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Sugarcane mosaic virus remodels multiple intracellular organelles to form genomic RNA replication sites

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Abstract

Positive-stranded RNA viruses usually remodel the host endomembrane system to form virus-induced intracellular vesicles for replication during infections. The genus Potyvirus of the family Potyviridae represents the largest number of positive single-stranded RNA viruses, and its members cause great damage to crop production worldwide. Although potyviruses have a wide host range, each potyvirus infects a relatively limited number of host species. Phylogenesis and host range analysis can divide potyviruses into monocot-infecting and dicot-infecting groups, suggesting that they differ in their infection mechanisms, probably during replication. Comprehensive studies on the model dicot-infecting turnip mosaic virus have shown that the 6K2-induced replication vesicles are derived from the endoplasmic reticulum (ER) and subsequently target chloroplasts for viral genome replication. However, the replication site of monocot-infecting potyviruses is unknown. In this study, we show that the precursor 6K2-VPg-Pro polyproteins of dicot-infecting potyviruses and monocot-infecting potyviruses cluster phylogenetically in two separate groups. With a typical gramineae-infecting potyvirus—sugarcane mosaic virus (SCMV)—we found that replicative double-stranded RNA (dsRNA) forms aggregates in the cytoplasm but does not associate with chloroplasts. SCMV 6K2-VPg-Pro-induced vesicles colocalize with replicative dsRNA. Moreover, SCMV 6K2-VPg-Pro-induced structures target multiple intracellular organelles, including the ER, Golgi apparatus, mitochondria, and peroxisomes, and have no evident association with chloroplasts.

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Acknowledgements

We sincerely thank Professor Aiming Wang (Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, Canada) for the dRBFC vectors, and Professor Andrew O. Jackson (University of California, Berkeley) for providing the pGD vectors.

Funding

This work was supported by grants from the National Natural Science Foundation of China (Grant 31871930), the Ministry of Agriculture and Rural Affairs of China (2018YFD020062, 2016ZX08010-001), and the Ministry of Education of China (the 111 Project B13006).

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Authors and 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, 100193, China

    Jipeng Xie, Tong Jiang, Zhifang Li, Zaifeng Fan & Tao Zhou

  2. Department of Plant Pathology, Shandong Agricultural University, Tai’an, 271018, China

    Xiangdong Li

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  1. Jipeng Xie
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  2. Tong Jiang
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  3. Zhifang Li
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Contributions

JX and TZ designed the experiments. JX performed most of the experiments. JX, TJ, ZL, XL, ZF, and TZ analyzed the data. JX and TZ wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Tao Zhou.

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Xie, J., Jiang, T., Li, Z. et al. Sugarcane mosaic virus remodels multiple intracellular organelles to form genomic RNA replication sites. Arch Virol 166, 1921–1930 (2021). https://doi.org/10.1007/s00705-021-05077-z

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