General control nonderepressible 4 activates the transcription of trehalose phosphorylase to improve trehalose production and abiotic stress tolerance in Ganoderma lucidum.

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Citation abstract

Trehalose plays an important role in enhancing abiotic stress tolerance. Although studies have reported the induction of trehalose by adverse environments, the molecular mechanism underlying its induction in fungi is unclear. In fungi, the trehalose phosphorylase (TreP) catalyzes the reversible reaction of trehalose formation. Here, we found that the carbon and nitrogen metabolism integrated transcription factor, general control nonderepressible 4 (GCN4) directly binds to the promoter of TreP in Ganoderma lucidum. GCN4 up-regulates the transcription and protein levels of TreP, leading to enhanced trehalose synthase activity and trehalose accumulation. A reduced abundance of GCN4 alleviated the low-nitrogen induced increase in Trep and trehalose contents. As a result, knockdown of both GCN4 and TreP leads to a reduction in the trehalose content and growth inhibition of mycelia, especially under low-nitrogen conditions. Furthermore, in addition to nitrogen deficiency, both high temperature and drought treatments increase the transcription and protein levels of GCN4 and TreP. The GCN4 or TreP knockdown strains are hypersensitive to heat stress and drought, while exogenous trehalose treatment enhances the mycelial growth under stressful conditions. Together, our results revealed that the GCN4-TreP module promotes trehalose accumulation in response to abiotic stresses to improve the stress tolerance of G. lucidum, and highlighted the pivotal role of GCN4 in integrating metabolic adaptation to environmental stresses.