A Violaxanthin Deepoxidase Interacts with a Viral Suppressor of RNA Silencing to Inhibit Virus Amplification

Abstract

RNA silencing plays a critical role against viral infection. To counteract this antiviral silencing, viruses have evolved various RNA silencing suppressors. Meanwhile, plants have evolved counter-counter defense strategies against RNA silencing suppression (RSS). In this study, the violaxanthin deepoxidase protein of maize (Zea mays), ZmVDE, was shown to interact specifically with the helper component-proteinase (HC-Pro; a viral RNA silencing suppressor) of Sugarcane mosaic virus (SCMV) via its mature protein region by yeast two-hybrid assay, which was confirmed by coimmunoprecipitation in Nicotiana benthamiana cells. It was demonstrated that amino acids 101 to 460 in HC-Pro and the amino acid glutamine-292 in ZmVDE mature protein were essential for this interaction. The mRNA levels of ZmVDE were down-regulated 75% to 65% at an early stage of SCMV infection. Interestingly, ZmVDE, which normally localized in the chloroplasts and cytoplasm, could relocalize to HC-Pro-containing aggregate bodies in the presence of HC-Pro alone or SCMV infection. In addition, ZmVDE could attenuate the RSS activity of HC-Pro in a specific protein interaction-dependent manner. Subsequently, transient silencing of the ZmVDE gene facilitated SCMV RNA and coat protein accumulation. Taken together, our results suggest that ZmVDE interacts with SCMV HC-Pro and attenuates its RSS activity, contributing to decreased SCMV accumulation. This study demonstrates that a host factor can be involved in secondary defense responses against viral infection in monocot plants.

Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

“…We used the Brome mosaic virus (BMV)‐derived virus‐induced gene silencing (VIGS) vector to knockdown ZmPAL transcript accumulation. BMV‐VIGS has been used successfully to decrease expression of specific maize genes for interaction studies of maize with fungal and viral pathogens (Cao et al ., ; Chen et al ., , ; van der Linde et al ., , ; Zhu et al ., ). Since the ten putative ZmPAL genes share high nucleotide sequence identity (Fig.…”

“…Substantial efforts have been devoted to understanding the molecular interactions between maize and SCMV in order to develop sustainable maize protection strategies. For instance, several maize proteins have been identified that interact directly with SCMV‐encoded proteins (Chen et al ., ; Cheng et al ., ; Zhu et al ., ). Gene and protein expression profiling have also been conducted to elucidate the response of maize to SCMV infection (Chen et al ., ; Shi et al ., , ; Uzarowska et al ., ; Wu et al ., ).…”

“…Gene and protein expression profiling have also been conducted to elucidate the response of maize to SCMV infection (Chen et al ., ; Shi et al ., , ; Uzarowska et al ., ; Wu et al ., ). However, until now, only two maize proteins (polyamine oxidase and violaxanthin deepoxidase protein) have been shown to improve resistance to SCMV (Chen et al ., , ). Thus, further studies of maize resistance to SCMV are required.…”

Chilli veinal mottle virus HCPro interacts with catalase to facilitate virus infection in Nicotiana tabacum

“…VSRs have been regarded as a counter for plant defenses to facilitate viral infection ( Mathioudakis et al , 2013 ; Chen et al , 2017 ; Hafrén et al ., 2018 ). The VSR of Tomato yellow leaf curl China virus increased the expression of the tobacco calmodulin-like protein rgs-CaM to strengthen the activity of RSS ( Makiyama et al , 2016 ).…”

Antiviral RNAi mediated Plant defense versus its suppression by viruses

“…The violaxanthin deepoxidase protein of maize (Zea mays), ZmVDE binds with HC-Pro of SCMV and this interaction down-regulates the RNA silencing suppression activity of HC-Pro. This down-regulation results in reduced accumulation of viral RNA and coat-protein in the infected cell [25]. Examples can also be drawn from geminivirus infection in tobacco cells.…”