Trehalose Phosphate Synthase Complex-Mediated Regulation of Trehalose 6-Phosphate Homeostasis Is Critical for Development and Pathogenesis in Magnaporthe oryzae
Xin Chen,
Yakubu Saddeeq Abubakar,
Chengdong Yang,
Xiaxia Wang,
Pengfei Miao,
Mei Lin,
Yuetong Wen,
Qiuqiu Wu,
Haoming Zhong,
Yuping Fan,
Meiru Zhang,
Zonghua Wang,
Jie Zhou,
Wenhui Zheng
Affiliations
Xin Chen
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Yakubu Saddeeq Abubakar
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Chengdong Yang
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Xiaxia Wang
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Pengfei Miao
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Mei Lin
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Yuetong Wen
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Qiuqiu Wu
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Haoming Zhong
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Yuping Fan
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Meiru Zhang
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Zonghua Wang
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Jie Zhou
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
Wenhui Zheng
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian University Key Laboratory for Plant-Microbe Interaction, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China
ABSTRACT 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 ΔMotps2 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 ΔMotps2 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.
