Trehalose phosphate synthase complex-mediated regulation of trehalose 6-phosphate homeostasis is critical for development and pathogenesis in magnaporthe oryzae

• Main Authors: Abubakar, Y.S (Author), Chen, X. (Author), Fan, Y. (Author), Lin, M. (Author), Miao, P. (Author), Wang, X. (Author), Wang, Z. (Author), Wen, Y. (Author), Wu, Q. (Author), Yang, C. (Author), Zhang, M. (Author), Zheng, W. (Author), Zhong, H. (Author), Zhou, J. (Author)
• Format: Article
• Language: English
• Published: American Society for Microbiology 2021
• Subjects: alanine; amino acid synthesis; Article; asparagine; aspartic acid; Cell wall integrity; cellular distribution; comparative study; controlled study; cytoplasm; energy metabolism; fungal cell wall; fungal development; Fungal development; fungal gene; fungal strain; gene deletion; glucose 6 phosphate; glutamic acid; glutamine; hydrophobicity; leucine; lysine; Magnaporthe oryzae; methionine; motps3 gene; nonhuman; pathogenesis; pathogenicity; phenotype; phenylalanine; phosphate metabolism; physiological adaptation; protein assembly; protein interaction; real time polymerase chain reaction; scaffold protein; spontaneous mutation; Spontaneous mutation; TPS complex; transmission electron microscopy; trehalose; Trehalose 6- phosphate homeostasis; turgor pressure; tyrosine; valine; vegetative growth; whole genome sequencing
• Online Access: View Fulltext in Publisher

 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 DMotps2 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. © 2021 Chen et al.