Genomic selection analyses reveal tradeoff between chestnut blight tolerance and genome inheritance from American chestnut (Castanea dentata) in (C. dentata x C. mollissima) x C. dentata backcross populations

American chestnut was once a foundation species of eastern North American forests, but was rendered functionally extinct in the early 20th century by an exotic fungal blight (Cryphonectria parasitica). Over the past 30 years, The American Chestnut Foundation (TACF) has pursued backcross breeding to generate hybrids that combine the timber-type form of American chestnut with the blight tolerance of Chinese chestnut. The backcross strategy has been implemented based on the hypothesis that blight tolerance is conferred by few major effect alleles. We tested this hypothesis by developing genomic prediction models for five presence/absence blight phenotypes of 1,230 BC3F2 selection candidates and average canker severity of their BC3F3 progeny. We also genotyped pure Chinese and American chestnut reference panels to estimate the proportion of BC3F2 genomes inherited from parent species. We found that genomic prediction from a method that assumes an infinitesimal model of inheritance (HBLUP) has a similar predictive ability to a method that tends to perform well for traits controlled by major genes (Bayes C). Furthermore, the proportion of BC3F2 trees’ genomes inherited from American chestnut was negatively correlated with the blight tolerance of BC3F2 trees and their progeny. On average, selected BC3F2 trees inherited 83% of their genome from American chestnut and have blight-tolerance that is intermediate between F1 hybrids and American chestnut. Results suggest polygenic rather than major gene inheritance for blight tolerance. The blight-tolerance of restoration populations will be enhanced by advancing additional sources of blight-tolerance through fewer backcross generations and by potentially by breeding with transgenic blight-tolerant trees.