Conservation of molecular responses upon viral infection in the non-vascular plantMarchantia polymorpha

Abstract

AbstractAfter their transition from water to land around 450 million years ago, plants colonized new habitats facing unprecedented pathogenic microbes. That expansion was mostly supported by a growing anatomical complexity based on the acquisition of developmental innovations, such as roots, stomata and vascular tissue. Despite several of those innovations became central for the interaction between plants and their associated microbes, little is known about their impact on plant immune programs and on the diversification of infection strategies of their pathogens. A paradigmatic case is the close relationship between plant vasculature and viruses. Vascular tissues provide a unique cellular environment for viral replication and existence, besides constituting a fast track for viral systemic spread throughout the plant. Since most of our knowledge about plant-virus interactions come from studies in vascular plants, we here present a comparative study to contribute to the understanding of the evolution of plant-virus interactions by molecularly characterizing the interplay between the bryophyte Marchantia polymorpha and viruses. Virome analysis of Marchantia plants shows that they are primarily associated with RNA viruses in natural settings. Additional molecular characterization of the interaction between Marchantia and tobacco mosaic virus (TMV) show conserved basic processes with vascular plants and divergent features. Viral infection triggers an extensive transcriptional reprogramming in Marchantia encompassing broad range defence responses, inhibition of cell cycle and photosynthesis and a sustained wound response that prevents further viral movement. Additionally, infected plants show premature aging and organ maturation. Notably, we found that some core responses that occur in infected areas in Marchantia, were described to be restricted to vascular tissues in Nicotiana, suggesting that evolutionary appearance of developmental innovations that became central in plants-virus interactions resulted in re-routing of defence responses. Finally, we uncover the conserved role of a transcription factor interacting with the TMV silencing suppressor p126 in specifically abrogating TMV infection.