Anthracnose, caused by
Colletotrichum
species, induces significant economic damages to crop plants annually, especially for
Camellia oleifera
. During infection, the counter-defence mechanisms of plant pathogens against ROS-mediated resistance, however, remain poorly understood. By employing Weighted Gene Co-expression Network Analysis (WGCNA), we identified ACTIVATOR PROTEIN-1 (AP-1), a bZIP transcription factor, as significant to infection. And deletion of
CfAP1
inhibited aerial hyphae formation and growth under oxidative stress. Furthermore, RNA-seq analysis post H
2
O
2
treatment revealed 33 significantly down-regulated genes in the AP-1 deficient strain, including A12032, a dual specificity phosphatase (DSP) homologous to MSG5 from
Saccharomyces cerevisiae
. This Δ
Cfmsg5
strain showed enhanced oxidative tolerance, reduced ROS scavenging, and negative regulation of the CWI MAPK cascade under oxygen stress, suggesting its involvement in oxidative signal transduction. Importantly, we provide evidence that CfMsg5 regulates growth, endoplasmic reticulum stress, and several unfolded protein response genes upregulated in Δ
Cfmsg5
. Collectively, this study identified core components during
C. fructicola
infection and highlights a potential regulatory module involving CfAp1 and CfMsg5 in response to host ROS bursts. It provides new insights into fungal infection mechanisms and potential targets like
CfAP1
and
CfMSG5
for managing anthracnose diseases.