Five novel ubiquitous totiviruses function as virulence-promoting symbionts in the obligate biotrophic fungus Puccinia triticina
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Mycoviruses modulate fungal fitness and pathogenicity, yet their biological roles in obligate biotrophic phytopathogens remain poorly understood. Here, we report the first functional characterization of totiviruses in rust fungi, identifying five novel totiviruses, designated Puccinia triticina totivirus 1 to 5 (PtTV1–PtTV5), from the wheat leaf rust fungus Puccinia triticina ( Pt ). All five PtTVs possess the canonical genomic architecture of Totiviridae , including two overlapping ORFs and a conserved−1 ribosomal frameshifting motif. Transcriptional profiling revealed that PtTVs are highly expressed during early Pt infection. PtTV-encoded proteins suppressed BAX-triggered programmed cell death in Nicotiana benthamiana , indicating immune-suppressive activity. Using BSMV-mediated host-induced gene silencing (HIGS), we showed that knockdown of PtTV transcripts significantly impaired fungal hyphal expansion and uredinial formation, concomitant with enhanced host H₂O₂ accumulation. A survey of 90 Pt field isolates from four major wheat-growing regions of China revealed that PtTVs are ubiquitously distributed in natural rust populations. Collectively, these findings demonstrate that totiviruses function as virulence-promoting symbionts in Pt , establishing for the first time a functional link between totiviral infection and enhanced pathogenicity in cereal rust fungi and identifying candidate targets for RNAi-based disease control.
IMPORTANCE
Obligate biotrophic rust fungi represent a major group of plant pathogens with severe global agricultural impacts, yet the biological functions of their native mycoviruses remain largely uncharacterized. This study identifies five novel totiviruses from the wheat leaf rust pathogen Pt and provides the first functional demonstration that totiviruses act as virulence-promoting symbionts in cereal rust fungi. The ubiquitous presence of these viruses across geographically diverse field isolates highlights their broad ecological relevance in natural pathogen populations. These findings advance our understanding of fungus-virus mutualism in obligate biotrophic systems and offer a promising, durable molecular target for RNA-based sustainable management of wheat rust diseases.
