Cold Stress-Induced Disease Resistance (SIDR): indirect effects of low temperatures on host-pathogen interactions and disease progress in the grapevine powdery mildew pathosystem

Erysiphe necator is an obligate biotroph capable of infecting three genera within the Vitaceae (Vitis, Parthenocissus, and Ampelopsis). The pathogen inhabits a niche unique to most powdery mildews, i.e., wholly external mycelial growth supported by haustoria within the subtending host epidermal cells. This growth habit coupled with its biotrophic reliance on the host makes E. necator sensitive to both direct effects of abiotic stresses on the pathogen and indirect abiotic effects via the host responses. Development of the pathogen during acute cold events (e.g., 1 h at 4 °C) results in death of hyphal segments and a prolonged latency, an effect further increased by the development of ontogenic resistance as epidermal tissues of leaves and berries age. Acute cold events can also stress the host prior to the arrival of the pathogen, and thereby reduce susceptibility to infection via cold Stress-Induced Disease Resistance (SIDR), a recently described phenomenon. This effect requires approximately 24 h post-cold before maximal resistance effect occurs, and is also transient in that the effect diminishes to a basal level within 48 h after exposure. Although the phenotypic responses to cold SIDR may be similar to those observed on ontogenically-resistant leaves, the effects of cold SIDR and ontogenic resistance are additive. Sufficient tools are now available for investigating the mechanistic basis of cold SIDR. While pathosystems involving obligate biotrophs complicate research on direct and indirect environmental effects on the pathogen, this requisite interaction also creates interesting systems to understand how the condition of the host may influence subsequent disease development. At the population level, the effects of repeated cold events have profound effects on the nature of epidemic progress and implications for management of grape powdery mildew. The objective in this review is to summarize our current knowledge regarding the indirect and consequential effects of low temperature on the development of grapevine powdery mildew.