Setosphaeria turcica ATR turns off appressorium‐mediated maize infection and triggers melanin‐involved self‐protection in response to genotoxic stress

Abstract

Eukaryotic organisms activate conserved signalling networks to maintain genomic stability in response to DNA genotoxic stresses. However, the coordination of this response pathway in fungal pathogens remains largely unknown. In the present study, we investigated the mechanism by which the northern corn leaf blight pathogen Setosphaeria turcica controls maize infection and activates self‐protection pathways in response to DNA genotoxic insults. Appressorium‐mediated maize infection by S. turcica was blocked by the S‐phase checkpoint. This repression was dependent on the checkpoint central kinase Ataxia Telangiectasia and Rad3 related (ATR), as inhibition of ATR activity or knockdown of the ATR gene recovered appressorium formation in the presence of genotoxic reagents. ATR promoted melanin biosynthesis in S. turcica as a defence response to stress. The melanin biosynthesis genes StPKS and StLac2 were induced by the ATR‐mediated S‐phase checkpoint. The responses to DNA genotoxic stress were conserved in a wide range of phytopathogenic fungi, including Cochliobolus heterostrophus, Cochliobolus carbonum, Alternaria solani, and Alternaria kikuchiana, which are known causal agents for plant diseases. We propose that in response to genotoxic stress, phytopathogenic fungi including S. turcica activate an ATR‐dependent pathway to suppress appressorium‐mediated infection and induce melanin‐related self‐protection in addition to conserved responses in eukaryotes.

Novel factors contributing to fungal pathogenicity at early stages of Setosphaeria turcica infection

“…We have previously shown that the plant fungal pathogen S. turcica has evolved the capacity to breach the intact cuticle of the plant host by elaborating a specialized structure called the appressorium (Gu et al, 2014 ; Zhang et al, 2012 ). Expression of pathogenicity‐related genes is often coupled to appressorium development (Gu et al, 2014 ; Zeng et al, 2020 ; Zhang et al, 2012 ). We therefore performed transcriptome analysis of S. turcica during appressorium development to identify crucial genes that may play essential roles in fungal pathogenicity.…”

“…Maize lesions and appressorium development on leaves were observed using a plant infection assay, as described previously, with minor modifications (Ma et al, 2018;Zeng et al, 2020).…”

“…To initiate appressorium development, the fungus responds to a set of inductive cues, including surface hardness, hydrophobicity, cuticular wax, and the absence of exogenous nutrients (Ebbole, 2007 ; Ryder & Talbot, 2015 ). We have previously demonstrated that cAMP and protein kinase A signalling pathway, a mitogen‐activated protein kinase pathway, and an ATR (Ataxia Telangiectasia and Rad3 related)‐mediated S‐phase checkpoint are necessary for efficient appressorium morphogenesis and the subsequent invasive growth of S. turcica in response to environmental signals or stresses (Gong et al, 2017 ; Shen et al, 2013 ; Zeng et al, 2020 ). However, essential S. turcica factors that couple appressorium formation to the ensuing pathogenicity are still largely unknown.…”

“…The AvrHt1 gene was mapped to a hybrid PKS‐NRPS gene #179218 in the Et28A‐v1.0 genome (Mideros et al, 2018 ). Several signalling pathways regulating cell development and pathogenicity in S. turcica have been reported in the last decade (Gong et al, 2017 ; Gu et al, 2014 ; Shen et al, 2013 ; Zeng et al, 2020 ). Septins have been found to be required for conidia formation and virulence in the closely related maize pathogen Cochliobolus heterostrophus (Zhang et al, 2020 ).…”

Yeast surface displayed xylanase is an efficient strategy to induce corn defence response

“…embl-heidelberg.de/) were used to analyze the conserved domain of the S. turcica xylanase GH11 family genes. And the software IBS (http://ibs.biocuckoo.org/) was used to draw the conserved domain following the procedures described previously [16].…”