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

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 v...

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Main Authors: Tong Jiang, Kaitong Du, Pei Wang, Xinhai Wang, Lianyi Zang, Dezhi Peng, Xi Chen, Geng Sun, Hao Zhang, Zaifeng Fan, Zhiyan Cao, Tao Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1099362/full
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author Tong Jiang
Tong Jiang
Kaitong Du
Pei Wang
Xinhai Wang
Lianyi Zang
Dezhi Peng
Xi Chen
Geng Sun
Hao Zhang
Zaifeng Fan
Zhiyan Cao
Tao Zhou
author_facet Tong Jiang
Tong Jiang
Kaitong Du
Pei Wang
Xinhai Wang
Lianyi Zang
Dezhi Peng
Xi Chen
Geng Sun
Hao Zhang
Zaifeng Fan
Zhiyan Cao
Tao Zhou
author_sort Tong Jiang
collection DOAJ
description 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.
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spelling doaj.art-b75c796ae6cb4470a8ac3507fa05d97d2023-01-09T10:16:30ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-01-011310.3389/fpls.2022.10993621099362Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infectionTong Jiang0Tong Jiang1Kaitong Du2Pei Wang3Xinhai Wang4Lianyi Zang5Dezhi Peng6Xi Chen7Geng Sun8Hao Zhang9Zaifeng Fan10Zhiyan Cao11Tao Zhou12State 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, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University, Baoding, Hebei, ChinaState 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, ChinaState 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, ChinaState 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, ChinaCollaborative Innovation Center of Fruit and Vegetable Quality and Efficient Production in Shandong, Shandong Agricultural University, Tai’an, ChinaState 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, ChinaState 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, ChinaState 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, ChinaState 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, ChinaState 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, ChinaState Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University, Baoding, Hebei, ChinaState 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, ChinaViruses 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.1099362/fullmetabolomicssugarcane mosaic virusmaizeanaerobic glycolysislactate dehydrogenaseviral replicase complexes
spellingShingle Tong Jiang
Tong Jiang
Kaitong Du
Pei Wang
Xinhai Wang
Lianyi Zang
Dezhi Peng
Xi Chen
Geng Sun
Hao Zhang
Zaifeng Fan
Zhiyan Cao
Tao Zhou
Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
Frontiers in Plant Science
metabolomics
sugarcane mosaic virus
maize
anaerobic glycolysis
lactate dehydrogenase
viral replicase complexes
title Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
title_full Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
title_fullStr Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
title_full_unstemmed Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
title_short Sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
title_sort sugarcane mosaic virus orchestrates the lactate fermentation pathway to support its successful infection
topic metabolomics
sugarcane mosaic virus
maize
anaerobic glycolysis
lactate dehydrogenase
viral replicase complexes
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1099362/full
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