Layered stomatal immunity contributes to resistance of Vitis riparia against downy mildew Plasmopara viticola

Abstract

Downy mildew (DM), 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 7 species for the sensitivity to P. viticola. Chardonnay belonging to the sensitive species V. vinifera and Qingdahean belonging to the well-known resistant species V. riparia were chosen for further investigation on the resistance mechanism against DM. 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 (MDA), which was significantly increased by P. viticola infection, toxic to the pathogen and had an interfering effect on the stomatal targeting. Furthermore, Qingdahean resisted pathogen invasion through the rapid induction of guard cell death and the hypersensitive responses (HR) of other cell types. These findings suggest that resistance to P. viticola consists of layered stomatal immunity in addition to the well-known HR in V. riparia, which is overcome by the pathogen in V. vinifera.