Current understanding of grapevine defense mechanisms against the biotrophic fungus (Erysiphe necator), the causal agent of powdery mildew disease

Abstract

The most economically important disease of cultivated grapevines worldwide is powdery mildew (PM) caused by the ascomycete fungus Erysiphe necator. The majority of grapevine cultivars used for wine, table grape, and dried fruit production are derived from the Eurasian grape species Vitis vinifera because of its superior aroma and flavor characteristics. However, this species has little genetic resistance against E. necator meaning that grape production is highly dependent on the frequent use of fungicides. The integration of effective genetic resistance into cultivated grapevines would lead to significant financial and environmental benefits and represents a major challenge for viticultural industries and researchers worldwide. This review will outline the strategies being used to increase our understanding of the molecular basis of V. vinifera susceptibility to this fungal pathogen. It will summarize our current knowledge of different resistance loci/genes that have evolved in wild grapevine species to restrict PM infection and assess the potential application of these defense genes in the generation of PM-resistant grapevine germplasm. Finally, it addresses future research priorities which will be important in the rapid identification, evaluation, and deployment of new PM resistance genes which are capable of conferring effective and durable resistance in the vineyard.

Figure 1

Mechanisms of grapevine defense against the biotrophic fungal pathogen powdery mildew (E. necator). Grapevine powdery mildew spores were inoculated onto detached leaves of M. rotundifolia (A & B), V. vinifera cv. Cabernet Sauvignon (C) and a V. vinifera backcross progeny plant containing the powdery mildew resistance gene MrRUN1 (D). Leaf samples were collected after 2 days and fixed and stained with Coomassie brilliant blue to visualize fungal structures. Panels A and B represent the same field of view but are focused at different levels to show the germinated conidium (c) and appressoria (ap) on the surface of the leaf (panel A) and the globular papillae (arrows) beneath the appressoria (panel B) which are blocking penetration and haustoria formation. Panel C shows normal growth of E. necator hyphae (hy) across the leaf surface of a susceptible grapevine cultivar. Panel D shows the induction of MrRUN1-mediated programmed cell death in penetrated epidermal cells (arrows) which effectively halts further growth of this biotrophic pathogen.

Figure 2

Use of the Arabidopsis pen1 mutant for rapid screening of candidate grapevine powdery mildew resistance genes. The pen1-1 mutant line that allows increased penetration of non-adapted powdery mildew species was transformed with the grapevine powdery mildew resistance gene MrRUN1 and inoculated with either grapevine powdery mildew (E. necator) or Arabidopsis powdery mildew (E. cichoracearum). Programmed cell death (PCD) was estimated by trypan blue staining of inoculated leaves at 2 dpi. Each data point is the mean of three independent experiments (±standard deviation). In each experiment, a minimum of 100 germinated conidia were scored on each of three leaves for each line. Asterisk indicates a statistically significant difference from pen1-1 (P < 0.05; Student's t-test).