Transcriptomatic profiling of acute cold stress-induced disease resistance (SIDR) genes and pathways in the grapevine powdery mildew pathosystem

Authors: WELDON, WILLIAM - Cornell University; PALUMBO, CAL - Rochester Institute Of Technology; KOVALESKI, ALISSON - Orise Fellow; TANCOS, KIERSTEN - Cornell University; GADOURY, DAVID - Cornell University; OSIER, MICHAEL - (NCE, CECR)networks Of Centres Of Exellence Of Canada, Centres Of Excellence For Commercilization A; Cadle-Davidson, Lance

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/21/2019
Publication Date: 2/1/2020
Citation: Weldon, W., Palumbo, C.D., Kovaleski, A.P., Tancos, K., Gadoury, D.M., Osier, M.V., Cadle Davidson, L.E. 2020. Transcriptomatic profiling of acute cold stress-induced disease resistance (SIDR) genes and pathways in the grapevine powdery mildew pathosystem. Molecular Plant-Microbe Interactions. 33(2):284-295. https://doi.org/10.1094/MPMI-07-19-0183-R.

Interpretive Summary: In response to non-freezing cold temperatures, several plant species develop temporary resistance to powdery mildew, termed cold stress-induced disease resistance (cold SIDR). In vineyards around the world, conditions for cold SIDR occur 14 to 21 times after budbreak, delaying powdery mildew epidemics. However, little is known of the gene expression basis of cold SIDR. We found that the maximum cold SIDR phenotype in grapevine occurs 24 hours post-cold treatment (hpc), resulting in a 15 to 25% reduction in infection. At that time, genes associated with photosynthesis are down-regulated, while starch and sugar metabolism are unaffected. This leads to ,an imbalance in carbohydrates needed by the pathogen. Additionally, 26 genes previously shown to be cold responsive had strong changes at the 24 hpc timepoint. Lastly, genes associated with transport of nutrients and amino acids were down-regulated. This analysis is the first effort to link the transient cold SIDR phenotype and underlying gene expression changes. It provides candidate genes for cold SIDR relevant to grapevine and crops with the prospect of identifying novel breeding or management targets for reduced powdery mildew severity.

Technical Abstract: In response to non-freezing cold temperatures of 2 to 8°C, several plant species have a transient induction of quantitative resistance to powdery mildew, termed cold stress-induced disease resistance (SIDR). In vineyards around the world, conditions for cold SIDR occur 14 to 21 times after budbreak and have been shown to significantly delay powdery mildew (Erysiphe necator) epidemics, but little is known of the molecular basis of this response. We analyzed cold SIDR to characterize the biology underlying the phenotype and to execute highly replicated RNAseq experiments to identify genes and pathways associated with the phenotype. Our results demonstrate the maximum cold SIDR phenotype in Vitis vinifera occurs 24 hours post-cold treatment (hpc), resulting in a 15 to 25% reduction in penetration success rate. This co-occurs with a sweeping transcriptional down-regulation of photosynthesis associated pathways, while starch and sugar metabolism pathways remained largely unaffected, which suggests an imbalance in carbohydrate supply and metabolism could result in temporarily sub-optimal host-pathogen interaction. Transcriptional changes in 26 cold responsive (COR) genes that were greatest in magnitude at the 24 hpc timepoint also represent potential transcriptional changes driving cold SIDR. Lastly, a subset of genes associated with transport of nutrients and amino acids accounted for 4 of the 8 most down-regulated transcripts. These include two nodulin 1A gene precursors, a precursor to nodulin MtN21, and a precursor to a Dynein light chain 1 motor protein. Reduced transport of plant nutrients could create localized nutrient sinks that would be sub-optimal from a pathogen perspective, again resulting in a temporary cold SIDR response. This RNAseq analysis is the first effort to link the transient cold SIDR phenotype and underlying transcriptional changes driving this form of induced host resistance. It provides an experimental framework and a library of candidate cold SIDR associated genes to further explore this response in grapevine and other host systems, with the prospect of identifying novel breeding or management targets for reduced powdery mildew severity.