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

Abstract

Two decades have passed since the strawberry (Fragaria x 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 wake of the global phase-out of soil fumigation with methyl bromide and appears to have been aggravated by an increase in climate change-associated abiotic stresses. Here we show that sources of resistance to this pathogen are rare in gene banks and that the favorable alleles they carry are phenotypically unobvious. The latter were exposed by transgressive segregation and selection in populations phenotyped for resistance to Macrophomina under heat and drought stress. The genetic gains were immediate and dramatic. The frequency of highly resistant individuals increased from 1% in selection cycle 0 to 74% in selection cycle 2. Using GWAS and survival analysis, we found that phenotypic selection had increased the frequencies of favorable alleles among 10 loci associated with resistance and that favorable alleles had to be accumulated among four or more of these loci for an individual to acquire resistance. An unexpectedly straightforward solution to the Macrophomina disease resistance breeding problem emerged from our studies, which showed that highly resistant cultivars can be developed by genomic selection per se or marker-assisted stacking of favorable alleles among a comparatively small number of large-effect loci.

Acknowledgements

We are grateful for the outstanding support of the field superintendents and staff at the UC Davis Wolfskill Experiment Orchard (Winters, CA), UC Davis Armstrong Plant Pathology Farm (Davis, CA), the UC Agricultural and Natural Resources South Coast Research and Extension Center (Irvine, CA), and Garcia Farms in cooperation with the USDA Agricultural Research Service (Salinas, CA). We especially thank Bryan Pellissier and Alexa Sommers Miller for supporting our disease resistance screening studies at Armstrong Farm. We thank Nayeli Valencia, Eduardo Garcia, and Bruce Campopiano for their assistance with our disease resistance breeding and genetic studies. This research was supported by grants to SJK from the United Stated Department of Agriculture (http://dx.doi.org/10.13039/100000199) National Institute of Food and Agriculture (NIFA) Specialty Crops Research Initiative (SCRI) (#2017-51181B6833), SJK, MJF, DDAP, MB, and PMH from the USDA NIFA SCRI (#2022-51181-38328-0), and SJK, GSC, MJF, DDAP, and MB from the California Strawberry Commission (http://dx.doi.org/10.13039/100006760).

Author Contributions

Conceptualization: SJK, GSC. Data curation: DDAP, RAF, GSC, MB, GSC, CJDE. Formal analysis: GSC, DDAP, CJDE, MB, RAF. Funding acquisition: SJK, GSC, MJF, DDAP, MB, PMH. Investigation: SJK, GSC, GSC. Methodology: DDAP, TRG, PMH, JMH, RAF. Project administration: SJK. Resources: GSC, TRG, PMH. Software: GSC, DDAP, MB. Supervision: SJK, PMH. Validation: SJK, GSC. Visualization: DDAP, GSC, SJK, MB. Writing - original draft: SJK. Writing - review & editing: GSC, DDAP, MB, GSC, CJDE, PMH, SJK.

Data availability statement

The phenotypic and genotypic data and supplemental material for these studies are available in a DRYAD repository (https://datadryad.org/stash/share/HEQtBXc6X04_xAvUyYGxl9AsByEgZswPTIoswt9aEAg).

Conflict of interests

The authors declare no conflicts of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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