UV-B Induced Flavonoids Contribute to Reduced Biotrophic Disease Susceptibility in Lettuce Seedlings

Biotrophic disease is one of the largest causes of decreased yield in agriculture. While exposure to ultraviolet B (UV-B) light (280-320 nm) has been previously observed to reduce plant susceptibility to disease, there is still a paucity of information regarding underlying biological mechanisms. In addition, recent advances in UV-LED technology raise the prospect of UV light treatments in agriculture which are practical and efficient. Here, we characterized the capability of UV-B LED pre-treatments to reduce susceptibility of a range of lettuce (Lactuca sativa) cultivars to downy mildew disease caused by the obligate biotroph Bremia lactucae. Innate cultivar susceptibility level did not seem to influence the benefit of a UV-B induced disease reduction with similar reductions as a percentage of the control observed (54-62% decrease in conidia count) across all susceptible cultivars. UV-B-induced reductions to conidia counts were sufficient to significantly reduce the infectivity of the diseased plant. Secondary infections caused by UV-B pre-treated plants exhibited yet further (67%) reduced disease severity. UV-B-induced flavonoids may in part mediate this reduced disease severity phenotype, as B. lactucae conidia counts of lettuce plants negatively correlated with flavonoid levels in a UV-B-dependent manner (r = -0.81). Liquid chromatography-mass spectrometry (LC-MS) was used to identify metabolic features which contribute to this correlation and, of these, quercetin 3-O-(6"-O-malonyl)-b-D-glucoside had the strongest negative correlation with B. lactucae conidia count (r = -0.68). When quercetin 3-O-(6"-O-malonyl)-b-D-glucoside was directly infiltrated into lettuce leaves, with those leaves subsequently infected, the B. lactucae conidia count was reduced (25-39%) in two susceptible lettuce cultivars. We conclude that UV-B induced phenolics, in particular quercetin flavonoids, may act as phytoanticipins to limit the establishment of biotrophic pathogens thus delaying or reducing their sporulation as measured by conidia count. These findings highlight the opportunity for UV-B morphogenesis to be exploited through the application of UV-LED technology, as part of the development of next-generation, sustainable disease control tools.