Vector-mediated viral exchange between crops and weedy plants

Abstract

While virus-vector-crop interactions have received considerable attention, free-living plants growing in cultivated areas (‘weeds’) can also serve as viral reservoirs. Although weed-to-crop transmission is well documented, less is known about crop-to-weed transmission and how the interplay between the two plant groups affects disease dynamics. We explored reciprocal viral transmission of Tomato chlorosis virus (ToCV) between tomatoes and ToCV-susceptible weeds by Bemisia tabaci MED. A field survey assessed Bemisia density and ToCV titer in virus-susceptible weeds; a parallel experiment demonstrated that their removal reduced ToCV infection in tomatoes. Weeds growing far from greenhouses had lower rates of ToCV infection than greenhouse-adjacent ones, suggesting reciprocal crop-weed viral exchange. While Bemisia preferred tomato over weeds, vector density and viral infection of near-greenhouse populations of the dominant weed Amaranthus retroflexus increased following tomato harvest. ToCV infection altered volatile production in A. retroflexus; the Bemisia-attractant compound neophytadiene increased 26-fold in infected plants. Because temperatures increase over the growing season, we also explored the relationship between temperature, neophytadiene levels, and whitefly preference: plants grown at higher temperatures produced more neophytadiene and were preferred by whiteflies. We also assessed volatile production and jasmonic acid levels in control A. retroflexus versus those previously fed upon by either virus-free or viruliferous Bemisia. The largest shifts occurred in plants fed upon by viruliferous whiteflies, demonstrating that ToCV rather than Bemisia feeding explained the observed changes. Our results suggest that post-harvest viral transfer from crops to weeds may play an important role in driving disease outbreaks the following season and identify some simple but effective ways of reducing transmission into weedy plant species.