The unfolded protein response plays dual roles in rice stripe virus infection through fine-tuning the movement protein accumulation
Open Access
- 4 March 2021
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Pathogens
- Vol. 17 (3), e1009370
- https://doi.org/10.1371/journal.ppat.1009370
Abstract
The movement of plant viruses is a complex process that requires support by the virus-encoded movement protein and multiple host factors. The unfolded protein response (UPR) plays important roles in plant virus infection, while how UPR regulates viral infection remains to be elucidated. Here, we show that rice stripe virus (RSV) elicits the UPR in Nicotiana benthamiana. The RSV-induced UPR activates the host autophagy pathway by which the RSV-encoded movement protein, NSvc4, is targeted for autophagic degradation. As a counteract, we revealed that NSvc4 hijacks UPR-activated type-I J-domain proteins, NbMIP1s, to protect itself from autophagic degradation. Unexpectedly, we found NbMIP1 stabilizes NSvc4 in a non-canonical HSP70-independent manner. Silencing NbMIP1 family genes in N. benthamiana, delays RSV infection, while over-expressing NbMIP1.4b promotes viral cell-to-cell movement. Moreover, OsDjA5, the homologue of NbMIP1 family in rice, behaves in a similar manner toward facilitating RSV infection. This study exemplifies an arms race between RSV and the host plant, and reveals the dual roles of the UPR in RSV infection though fine-tuning the accumulation of viral movement protein. The unfolded protein response (UPR) is a cellular response aiming to eliminate abnormal proteins in and restoring ER homeostasis. The infection of many plant viruses can induce the UPR of plant cells, and previous studies show that in most cases, the UPR benefits plant viral infections. However, how the UPR regulates plant viral infections is still poorly understood. Here, we find that a plant virus, rice stripe virus (RSV), can induce host UPR, and the UPR plays dual roles in RSV infection. On the one hand, the RSV-induced UPR activates the host autophagy pathway by which the virus-encoded movement protein, NSvc4, is degraded. On the other hand, the RSV-induced UPR also upregulates the expression of a type-I J-domain protein family in plant, which is hijacked by NSvc4 to protect itself from autophagic degradation. We present an example for an arms race between RSV and the host plant, and illustrate a new model of the UPR regulating viral infection in plants by fine-tuning the accumulation of virus-encoded MP.Keywords
Funding Information
- Earmarked Fund for Modern Agro-industry Technology Research System (nycytx-001)
- Ministry of Agriculture and Rural Affairs of the People's Republic of China (2016ZX08009003-001)
- National Natural Science Foundation of China (31772125)
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