Layered stomatal immunity contributes to resistance of <i>Vitis riparia</i> against downy mildew <i>Plasmopara viticola</i>

Downy mildew, caused by Plasmopara viticola, is one of the most serious grapevine diseases. Resistant grapevines are a well-known tool for mitigating pathogen-caused damage. We evaluated 29 global grapevine cultivars from seven species for sensitivity to P. viticola. Chardonnay, belonging to the sensitive species Vitis vinifera, and Qingdahean, belonging to the well-known resistant species V. riparia, were chosen for further investigation into the resistance mechanism against downy mildew. Unlike Chardonnay, Qingdahean exerted an inhibitory effect on stomatal targeting, suppression of stomatal closure, stomatal penetration of P. viticola, and the development of primary hyphae and haustoria during the early phase of infection, and contained higher levels of malondialdehyde. Malondialdehyde was significantly increased by P. viticola infection, was toxic to the pathogen, and had an interfering effect on stomatal targeting. Furthermore, Qingdahean resisted pathogen invasion through the rapid induction of guard cell death and hypersensitive responses of other cell types. These findings suggest that resistance to P. viticola in V. riparia consists of layered stomatal immunity in addition to the well-known hypersensitive response, which is overcome by the pathogen in V. vinifera.