STAYGREEN, STAY HEALTHY: a loss-of-susceptibility mutation in the STAYGREEN gene provides durable, broad-spectrum disease resistances for over 50 years of U.S. cucumber production

Authors: WANG, Y - University Of Wisconsin; TAN, JY - University Of Wisconsin; WU, ZM - University Of Wisconsin; VANDENLANGENBERG, K - North Carolina State University; WEHNER, TC - North Carolina State University; WEN, CL - Beijing Academy Of Agricultural Sciences; ZHENG, XY - Magnum Seeds Inc; OWENS, K - Magnum Seeds Inc; THORNTON, A - Harris Moran Seed Company; BANG, HH - Harris Moran Seed Company; HOEFT, E - Harris Moran Seed Company; KRAAN, PAG - Bayer Crop Sciences, Germany; SUELMANN, J - Bayer Crop Sciences, Germany; PAN, JS - University Of Wisconsin; Weng, Yiqun

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/13/2018
Publication Date: 7/19/2018
Citation: Wang, Y., Tan, J., Wu, Z., Vandenlangenberg, K., Wehner, T., Wen, C., Zheng, X., Owens, K., Thornton, A., Bang, H., Hoeft, E., Kraan, P., Suelmann, J., Pan, J., Weng, Y. 2018. STAYGREEN, STAY HEALTHY: a loss-of-susceptibility mutation in the STAYGREEN gene provides durable, broad-spectrum disease resistances for over 50 years of U.S. cucumber production. New Phytologist. 221:415-430. https://doi.org/10.1111/nph.15353.
DOI: https://doi.org/10.1111/nph.15353

Interpretive Summary: Development of varieties with multiple disease resistances is always a goal for plant breeders. In reality, resistances to different pathogens are controlled by different genes, which makes breeding work more challenging. One category of disease resistance genes called loss-of-susceptible resistance gene, is ideal, in which a single gene often contributes to resistance to multiple pathogens. Very few such genes have been identified in some cereal crops. In cucumber, the Gy14 cucumber has been known to be resistant against the downy mildew (DM, an oomycyte pathogen), angular leaf spot (ALS, a bacterial pathogen) and the anthracnose (AR, a fungal pathogen) pathogens, but the underlying molecular mechanisms are unknown. In this study, we conducted QTL mapping for the disease resistances in Gy14 and further map-based cloning identified a candidate gene for the three resistances. We show that the triple-disease resistances in Gy14 were controlled by the cucumber STAYGREEN gene, which plays an important regulatory role in the chlorophyll degradation pathway. We found that the durable, broad-spectrum disease resistance in cucumber is due to loss-of-susceptibility mutation in the STAYGREEN gene. From this study, we found a novel function of the highly conserved STAYGREEN gene in plants. Molecular markers developed from this study have been successfully used in cucumber breeding for the DM and anthroacnose resistances by commercial breeding programs.

Technical Abstract: 1. The Gy14 cucumber (Cucumis sativus L.) is resistant against the oomyceteous downy mildew (DM), bacterial angular leaf spot (ALS) and fungal anthracnose (AR) pathogens, but the underlying molecular mechanisms are unknown. 2. QTL mapping for the disease resistances in Gy14 and further map-based cloning identified a candidate gene for the resistant loci, which was validated and functionally characterized by spatial-temporal gene expression profiling, allelic diversity and phylogenetic analysis, as well as local association studies. 3. We show that the triple-disease resistances in Gy14 were controlled by the cucumber STAYGREEN (CsSGR) gene. A SNP in the coding region resulted in a nonsynonymous amino acid substitution in the CsSGR protein, and thus disease resistance. Genes in the chlorophyll degradation pathway showed differential expression between resistant and susceptible lines in response to pathogen inoculation. The causal SNP was significantly associated with disease resistances in natural and breeding populations. The resistance allele has undergone selection in cucumber breeding. 4. The durable, broad-spectrum disease resistance is due to loss-of-susceptibility mutation of CsSGR. Likely, this is achieved through inhibition of reactive oxygen species over-accumulation and phytotoxic catabolite over-buildup in the chlorophyll degradation pathway. The CsSGR-mediated host resistance represents a novel function of this highly conserved gene in plants.