Begomoviral βC1 orchestrates organellar genomic instability to augment viral infection

Abstract

Chloroplast is the site for transforming light energy to chemical energy. It also acts as a production unit for a variety of defense-related molecules. These defense moieties are necessary to mount a successful counter defense against pathogens, including viruses. Previous studies indicated disruption of chloroplast homeostasis as a basic strategy of Begomovirus for its successful infection leading to the production of veinclearing, mosaic, and chlorotic symptoms in infected plants. Although begomoviral pathogenicity determinant protein Beta C1 (bC1) was implicated for pathogenicity, the underlying mechanism was unclear. Here we show that, begomoviral bC1 directly interferes with the host plastid homeostasis. bC1 induced DPD1, an organelle-specific nuclease, implicated in nutrient salvage and senescence, as well as modulated the function of a major plastid genome maintainer protein RecA1, to subvert plastid genome. We show that bC1 was able to physically interact with bacterial RecA and its plant homolog RecA1, resulting in its altered activity. We observed that knocking-down DPD1 during virus infection significantly reduced virus-induced necrosis. These results indicate the presence of a strategy in which a viral protein alters host defense by targeting modulators of chloroplast DNA. We predict that the mechanism identified here might have similarities in other plant-pathogen interactions.

Characterization of organelle DNA degradation mediated by DPD1 exonuclease in the rice genome-edited line

“…In general, fine tuning of orgDNA levels is important, because the complete loss of cpDNAs in chloroplasts may eventually lead to cell death. Recent finding of DPD1 responding to biotic stress (Nair et al 2023 ) implicates such a critical role.…”

“…However, the precise role of orgDNA degradation might vary between species, as evidenced by differing modes of orgDNA inheritance. Moreover, a recent study revealed orgDNA degradation related to biotic stress, showing that a pathogenic factor originating from Begomovirus upregulated the expression of DPD1 , resulting in vein-clearing, mosaic, and chlorotic symptoms in tobacco plants (Nair et al 2023 ). Here, to characterize DPD1 in more detail, we attempted to generate a mutant lacking DPD1 function in rice by genome editing.…”