Synergistic dispersal of plant pathogen spores by jumping-droplet condensation and wind

Plant pathogens are responsible for the annual yield loss of crops worldwide and pose a significant threat to global food security. A necessary prelude to many plant disease epidemics is the short-range dispersal of spores, which may generate several disease foci within a field. New information is needed on the mechanisms of plant pathogen spread within and among susceptible plants. Here, we show that self-propelled jumping dew droplets, working synergistically with low wind flow, can propel spores of a fungal plant pathogen (wheat leaf rust) beyond the quiescent boundary layer and disperse them onto neighboring leaves downwind. An array of horizontal water-sensitive papers was used to mimic healthy wheat leaves and showed that up to 25 spores/h may be deposited on a single leaf downwind of the infected leaf during a single dew cycle. These findings reveal that a single dew cycle can disperse copious numbers of fungal spores to other wheat plants, even in the absence of rain splash or strong gusts of wind.

Spores of plant pathogenic fungi are spread through the atmosphere in three stages: liberation from the host by some active or passive method(s), drift by biotic or abiotic factors, and deposition onto a new host (1). Examples of active liberation mechanisms include osmotic pressure–driven ejection of ascospores of Fusarium graminearum (the causal agent of Fusarium head blight of wheat) and ballistospore ejection from the tip of a sterigma due to the chemical secretion of a Buller’s drop (2, 3). In the absence of wind, the resulting dispersal distance is a function of both the weight of the spore(s) and the initial discharge velocity, with the range of discharge varying from 40 μm for basidiospores (4) to 6 m for the artillery fungus (5). Passive liberation and dispersal mechanisms, such as wind and rain splash, can spread fungal diseases in plants (6). For wind to successfully liberate dry spores, an unusually strong and/or sudden gust of wind is often required (1, 6–9). In contrast, rain splash can liberate spores from a plant either through transferring momentum to the leaf to launch spores off (10, 11) or by adhering spores to splashed satellite droplets (12, 13). Spores ejected by active methods or rain splash can only disperse over a very short distance in the absence of wind (14) but when carried in moderate winds, can travel for many kilometers (15, 16).One recent study reported an entirely new mode of pathogen liberation, where coalescing dew droplets on superhydrophobic wheat leaves jump with considerable velocity (0.1 to 1.0 m/s) and carry adhered spores of a fungal plant pathogen (17). Mechanistically, the out-of-plane motion is a result of symmetry breaking as the expanding liquid bridge during coalescence impinges upon the bottom substrate (18–20) (Fig. 1A). While this initial report characterized the jumping-droplet liberation of spores in the absence of wind (17), it did not consider the subsequent dispersal or deposition, which ultimately governs the rate of disease spread. Here, we characterize the dispersal of spores of leaf rust (Puccinia triticina) after they are liberated from a diseased wheat leaf via jumping-droplet condensation. Two different scenarios are explored: short-range and long-range drift and deposition in the absence and presence of wind flow, respectively (Fig. 1 B and C). We found that even a low wind speed (0.5 m/s) is capable of dispersing as many as 100 jumping droplets and 25 spores to a single leaf downwind of a diseased leaf saturated in dew. Our ability to quantify both the liberation and dispersal of fungal spores from a diseased leaf during a dew cycle improves our understanding of disease spread within and among plants (1, 21–23).Open in a separate windowFig. 1.Spore dispersal via jumping-droplet condensation. (A) Jumping-droplet condensation on a healthy wheat leaf. Two condensed droplets coalesce (second frame) and jump off from the superhydrophobic wheat leaf (third frame). (B) Without any wind, the jumped droplets with spores can land on an adjacent healthy leaf, spreading the disease within the plant. (C) In low (0.5 m/s) to moderate (1.5 m/s) wind speed, the spore-laden jumped droplets can travel long-range to land on different healthy plants within the field.