Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

Tong Jiang; Kaitong Du; Pei Wang; Xinhai Wang; Lianyi Zang; Dezhi Peng; Xi Chen; Geng Sun; Hao Zhang; Zaifeng Fan; Zhiyan Cao; Tao Zhou

doi:10.3389/fpls.2022.1099362

Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection

Front Plant Sci. 2023 Jan 9:13:1099362. doi: 10.3389/fpls.2022.1099362. eCollection 2022.

Authors

Tong Jiang^{1

2}, Kaitong Du¹, Pei Wang¹, Xinhai Wang¹, Lianyi Zang³, Dezhi Peng¹, Xi Chen¹, Geng Sun¹, Hao Zhang¹, Zaifeng Fan¹, Zhiyan Cao², Tao Zhou¹

Affiliations

¹ State Key Laboratory for Agro-Biotechnology, and Ministry of Agriculture and Rural Affairs, Key Laboratory for Pest Monitoring and Green Management, Department of Plant Pathology, China Agricultural University, Beijing, China.
² State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University, Baoding, Hebei, China.
³ Collaborative Innovation Center of Fruit and Vegetable Quality and Efficient Production in Shandong, Shandong Agricultural University, Tai'an, China.

Abstract

Viruses often establish their own infection by altering host metabolism. How viruses co-opt plant metabolism to support their successful infection remains an open question. Here, we used untargeted metabolomics to reveal that lactate accumulates immediately before and after robust sugarcane mosaic virus (SCMV) infection. Induction of lactate-involved anaerobic glycolysis is beneficial to SCMV infection. The enzyme activity and transcriptional levels of lactate dehydrogenase (LDH) were up-regulated by SCMV infection, and LDH is essential for robust SCMV infection. Moreover, LDH relocates in viral replicase complexes (VRCs) by interacting with SCMV-encoded 6K2 protein, a key protein responsible for inducing VRCs. Additionally, lactate could promote SCMV infection by suppressing plant defense responses. Taken together, we have revealed a viral strategy to manipulate host metabolism to support replication compartment but also depress the defense response during the process of infection.

Keywords: anaerobic glycolysis; lactate; lactate dehydrogenase; maize; metabolomics; sugarcane mosaic virus; viral replicase complexes.

Grants and funding

This study was supported by grants from State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2021KF-10), China Agriculture Research System of MOF and MARA of China, the National Natural Science Foundation of China (Grant 31871930).