A selective autophagy receptor VISP1 induces symptom recovery by targeting viral silencing suppressors

Tong, Xin; JiaJia, Zhao; Feng, Yan-Jie; Zou, Jing-Ze; Jian, Ye; Liu, Junfeng; Han, Chenggui; Li, Dawei; Wang, Xianbing

doi:10.1038/s41467-023-39426-0

Cited by 10 publications

(3 citation statements)

References 66 publications

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“…Furthermore, the βC1 protein is the first identified plant viral activator of autophagy and induces autophagy by interacting with the autophagy‐negative regulator glyceraldehyde‐3‐phosphate dehydrogenases (GAPCs) (Han et al, 2015; Ismayil et al, 2020a). Virus‐induced small peptide 1 (VISP1) exhibits antiviral activity by mediating autophagic degradation of suppressors of RNA silencing (VSRs), such as CMV 2b, the P14 protein of pothos latent virus (PoLV), the C2 protein of beet severe curly top virus (BSCTV), and the AC2 protein of cabbage leaf curl virus (CaLCuV) (Tong et al, 2023). Autophagy also plays an antiviral role during −ssRNA virus infection, and both the VSR proteins P3 and P2 from RSV are degraded by autophagy (Jiang et al, 2021; X.…”

Section: Antiviral Defense and Viral Counter‐defense In Plants At The...mentioning

confidence: 99%

Plant virology in the 21st century in China: Recent advances and future directions

Wu,

Zhang,

et al. 2024

JIPB

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Plant viruses are a group of intracellular pathogens that persistently threaten global food security. Significant advances in plant virology have been achieved by Chinese scientists over the last 20 years, including basic research and technologies for preventing and controlling plant viral diseases. Here, we review these milestones and advances, including the identification of new crop‐infecting viruses, dissection of pathogenic mechanisms of multiple viruses, examination of multilayered interactions among viruses, their host plants, and virus‐transmitting arthropod vectors, and in‐depth interrogation of plant‐encoded resistance and susceptibility determinants. Notably, various plant virus‐based vectors have also been successfully developed for gene function studies and target gene expression in plants. We also recommend future plant virology studies in China.This article is protected by copyright. All rights reserved.

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Section: Antiviral Defense and Viral Counter‐defense In Plants At The...mentioning

confidence: 99%

Plant virology in the 21st century in China: Recent advances and future directions

Wu,

Zhang,

et al. 2024

JIPB

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“…Mutating the AIM in Beclin1 disrupts its interaction with ATG8a, resulting in impaired capacity to induce autophagosome formation and compromised ability to degrade NIb [ 64 ]. Recent research reported that the VIRUS-INDUCED SMALL PEPTIDE 1 (VISP1), a selective autophagy receptor containing an ATG8-interacting UIM domain, induces symptom recovery from severe infections of plant viruses through controlling the stability of multiple VSRs, including the well-documented 2b encoded by cucumber mosaic virus (CMV) and the C2/AC2 of two geminiviruses [ 65 ].…”

Section: Autophagy–virus Interplay In Plants: From Antiviral Recognit...mentioning

confidence: 99%

The Great Game between Plants and Viruses: A Focus on Protein Homeostasis

Sun

Jing

Wang

et al. 2023

IJMS

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Plant viruses are tiny pathogenic obligate parasites that cause significant damage to global crop production. They exploit and manipulate the cellular components of host plants to ensure their own survival. In response, plants activate multiple defense signaling pathways, such as gene silencing and plant hormone signaling, to hinder virus propagation. Growing evidence suggests that the regulation of protein homeostasis plays a vital role in the ongoing battle between plants and viruses. The ubiquitin-proteasome-degradation system (UPS) and autophagy, as two major protein-degradation pathways, are widely utilized by plants and viruses in their arms race. One the one hand, these pathways act as essential components of plant’s antiviral defense system by facilitating the degradation of viral proteins; on the other hand, viruses exploit the UPS and autophagy to create a favorable intracellular environment for viral infection. This review aims to provide a comprehensive summary of the events involved in protein homeostasis regulation during viral infection in plants. Gaining knowledge in this area will enhance our understanding of the complex interplay between plants and viruses.

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“…However, several viruses block autophagy or utilize autophagy to degrade host defense factors, whereas other viruses exploit autophagy to support virus replication [60][61][62][63][64][65][66][67][68]. Autophagy also targets plant viruses and it is a major player in antiviral innate immunity [69][70][71][72][73][74][75]. Several plant viruses manipulate the autophagy machinery to inhibit antiviral defenses in plants [76][77][78][79][80].…”

Section: Introductionmentioning

confidence: 99%

Subversion of selective autophagy for the biogenesis of tombusvirus replication organelles inhibits autophagy

Kang,

Lin,

Nagy

2024

PLoS Pathog

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Elaborate viral replication organelles (VROs) are formed to support positive-strand RNA virus replication in infected cells. VRO formation requires subversion of intracellular membranes by viral replication proteins. Here, we showed that the key ATG8f autophagy protein and NBR1 selective autophagy receptor were co-opted by Tomato bushy stunt virus (TBSV) and the closely-related carnation Italian ringspot virus. Knockdown of ATG8f or NBR1 in plants led to reduced tombusvirus replication, suggesting pro-viral function for selective autophagy. BiFC and proximity-labeling experiments showed that the TBSV p33 replication protein interacted with ATG8f and NBR1 to recruit them to VROs. In addition, we observed that several core autophagy proteins, such as ATG1a, ATG4, ATG5, ATG101 and the plant-specific SH3P2 autophagy adaptor proteins were also re-localized to TBSV VROs, suggesting that TBSV hijacks the autophagy machinery in plant cells. We demonstrated that subversion of autophagy components facilitated the recruitment of VPS34 PI3 kinase and enrichment of phospholipids, such as phosphatidylethanolamine and PI3P phosphoinositide in the VRO membranes. Hijacking of autophagy components into TBSV VROs led to inhibition of autophagic flux. We also found that a fraction of the subverted ATG8f and NBR1 was sequestered in biomolecular condensates associated with VROs. We propose that the VRO-associated condensates trap those autophagy proteins, taking them away from the autophagy pathway. Overall, tombusviruses hijack selective autophagy to provide phospholipid-rich membranes for replication and to regulate the antiviral autophagic flux.

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A selective autophagy receptor VISP1 induces symptom recovery by targeting viral silencing suppressors

Cited by 10 publications

References 66 publications

Plant virology in the 21st century in China: Recent advances and future directions

Plant virology in the 21st century in China: Recent advances and future directions

The Great Game between Plants and Viruses: A Focus on Protein Homeostasis

Subversion of selective autophagy for the biogenesis of tombusvirus replication organelles inhibits autophagy

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