Genome-wide associations within diverse wild apple germplasm for postharvest blue mold resistance to Penicillium expansum

Authors: WHITT, LAUREN - Oak Ridge Institute For Science And Education (ORISE); Bennett, John; Collum, Tamara; Evans, Breyn; Raines, Charles; Gutierrez, Benjamin; JANISIEWICZ, WOJCIECH - Retired ARS Employee; Jurick Ii, Wayne; Gottschalk, Christopher

Submitted to: Postharvest Biology and Technology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/7/2025
Publication Date: 3/18/2025
Citation: Whitt, L., Bennett, J.S., Collum, T.D., Evans, B.E., Raines, C.D., Gutierrez, B.L., Janisiewicz, W., Jurick Ii, W.M., Gottschalk, C.C. 2025. Genome-wide associations within diverse wild apple germplasm for postharvest blue mold resistance to Penicillium expansum. Postharvest Biology and Technology. 225(113513). https://doi.org/10.1016/j.postharvbio.2025.113513.
DOI: https://doi.org/10.1016/j.postharvbio.2025.113513

Interpretive Summary: Blue mold rot is a fungal disease responsible for major losses in the apple industry due to a lack of natural resistance in our domesticated apple varieties. Previous studies have found some wild apple species within the USDA-ARS apple collection that exhibit natural resistance to blue mold, with varying degrees of resistance among the different apple species. We revisited the USDA-ARS apple collection to sequence the genomes of these apple trees and identify what genes could be responsible for blue mold rot resistance. By combining our new sequencing data with the historical blue mold resistance data, we were able to significantly associate multiple regions of the apple genome with changes in blue mold resistance. These genomic regions also contained many genes known to be involved with disease response, indicating that the beneficial versions of multiple genes are needed for complete resistance to blue mold. These genetic regions serve as markers for breeding programs to identify desirable wild apple trees for bringing blue mold resistance into domesticated apple.

Technical Abstract: Post-harvest disease caused by the blue mold fungus, Penicillium expansum, accounts for a substantial proportion of economic loss in United States apple crop industry. Multiple modes of entry in the apple supply chain, plus emerging fungicide resistance, limit the current and long-term viability of using chemical controls alone. Previous phenotypic screens of Malus accessions in the USDA-ARS apple germplasm have identified varying levels of blue mold disease resistance in some wild apple accessions and hybrids. These wild apple species contain reservoirs of genetic resistance that can be integrated into apple breeding programs to complement the previously identified qM-Pe3.1 marker from Malus sieversii. We sought to identify these novel loci by combining historic phenotypes of the USDA-ARS wild apple germplasm with low-pass genomic sequencing to perform association mapping. Multi-locus mixed models identified five single nucleotide polymorphisms (SNPs) significantly associated to reduced post-harvest rot under high concentrations of P. expansum inoculum, and one SNP associated under low concentrations. Within a 25,000 base pair windows of these SNPs, we found candidate genes encoding proteins with known pathogen immune response roles, such as a PR5-like receptor kinase, locus-receptor-like (LRL) protein kinase, and a putative resistance protein RGA3. Additionally, many candidates had annotations that are likely related to broad-spectrum pathogen resistance, such as those with annotated roles in the cell wall and epidermis secretion. We present these loci as targets for identifying accessions with beneficial alleles that can be targeted for fine mapping along with integration into Malus breeding programs to work towards M. domestica lines with natural post-harvest rot resistance.