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Trehalose biosynthesis pathway is a potential target for antifungal drug development, and trehalose 6-phosphate (T6P) accumulation is widely known to have toxic effects on cells. However, how organisms maintain a safe T6P level and cope with its cytotoxicity effects when accumulated have not been reported. Herein, we unveil the mechanism by which the rice blast fungus  Magnaporthe oryzae  avoids T6P accumulation and the genetic and physiological adjustments it undergoes to self-adjust the metabolite level when it is unavoidably accumulated. We found that T6P accumulation leads to defects in fugal development and pathogenicity. The accumulated T6P impairs cell wall assembly by disrupting actin organization. The disorganization of actin impairs the distribution of chitin synthases, thereby disrupting cell wall polymer distribution. Additionally, accumulation of T6P compromise energy metabolism.  M. oryzae  was able to overcome the effects of T6P accumulation by self-mutation of its  MoTPS3  gene at two different mutation sites. We further show that mutation of  MoTPS3  suppresses MoTps1 activity to reduce the intracellular level of T6P and partially restore Δ Motps2  defects. Overall, our results provide insights into the cytotoxicity effects of T6P accumulation and uncover a spontaneous mutation strategy to rebalance accumulated T6P in  M. oryzae .   IMPORTANCE   M. oryzae , the causative agent of the rice blast disease, threatens rice production worldwide. Our results revealed that T6P accumulation, caused by the disruption of  MoTPS2 , has toxic effects on fugal development and pathogenesis in  M. oryzae . The accumulated T6P impairs the distribution of cell wall polymers via actin organization and therefore disrupts cell wall structure.  M. oryzae  uses a spontaneous mutation to restore T6P cytotoxicity. Seven spontaneous mutation sites were found, and a mutation in  MoTPS3  was further identified. The spontaneous mutation in  MoTPS3  can partially rescue Δ Motps2  defects by suppressing MoTps1 activity to alleviate T6P cytotoxicity. This study provides clear evidence for better understanding of T6P cytotoxicity and how the fungus protects itself from T6P’s toxic effects when it has accumulated to severely high levels.

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Trehalose Phosphate Synthase Complex-Mediated Regulation of Trehalose 6-Phosphate Homeostasis Is Critical for Development and Pathogenesis in Magnaporthe oryzae