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Salicylic Acid-Dependent Restriction of Tomato ringspot virus Spread in Tobacco Is Accompanied by a Hypersensitive Response, Local RNA Silencing, and Moderate Systemic Resistance

Tomato ringspot virus (ToRSV, a Nepovirus sp.) systemically infects many herbaceous plants. Viral RNA accumulates in symptomatic leaves and in young, asymptomatic leaves that emerge late in infection. Here, we show that systemic infection by ToRSV is restricted in tobacco. After an initial hypersensitive response in inoculated leaves, only a few plants showed limited systemic symptoms. Viral RNA did not usually accumulate to detectable levels in asymptomatic leaves. ToRSV-derived small-interfering RNAs and PR1a transcripts were only detected in tissues that contained viral RNA, indicating local induction of RNA silencing and salicylic acid (SA)-dependent defense responses. Lesion size and viral systemic spread were reduced with SA pretreatment but enhanced in NahG transgenic lines deficient in SA accumulation, suggesting that SA-dependent mechanisms play a key role in limiting ToRSV spread in tobacco. Restriction of virus infection was enhanced in transgenic lines expressing the P1-HC-Pro suppressor of silencing. Knocking down the SA-inducible RNA-dependent RNA polymerase 1 exacerbated the necrotic reaction but did not affect viral systemic spread. ToRSV-infected tobacco plants were susceptible to reinoculation by ToRSV or Tobacco mosaic virus, although a small reduction in lesion size was observed. This moderate systemic resistance suggests inefficient induction or spread of RNA silencing and systemic acquired resistance signal molecules.