Roles of GFAT and PFK genes in energy metabolism of brown planthopper, Nilaparvata lugens

Hui-Ru Si; Si-Si Sun; Yong-Kang Liu; Ling-Yu Qiu; Bin Tang; Fang Liu; Qiang Fu; Cai-Di Xu; Pin-Jun Wan

doi:10.3389/fphys.2023.1213654

Roles of GFAT and PFK genes in energy metabolism of brown planthopper, Nilaparvata lugens

Front Physiol. 2023 Jun 21:14:1213654. doi: 10.3389/fphys.2023.1213654. eCollection 2023.

Authors

Hui-Ru Si^{1

2}, Si-Si Sun³, Yong-Kang Liu², Ling-Yu Qiu^{1

2}, Bin Tang², Fang Liu¹, Qiang Fu¹, Cai-Di Xu⁴, Pin-Jun Wan¹

Affiliations

¹ State Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou, Zhejiang, China.
² College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, Zhejiang, China.
³ Guizhou Institute of Mountainous Environment and Climate, Guiyang, China.
⁴ Jing Hengyi School of Education, Hangzhou Normal University, Hangzhou, Zhejiang, China.

Abstract

Glutamine:fructose-6-phosphate aminotransferases (GFATs) and phosphofructokinase (PFKs) are the principal rate-limiting enzymes involved in hexosamine biosynthesis pathway (HBP) and glycolysis pathway, respectively. In this study, the NlGFAT and NlPFK were knocked down through RNA interference (RNAi) in Nilaparvata lugens, the notorious brown planthopper (BPH), and the changes in energy metabolism were determined. Knockdown of either NlGFAT or NlPFK substantially reduced gene expression related to trehalose, glucose, and glycogen metabolism pathways. Moreover, trehalose content rose significantly at 72 h after dsGFAT injection, and glycogen content increased significantly at 48 h after injection. Glucose content remained unchanged throughout the experiment. Conversely, dsPFK injection did not significantly alter trehalose, but caused an extreme increase in glucose and glycogen content at 72 h after injection. The Knockdown of NlGFAT or NlPFK significantly downregulated the genes in the glycolytic pathway, as well as caused a considerable and significant decrease in pyruvate kinase (PK) activity after 48 h and 72 h of inhibition. After dsGFAT injection, most of genes in TCA cycle pathway were upregulated, but after dsNlPFK injection, they were downregulated. Correspondingly, ATP content substantially increased at 48 h after NlGFAT knockdown but decreased to an extreme extent by 72 h. In contrast, ATP content decreased significantly after NlPFK was knocked down and returned. The results have suggested the knockdown of either NlGFAT or NlPFK resulted in metabolism disorders in BPHs, highlighting the difference in the impact of those two enzyme genes on energy metabolism. Given their influence on BPHs energy metabolism, developing enzyme inhibitors or activators may provide a biological control for BPHs.

Keywords: Nilaparvata lugens; RNA interference; energy metabolism; glutamine: fructose-6-phosphate aminotransferase; phosphofructokinase.

Grants and funding

This work was supported by the “Pioneer” and “Leading Goose” R&D Program of Zhejiang (2022C02047), the National Natural Science Foundation of China (Grant No. 32272608), the Rice Pest Management Research Group of the Agricultural Science and Technology Innovation Program of China Academy of Agricultural Science (CAAS-ASTIP-2016-CNRRI), the Guizhou Provincial Science and Technology Foundation [ZK (2021) 210], and Hangzhou Normal University’s Starlight Plan in 2023 and Hangzhou Normal University Undergraduate Innovation Ability Improvement Project.