Turnip mosaic virus in oilseed rape activates networks of sRNA-mediated interactions between viral and host genomes

Nicolas Pitzalis,David Pflieger,Khalid Amari,César Llave,Manfred Heinlein,Stéfanie Graindorge,Livia Donaire,Michael Wassenegger

doi:10.1038/s42003-020-01425-y

Abstract

Virus-induced plant diseases in cultivated plants cause important damages in yield. Although the mechanisms of virus infection are intensely studied at the cell biology level, only little is known about the molecular dialog between the invading virus and the host genome. Here we describe a combinatorial genome-wide approach to identify networks of sRNAs-guided post-transcriptional regulation within local Turnip mosaic virus (TuMV) infection sites in Brassica napus leaves. We show that the induction of host-encoded, virus-activated small interfering RNAs (vasiRNAs) observed in virus-infected tissues is accompanied by site-specific cleavage events on both viral and host RNAs that recalls the activity of small RNA-induced silencing complexes (RISC). Cleavage events also involve virus-derived siRNA (vsiRNA)–directed cleavage of target host transcripts as well as cleavage of viral RNA by both host vasiRNAs and vsiRNAs. Furthermore, certain coding genes act as virus-activated regulatory hubs to produce vasiRNAs for the targeting of other host genes. The observations draw an advanced model of plant-virus interactions and provide insights into the complex regulatory networking at the plant-virus interface within cells undergoing early stages of infection.

Highlights

Virus-induced plant diseases in cultivated plants cause important damages in yield
Tanto and Drakkar cultivars of B. napus are susceptible for infection by a green fluorescent protein (GFP)-tagged Turnip mosaic virus (TuMV) (TuMV-GFP)
We focus on several representative examples to depict a model (Fig. 7a) whereby viral susceptibility in plants can be explained on the basis of a genome-wide, complex and interactive small RNAs (sRNAs)-guided regulatory network that functions in a bidirectional fashion to control the expression of both viral and host genomes

Summary

Introduction

Virus-induced plant diseases in cultivated plants cause important damages in yield. the mechanisms of virus infection are intensely studied at the cell biology level, only little is known about the molecular dialog between the invading virus and the host genome. We uncover a complex network of sRNA-guided regulatory events at the virus infection front by investigating the role of virus- and host-derived sRNAs in guiding RNA target cleavage in the cells of initial sites of infection by Turnip mosaic virus (TuMV) within leaves of oilseed rape (Brassica napus). We address their potential contribution to viral susceptibility in Drakkar and Tanto cultivars. By allowing mutual regulation, RNA silencing plays a bidirectional role in virus–host compatibility

Methods

Results

Conclusion