inducing activity. Furthermore, all predicted RXLR genes were cloned from two biocontrol agents, P. oligandrum and P. periplocum, and three of the RXLR genes were found to induce a defense response in Nicotiana benthamiana. Taken together, our findings represent the first evidence of RXLR effectors in Pythium species, providing valuable information on their evolutionary patterns and the mechanisms of their interactions with diverse hosts.

RNA-binding proteins (RBPs) participate in a diverse set of biological processes in plants, but their functions and underlying mechanisms in plant–pathogen interactions are largely unknown. We previously showed that Arabidopsis thaliana BPA1-LIKE PROTEIN3 (BPL3) belongs to a conserved plant RBP family and negatively regulates reactive oxygen species (ROS) accumulation and cell death under biotic stress. In this study, we demonstrate that BPL3 suppresses FORKED-LIKE7 (FL7) transcript accumulation and raises levels of the cis-natural antisense long non-coding RNA (lncRNA) of FL7 (nalncFL7). FL7 positively regulated plant immunity to Phytophthora capsici while nalncFL7 negatively regulated resistance. We also showed that BPL3 directly binds to and stabilizes nalncFL7. Moreover, nalncFL7 suppressed accumulation of FL7 transcripts. Furthermore, FL7 interacted with HIGHLY ABA-INDUCED PP2C1 (HAI1), a type 2C protein phosphatase, and inhibited HAI1 phosphatase activity. By suppressing HAI1 activity, FL7 increased the phosphorylation levels of MITOGEN-ACTIVATED PROTEIN KINASE 3 (MPK3) and MPK6, thus enhancing immunity responses. BPL3 and FL7 are conserved in all plant species tested, but the BPL3–nalncFL7–FL7 cascade was specific to the Brassicaceae. Thus, we identified a conserved BPL3–nalncFL7–FL7 cascade that coordinates plant immunity.