Susceptibility factor RTP1 negatively regulates Phytophthora parasitica resistance via modulating UPR regulators bZIP60 and bZIP28

Abstract

The unfolded protein response (UPR) is a conserved stress adaptive signaling pathway in eukaryotic organisms activated by the accumulation of misfolded proteins in the endoplasmic reticulum (ER). UPR can be elicited in the course of plant defense, playing important roles in plant-microbe interactions. The major signaling pathways of plant UPR rely on the transcriptional activity of activated forms of ER membrane-associated stress sensors bZIP60 and bZIP28, which are transcription factors that modulate expression of UPR genes. In this study, we report the plant susceptibility factor RTP1 (Resistance to Phytophthora parasitica 1) is involved in ER stress sensing and rtp1-mediated resistance against P. parasitica is synergistically regulated with UPR, as demonstrated by the simultaneous strong induction of UPR and ER stress-associated immune genes in Arabidopsis thaliana rtp1 mutant plants during infection by P. parasitica. We further demonstrate RTP1 contributes to stabilization of the ER membrane-associated bZIP60 and bZIP28 through manipulating the bifunctional protein kinase/ribonuclease IRE1-mediated bZIP60 splicing activity and interacting with bZIP28. Consequently, we find rtp1bzip60 and rtp1bzip28 mutant plants exhibit compromised resistance accompanied with attenuated induction of ER stress-responsive immune genes and reduction of callose deposition in response to P. parasitica infection. Taken together, we demonstrate RTP1 may exert negative modulating roles in the activation of key UPR regulators bZIP60 and bZIP28, which are required for rtp1-mediated plant resistance to P. parasitica. This facilitates our understanding of the important roles of stress adaptive UPR and ER stress in plant immunity.

A plant receptor domain with functional analogies to animal malectin disables ER stress responses upon infection

“…In plants, infection with microbial pathogens frequently results in the onset of the UPR, which can in turn contribute to immune responses (Xu et al, 2019;Chakraborty et al, 2020) and programmed cell death, responses that aim at confining microbes and limiting the spreading of disease (Carvalho et al, 2014;Mishiba et al, 2013;Verchot and Pajerowska-Mukhtar, 2021). To countervail such responses, oomycete pathogens from the genus Phytophthora attenuate the UPR by secreting effectors into host cells that interact with ER stress-regulatory proteins (Jing et al, 2016;Fan et al, 2018;Qiang et al, 2021). However, the molecular mechanisms that connect biotic stress to the UPR and the plant immune system remain largely unknown.…”

Phytophthora infection signals‐induced translocation of NAC089 is required for endoplasmic reticulum stress response‐mediated plant immunity

“…Pseudomonas syringae was also reported to induce the elevated expression of UPR marker genes IRE1a and IRE1b upon infection (Gaguancela et al., 2016). RTP1 negatively modulates the activation of the key UPR regulators bZIP60 and bZIP28, which are required for rtp1 ‐mediated plant resistance to P. parasitica (Qiang et al., 2021). These findings highlight the important role of the UPR pathway in plant immunity.…”

“…Two NAC transcription factors with transmembrane region, NAC targeted by Phytophthora (NTP) 1 and NTP2 from potato, are also rapidly upregulated after CF treatment and translocated from the ER membrane to the nuclei (McLellan et al., 2013). In addition, RTP1 that modulates the activation of bZIP60 and bZIP28 was also found to negatively regulate gene expression involved in the PTI, such as the PTI marker genes MPK11 and CYP71A12 (Qiang et al., 2021).…”

“…PcAvr3a12 from P. capsici inhibits the ER‐localized FKBP15‐2 to mediate plant immunity (Fan et al., 2018). The plant susceptibility factor, Resistance to Phytophthora parasitica 1 (RTP1) negatively modulates the activation of the key UPR regulators bZIP60 and bZIP28, which are required for rtp1 ‐mediated plant resistance to P. parasitica (Qiang et al., 2021). Although these previous studies have provided a glimpse into the importance of such ER stress‐mediated plant immunity (ERSI) (Jing et al., 2016; Jing and Wang, 2020), our knowledge on how the ER stress pathway regulates plant immunity remains limited.…”

Cell Death Signaling From Endoplasmic Reticulum Stress: Plant-Specific and Conserved Features

“…Silencing NbbZIP17/28 significantly inhibited RSV infection. Likewise, the plant susceptibility factor Resistance to Phytophthora parasitica 1 (RTP1) has been recently shown to be involved in ER stress sensing (Qiang et al, 2021). RTP1 negatively modulates the IRE1/bZIP60 splicing activity and binds to bZIP28.…”