The GCN4-Swi6B module mediates low nitrogen-induced cell wall remodeling in Ganoderma lucidum.

Abstract

In natural habitats, microorganisms encounter various unfavorable environmental stresses, including nitrogen deficiency. As the outermost barrier, the cell wall plays a crucial role in the interaction between the cell and the external environment. However, the effect of low nitrogen on cell wall thickness, especially the underlying molecular mechanism, is unclear. Here, we found that compared with those under normal nitrogen conditions, both the cell wall thickness and polysaccharide content of Ganoderma lucidum are increased under low nitrogen conditions. Furthermore, the abundance of SWI6B, a transcription factor that participates in cell wall remodeling, is also increased in low-nitrogen environments. The thickness and polysaccharide content of the cell wall increased in SWI6B-overexpression strains (SWI6B-OEs) but decreased in SWI6-knockdown strains (swi6-kds). Moreover, although the cell wall thickness of all the genotypes increased under nitrogen-limited conditions, the percentage of upregulated swi6-kds was significantly lower than that of the WT, and the percentage of increased SWI6B-OEs was the highest. Moreover, GCN4, a key transcription factor of the low-nitrogen signaling pathway, was found to directly bind to the promoter of SWI6. The transcriptional and translational levels of SWI6B were reduced in GCN4-knockdown strains (gcn4-kds), indicating a positive regulation of SWI6B by GCN4. Consistently, the cell wall thickness of gcn4-kds was also lower than that of the wild type. Taken together, our results revealed that the GCN4-Swi6B module regulates cell wall remodeling in G. lucidum under nitrogen deficiency conditions.

Importance: To survive in stressful environments, fungi initiate cell wall remodeling pathways to adaptively modify the cell wall composition and structure. Here, we found that nitrogen deficiency upregulated the cell wall polysaccharide content and cell wall thickness through the GCN4-SWI6B signaling pathway. Our findings provide valuable insights into the environmental adaptation of fungal cell walls, contributing to a deeper understanding of fungal responses to environmental stress.