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

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Abstract

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.

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Acknowledgments

The authors would like to acknowledge the contributions of students and technicians who helped to collect data related to acute cold responses, including: Bill Weldon, Kiersten Bekoscke, Mary Jean Welser, Michelle Schaub, Hema Kasinathan, Anna Nowogrodzki, Paige Appleton, Jackie Lillis, and Breanne Kisselstein. Funding was provided by the United States Department of Agriculture Viticulture Consortium-East, the Pennsylvania Wine Marketing Board, the New York Wine and Grape Foundation, the New York Grape Production Research Fund, the Kaplan Fund, and the American Society for Enology and Viticulture National and Eastern Sections.

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  1. Department of Horticulture, Viticulture and Enology Program, Washington State University, IAREC, Prosser, WA, USA

    Michelle M. Moyer

  2. USDA-ARS Grape Genetics Research Unit, NYSAES, Geneva, NY, USA

    Jason Londo & Lance Cadle-Davidson

  3. Section of Plant Pathology and Plant-Microbe Biology, Cornell University, NYSAES, Geneva, NY, USA

    David M. Gadoury

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  1. Michelle M. Moyer
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Correspondence to Lance Cadle-Davidson.

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Moyer, M.M., Londo, J., Gadoury, D.M. et al. Cold Stress-Induced Disease Resistance (SIDR): indirect effects of low temperatures on host-pathogen interactions and disease progress in the grapevine powdery mildew pathosystem. Eur J Plant Pathol 144, 695–705 (2016). https://doi.org/10.1007/s10658-015-0745-1

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