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GCN4 Regulates Secondary Metabolism through Activation of Antioxidant Gene Expression under Nitrogen Limitation Conditions in Ganoderma lucidum.

ABSTRACT: Nitrogen limitation has been widely reported to affect the growth and development of fungi, and the transcription factor GCN4 (general control nonderepressible 4) is involved in nitrogen restriction. Here, we found that nitrogen limitation highly induced the expression of GCN4 and promoted the synthesis of ganoderic acid (GA), an important secondary metabolite in Ganoderma lucidum. The activated GCN4 is involved in regulating GA biosynthesis. In addition, the accumulation of reactive oxygen species (ROS) also affects the synthesis of GA under nitrogen restrictions. The silencing of the gcn4 gene led to further accumulation of ROS and increased the content of GA. Further studies found that GCN4 activated the transcription of antioxidant enzyme biosynthesis genes gr, gst2, and cat3 (encoding glutathione reductase, glutathione S-transferase, and catalase, respectively) through direct binding to the promoter of these genes to reduce the ROS accumulation. In conclusion, our study found that GCN4 directly interacts with the ROS signaling pathway to negatively regulate GA biosynthesis under nitrogen-limiting conditions. This provides an essential insight into the understanding of GCN4 transcriptional regulation of the ROS signaling pathway and enriches the knowledge of nitrogen regulation mechanisms in fungal secondary metabolism of G. lucidum. IMPORTANCE Nitrogen has been widely reported to regulate secondary metabolism in fungi. Our study assessed the specific nitrogen regulatory mechanisms in Ganoderma lucidum. We found that GCN4 directly interacts with the ROS signaling pathway to negatively regulate GA biosynthesis under nitrogen-limiting conditions. Our research highlights a novel insight that GCN4, the nitrogen utilization regulator, participates in secondary metabolism through ROS signal regulation. In addition, this also provides a theoretical foundation for exploring the regulation of other physiological processes by GCN4 through ROS in fungi.

SUBMITTER: Lian L

PROVIDER: S-EPMC8231712 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Fungi actively alter their metabolic and synthetic pathways to cope with changing environmental conditions. The mitochondrial pyruvate carrier (MPC) plays a vital role in transporting pyruvate into mitochondria and regulating carbon metabolic homeostasis. However, the mechanism by which MPC regulates carbon metabolism in response to environmental stress in fungi remains unclear. In this study, yeast one-hybrid library screening assays were employed to screen for transcription factors in Ganoderma lucidum that may interact with GlMPC. General control non-derepressible 4 (GCN4), a key transcription factor responding to nitrogen metabolism, was found to interact with the GlMPC promoter region. This interaction was further confirmed by electrophoretic mobility shift assays and chromatin immunoprecipitation quantitative PCR assays, demonstrating that GCN4 is capable of binding to the GlMPC promoter region in vitro and in vivo. Further results indicated that GCN4 could activate GlMPC expression and participate in regulating the tricarboxylic acid (TCA) cycle and ganoderic acid (GA) biosynthesis under low nitrogen conditions in G. lucidum. These findings revealed a specific regulatory mechanism by which GCN4-activated GlMPC regulates the TCA cycle and secondary metabolism under nitrogen limitation conditions in G. lucidum, providing crucial insights into the regulation of carbon and nitrogen metabolism in fungi. IMPORTANCE Mitochondrial pyruvate carrier (MPC) is a pyruvate transporter that plays a crucial role in regulating the carbon metabolic flow and is considered an essential mechanism for microorganisms to adapt to environmental changes. However, it remains unclear how MPC responds to environmental stress in organisms. General control non-derepressible 4 (GCN4), a key regulator of nitrogen metabolism, plays a pivotal role in the growth and development of fungi. In this study, we report that GCN4 can directly bind to the promoter region and activate the expression of GlMPC, thereby regulating the tricarboxylic acid cycle and secondary metabolism under nitrogen limitation conditions in Ganoderma lucidum. These findings provide significant insights into the regulation of carbon and nitrogen metabolism in fungi, highlighting the critical role of GCN4 in coordinating metabolic adaptation to environmental stresses.

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GCN4 Regulates Secondary Metabolism through Activation of Antioxidant Gene Expression under Nitrogen Limitation Conditions in Ganoderma lucidum.

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