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

Abstract

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.

A novel strategy for improving watermelon resistance to cucumber green mottle mosaic virus by exogenous boron application

“…Twelve genes in N. benthamiana that were homologous with the above watermelon genes were selected to be silenced by TRV‐based VIGS vector (Jiao et al, 2020 ). These approximately 330 bp fragments representing the partial sequence of the 12 genes were amplified individually from an N. benthamiana cDNA through PCR using the PrimeSTAR Max DNA polymerase (TaKaRa) and specific primers (Table S9 ).…”

“…Cucumber green mottle mosaic virus (CGMMV) is an RNA virus in the genus Tobamovirus. CGMMV can infect many cucurbit crops, including watermelon, and cause severe watermelon blood fresh disease (WBFD) in watermelon fruits (Dombrovsky et al, 2017;Li et al, 2017Li et al, , 2020. The CGMMV-infected watermelon fruits often show spongy rot, discolouration, and acidification, resulting in significant economic losses (Dombrovsky et al, 2017;Li et al, 2020).…”

“…In 2007, the Agricultural Ministry of China declared CGMMV as a plant quarantine pest that could potentially threat the production of cucurbit crops in China (http:// www.moa.gov.cn/). In recent years, several research laboratories have analysed the effects of CGMMV infection on gene expression in watermelon plants (Li et al, 2017(Li et al, , 2020Sun et al, 2019).…”

Effects of the Noncoding Subgenomic RNA of Red Clover Necrotic Mosaic Virus in Virus Infection

“…10A ). These pathways are frequently found to be enriched during viral infections ( 54 , 55 ). Most of the enriched pathways can be grouped under metabolic pathways and it shows the significant impact of wt RCNMV infection on the plant’s metabolism.…”

Selective autophagic receptor NbNBR1 prevents NbRFP1-mediated UPS-dependent degradation of βC1 to promote geminivirus infection

“…Autophagy was initially shown to regulate plant immunity to DNA and RNA viruses, including CaMV, CLCuMuV, TYLCCNV, TMV, TuMV, cucumber mosaic virus, rice stripe virus and pepper mild mottle virus [15][16][17][18][33][34][35][36]. To counteract autophagy-mediated host resistance, many RNA viruses have evolved specific abilities to manipulate host autophagy machinery directly or indirectly to benefit their infections [18,19,21,[37][38].…”