MoIug4 is a novel secreted effector promoting rice blast by counteracting host OsAHL1‐regulated ethylene gene transcription

Abstract

Summary Magnaporthe oryzae secretes several effectors that modulate and hijack rice processes to colonize host cells, but the underlying mechanisms remain unclear. We report on a novel cytoplasmic effector MoIug4 that targets the rice ethylene pathway as a transcription repressor to subvert host immunity. We found that MoIug4 binds to the promoter of the host OsEIN2 gene that encodes a central signal transducer in the ethylene‐signaling pathway. We also identified a MoIug4 interacting protein, OsAHL1, which acts as an AT‐hook motif‐containing protein binding to the A/T‐rich promoter regions. Our knockout and overexpression studies showed that OsAHL1 positively regulates plant immunity in response to M. oryzae infection. OsAHL1 exhibits transcriptional regulatory activities by binding the OsEIN2 promoter region, similar to MoIug4. Intriguingly, we found that MoIug4 exhibits a higher binding affinity than OsAHL1 to the OsEIN2 promoter, suggesting differential regulatory specificities. These results revealed a counter‐defense strategy by which the pathogen effector suppresses the activation of host defense genes by interfering with host transcription activator functions.

Novel stripe rust effector boosts the transcription of a host susceptibility factor through affecting histone modification to promote infection in wheat

“…Chromatin immunoprecipitation (ChIP) was performed as described previously with some modifications (Sharma et al ., 2019; X. Y. Liu et al ., 2022). The second leaf samples (3 g) from Fielder and transgenic wheat seedlings overexpressing PstGTA1 were cut into 50‐ml conical tubes and 1% (v/v) formaldehyde was used for in vitro cross‐linking for 15 min in vacuum.…”

“…For example, the oomycete pathogen Hyaloperonospora arabidopsidis delivers HaRxLL470, a conserved RxLR effector, which attenuates the DNA‐binding activity of HY5, a host transcription factor regulating photomorphogenesis and innate immunity, thereby enhancing the plant's susceptibility to the pathogen (Chen et al ., 2021). Similarly, the fungal effector MoIug4 secreted by Magnaporthe oryzae was shown to suppress the expression of the ethylene signaling pathway component OsEIN2 in rice by binding to the promoter element of OsEIN2 , preventing binding of its transcriptional activator OsAHL1 (X. Y. Liu et al ., 2022). These studies suggest that host transcriptional reprogramming is a significant target for pathogen effectors.…”

Effector‐triggered susceptibility by the rice blast fungus Magnaporthe oryzae

“…Kim et al, 2013), PsAvh238 of Phytophthora sojae (Yang et al, 2019), SsERP1 of Sclerotinia sclerotiorum (Fan et al, 2021), and the Jsi1 effector of Ustilago maydis (Darino et al, 2021). In M. oryzae, the cytoplasmic effector Iug4 (M. oryzae isolate-unique gene 4) acts as a transcriptional repressor to target the ethylene pathway, via OsAHL1, to disrupt host immunity (Liu et al, 2022;Fig. 4).…”

“…The ability to manipulate and reprogram host plant cell signaling and metabolism is a hallmark of biotrophic pathogens (Oliveira‐Garcia & Valent, 2015; Presti et al ., 2015; Uhse & Djamei, 2018). Effectors of M. oryzae can act in specific host cell compartments, such as chloroplasts, nuclei, or ER, to reprogram host metabolism and promote biotrophic growth (Khang et al ., 2010; Kim et al ., 2020; Liu et al ., 2022; Ning et al ., 2022). This is the case, for example, with the peroxisome‐targeted effector protein Ptep1, which localizes to plant peroxisomes and is required for infection (Ning et al ., 2022).…”

“…Specifically, MoIug4 binds to the promoter of rice OsEIN2 which encodes a central signal transducer in ethylene signaling. Moreover, MoIug4 interacting protein, OsAHL1, acts as an AT‐hook motif‐containing protein binding to the A/T‐rich promoter regions and positively regulates plant immunity in response to M. oryzae infection (Liu et al ., 2022). Both MoIug4 and OsAHL1 possess transcriptional regulatory activities by binding the OsEIN2 promoter region (Fig.…”