Transgressive segregation, hopeful monsters, and phenotypic selection drove rapid genetic gains and breakthroughs in predictive breeding for quantitative resistance to Macrophomina in strawberry

Authors: KNAPP, STEVEN - University Of California; COLE, GLENN - University Of California; PINCOT, DOMINIQUE - University Of California; DILLA-ERMITA, CHRISTINE - University Of California; BJORNSON, MARTA - University Of California; FAMULA, RANDI - University Of California; GORDON, THOMAS - University Of California; HARSHMAN, JULIA - University Of California; Henry, Peter; FELDMANN, MITCHELL - University Of California

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/15/2023
Publication Date: 1/3/2024
Citation: Knapp, S.J., Cole, G.S., Pincot, D.D., Dilla-Ermita, C.J., Bjornson, M., Famula, R.A., Gordon, T.R., Harshman, J.M., Henry, P.M., Feldmann, M.J. 2024. Transgressive segregation, hopeful monsters, and phenotypic selection drove rapid genetic gains and breakthroughs in predictive breeding for quantitative resistance to Macrophomina in strawberry. Horticulture Research. 11(2). Article uhad289. https://doi.org/10.1093/hr/uhad289.
DOI: https://doi.org/10.1093/hr/uhad289

Interpretive Summary: Macrophomina phaseolina is a soilborne fungus that causes severe and lethal disease on strawberry plants. This pathogen spread to strawberry growing regions worldwide around twenty years ago. Losses to the pathogen have increased as climate change has increased abiotic stresses and the highly effective soil fumigant, methyl bromide, was phased out of use due to its ozone depleting effects. This work identified genetic loci in specific strawberry varieties that are correlated with increased resistance to disease caused by Macrophomina phaseolina. These loci were discovered across multiple years and locations testing for disease resistance in strawberry seedlings from select crosses. The results show that at least three of these favorable alleles must be present in a strawberry plant’s genome to confer robust resistance. Breeding for resistance to Macrophomina can accelerate by screening seedlings for these loci before costly in-field testing.

Technical Abstract: Two decades have passed since the strawberry (Fragaria ' ananassa) disease caused by Macrophomina phaseolina, a necrotrophic soilborne fungal pathogen, began surfacing in California, Florida, and elsewhere. This disease has since become one of the most common causes of plant death and yield losses in strawberry. The Macrophomina problem emerged and expanded in the aftermath of the worldwide prohibition of soil fumigation with methyl bromide, a toxic ozone-depleting substance, and appears to have been aggravated by increased abiotic stress and climate change. Here we show that resistance to Macrophomina, which was rare among strawberry gene bank accessions, can be greatly increased by stacking previously and newly identified favorable alleles. Genetic variants in linkage disequilibrium with the underlying causal loci were uncovered by genome-wide association studies among diverse genetic resources and segregating populations where intense phenotypic selection for increased resistance to the pathogen had been applied under induced drought stress and high summer temperatures. The effects of some of the loci predicted to underlie resistance to Macrophomina were selection cycle specific. They were validated by showing that selection rapidly and significantly increased the frequencies of favorable alleles and that three or more favorable alleles had to be accumulated to surpass the threshold necessary for resistance. A formulaic solution to the Macrophomina disease resistance breeding problem emerged from our studies, which showed that resistant cultivars can be developed by marker-assisted stacking of favorable alleles among five or possibly fewer loci.