Shedding light on autophagy coordinating with cell wall integrity signaling to govern pathogenicity of Magnaporthe oryzae

Abstract

Cells are faced with various stresses during their growth and development, and autophagy is a degradative process in which cells can break down their own components to recycle macromolecules and provide energy under these stresses. For pathogenic fungi that utilize cell wall as the first barrier against external stress, the cell wall integrity (CWI) pathway also provides an essential role in responding to these stresses. However, the specific connection between autophagy and CWI remains elusive in either the model fungi including budding yeast Saccharomyces cerevisiae or the rice blast fungus Magnaporthe oryzae. Here, we provided evidence that the endoplasmic reticulum (ER) stress is highly induced during M. oryzae infection and that CWI MAP kinase kinase MoMkk1 (S. cerevisiae Mkk1/2 homolog) was subject to phosphorylation regulation by MoAtg1, the only identified kinase in the core autophagy machinery. We also identified MoMkk1 serine 115 as the MoAtg1dependent phosphorylation site and this phosphorylation could activate CWI, similar to that by the conserved MAP kinase kinase kinase MoMck1 (S. cerevisiae Bck1 homolog). Together with the first report of MoMkk1 subjects to phosphorylation regulation by MoAtg1, we revealed a new mechanism by which autophagy coordinates with CWI signaling under ER stress, and this MoAtg1-dependent MoMkk1 phosphorylation is essential for the pathogenicity of M. oryzae.

UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens

“…Autophagy is known to be related to several stress responses (Yin et al 2019). However, it remains unclear whether UvATG8 regulates stress responses of U. virens.…”

Endoplasmic reticulum‐associated degradation mediated by MoHrd1 and MoDer1 is pivotal for appressorium development and pathogenicity of Magnaporthe oryzae

“…Our previous study revealed that M. oryzae suffers additional ER stress when it switches from vegetative growth to asexual reproduction (Tang et al, 2015). Recently, Yin et al reported the presence of ER stress during M. oryzae infection (Yin et al, 2020). These data indicated that M. oryzae had to adapt to ER stress changes during fungal development.…”

“…Recently, Yin et al reported that DTT imposed ER stress induces autophagy in M. oryzae (Yin et al, 2020).…”

Balancing of the mitotic exit network and cell wall integrity signaling governs the development and pathogenicity in Magnaporthe oryzae

“…We previously found that MoMkk1 also mediates crosstalk between the CWI pathway and other pathways, including the unfolded protein response (UPR) pathway, the high osmolality glycerol (HOG) MAPK pathway, and autophagy [ 10 ]. We demonstrated that the autophagy-related kinase MoAtg1 phosphorylates MoMkk1 under ER stress [ 16 ]. By identifying the cell cycle-related kinase MoSep1 that phosphorylates MoMkk1 to enhance the CWI activity, we revealed the complex and multitude of signaling pathway crosstalk surrounding CWI.…”

“…oryzae , the MAP kinase pathway is composed of MoMck1 (the Bck1 homolog), MoMkk1 (the Mkk1/2 homolog), and MoMps1 (the Mpk1/Slt2 homolog) that play an essential role in aerial hyphae morphogenesis, appressorium formation, and pathogenicity [ 10 , 14 – 15 ]. In addition, recent studies have found that other kinases, such as autophagy-related MoAtg1, could also phosphorylate MoMkk1 in response to the endoplasmic reticulum (ER) stress [ 16 ]. This study suggested the importance and the multitude of regulatory mechanisms by CWI signaling.…”