Autophagy is involved in assisting the replication of Bamboo mosaic virus in Nicotiana benthamiana

Huang, Y. S.; Huang, Ying-Wen; Hsiao, Y.-Y.; Li, Siou-Cen; Hsu, Yau-Heiu; Tsai, Ching Hsiu

doi:10.1093/jxb/erz244

Cited by 29 publications

(21 citation statements)

References 71 publications

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“…Other studies have shown the specific roles of autophagy in eliminating viruses in mammalian cells [ 47 , 48 ]. On the other hand, several plant viruses have been shown to inhibit or utilize autophagy to promote their infections in plants [ 26 , 28 , 49 – 51 ]. Here, we show that autophagy plays an important role in pepper defense responses to PMMoV infection.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection

Jiao

et al. 2020

BMC Plant Biol

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Background Pepper mild mottle virus (PMMoV) is a member in the genus Tobamovirus and infects mainly solanaceous plants. However, the mechanism of virus-host interactions remains unclear. To explore the responses of pepper plants to PMMoV infection, we analyzed the transcriptomic changes in pepper plants after PMMoV infection using a high-throughput RNA sequencing approach and explored the roles of host autophagy in regulating PMMoV infection. Results A total of 197 differentially expressed genes (DEGs) were obtained after PMMoV infection, including 172 significantly up-regulated genes and 25 down-regulated genes. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses revealed that most up-regulated DEGs were involved in plant abiotic and biotic stresses. Further analyses showed the expressions of multiple autophagy-related genes (ATGs) were increased after PMMoV infection in pepper and Nicotiana benthamiana plants. Through confocal microscopy and transmission electron microscopy, we have found that PMMoV infection in plant can induce autophagy, evidenced by the increased number of GFP-ATG8a fluorescent punctate and the appearance of double membrane autophagic structures in cells of N. benthamiana. Additionally, inhibition of autophagy significantly increased PMMoV RNA accumulation and aggravated systemic PMMoV symptoms through autophagy inhibitor (3-MA and E64d) treatment and silencing of NbATG expressions by a Tobacco rattle virus-induced gene silencing assays. These results indicated that autophagy played a positive role in plant resistance to PMMoV infection. Conclusions Taken together, our results provide a transcriptomic insight into pepper responding to PMMoV infection and reveal that autophagy induced by PMMoV infection has an antiviral role in regulating PMMoV infection. These results also help us to better understand the mechanism controlling PMMoV infection in plants and to develop better strategies for breeding projects for virus-resistant crops.

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Section: Discussionmentioning

confidence: 99%

Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection

Jiao

et al. 2020

BMC Plant Biol

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“…On the other hand, pro‐viral roles of autophagy are found in polioviruses, and likely the closely related rhinoviruses, which use the formation of autophagosome‐like structures to serve as the membrane scaffolds for RNA replication (Jackson et al , ; Chiramel et al , ). Recently, new evidence demonstrated that some plant viruses can repress or use autophagy to promote the viral infection (Hofius et al , ; Li et al , ; Hafrén et al , ; Yang et al , ; Huang et al , ). A growing body of data is helping delineate the role of autophagy in the arms race between plant viruses and their hosts.…”

Section: Discussionmentioning

confidence: 99%

Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants

Zhang

et al. 2019

New Phytologist

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Autophagy is an evolutionarily conserved degradation pathway in the cytoplasm and has emerged as a key defense mechanism against invading pathogens. However, there is no evidence showing nuclear autophagy in plants.Here, we show that a geminivirus nuclear protein, C1 of tomato leaf curl Yunnan virus (TLCYnV) induces autophagy and interacts directly with the core autophagy-related protein ATG8h. The interaction between ATG8h and C1 leads to the translocation of the C1 protein from the nucleus to the cytoplasm and the decreased protein accumulation of C1, which is dependent on the exportin1-mediated nuclear export pathway. The degradation of C1 is blocked by autophagy inhibitors and compromised when the autophagy-related genes (ATGs) ATG8h, ATG5, or ATG7 are knocked down. Similarly, silencing of these ATGs also promotes TLCYnV infection in Nicotiana benthamiana and Solanum lycopersicum plants.The mutation of a potential ATG8 interacting motif (AIM) in C1 abolishes its interaction with ATG8h in the cytoplasm but favors its interaction with Fibrillarin1 in the nucleolus. TLCYnV carrying the AIM mutation displays enhanced pathogenicity in solanaceous plants.Taken together, these data suggest that a new type of nuclear autophagy-mediated degradation of viral proteins through an exportin1-dependent nuclear export pathway restricts virus infection in plants.

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“…Autophagy inhibitor 3-MA treatment blocked autophagosome formation and reduced the accumulation of the viral coat protein, whereas rapamycin, an inducer treatment, enhanced the expression of the viral coat protein. BaMV-induced autophagy may offer an environment more conductive to viral replication or a shelter to evade from the RNA silencing (Huang et al, 2019). However, the autophagy mechanism contributing to BaMV RNA increase, and which viral protein of BaMV plays the crucial role in autophagy induction require further study.…”

Section: Plant Virus Promotes Infection Through Host Autophagymentioning

confidence: 99%

Friend or Enemy: A Dual Role of Autophagy in Plant Virus Infection

et al. 2020

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Autophagy is a primary protective process that involves removing damaged organelles or dysfunctional proteins in eukaryotes. The autophagy pathway not only maintains cellular homeostasis, but also modulates the host's cellular response to pathogen infection. Several studies proved that autophagy plays a dominant role in plant fitness and immunity. As intracellular parasites, the replication and spread of viruses entirely rely upon the molecular machinery of the host cell, including the autophagy process. Plant viruses severely affect crop yields and quality. During infection, complex interactions occur between viral proteins and host factors in relation to plant defense and virus counter-defense. An increasing number of studies demonstrated that plants use autophagy to eliminate and inhibit viruses; some viruses were shown to manipulate the process of autophagy to promote their own replication and survival in plant cells. In this review, we summarize recent advances in plant autophagy, with an emphasis on the role of autophagy in plant virus infection.

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Autophagy is involved in assisting the replication of Bamboo mosaic virus in Nicotiana benthamiana

Cited by 29 publications

References 71 publications

Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection

Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection

Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants

Friend or Enemy: A Dual Role of Autophagy in Plant Virus Infection

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