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...
Main Authors: | , , , , , , , , , , , |
---|---|
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 |
_version_ | 1797957628124463104 |
---|---|
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. |
first_indexed | 2024-04-11T00:07:59Z |
format | Article |
id | doaj.art-b75c796ae6cb4470a8ac3507fa05d97d |
institution | Directory Open Access Journal |
issn | 1664-462X |
language | English |
last_indexed | 2024-04-11T00:07:59Z |
publishDate | 2023-01-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Plant Science |
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 |
work_keys_str_mv | AT tongjiang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT tongjiang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT kaitongdu sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT peiwang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT xinhaiwang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT lianyizang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT dezhipeng sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT xichen sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT gengsun sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT haozhang sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT zaifengfan sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT zhiyancao sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection AT taozhou sugarcanemosaicvirusorchestratesthelactatefermentationpathwaytosupportitssuccessfulinfection |