Domestication of temperate and coastal hybrids with distinct ancestral gene selection in octoploid strawberry

Authors: HARDIGAN, MICHAEL - University Of California, Davis; POORTAN, THOMAS - University Of California, Davis; ACHARYA, CHARLOTTE - University Of California, Davis; COLE, GLENN - University Of California, Davis; Hummer, Kim; Bassil, Nahla; EDGER, PATRICK - Michigan State University; KNAPP, STEPHEN - University Of California, Davis

Submitted to: The Plant Genome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/26/2018
Publication Date: 11/8/2018
Citation: Hardigan, M., Poortan, T., Acharya, C., Cole, G., Hummer, K.E., Bassil, N.V., Edger, P., Knapp, S.J. 2018. Domestication of temperate and coastal hybrids with distinct ancestral gene selection in octoploid strawberry. The Plant Genome. 11(3):180049. https://doi.org/10.3835/plantgenome2018.07.0049.
DOI: https://doi.org/10.3835/plantgenome2018.07.0049

Interpretive Summary: The Garden strawberry originated as an accidental cross between 2 American species 300 years ago. This is a uniquely short timespan for plant domestication. Since its discovery in the 1750s, migration, selection, and population bottlenecks reshaped strawberry diversity to produce special fruit-bearing groups. Due to DNA complexity, the architecture of historic and modern strawberry populations remained hard to determine. To resolve the impacts of domestication, we analyzed the whole DNA profiles of 1,300 clonally preserved octoploids (1814 - present) including wild species, historic varieties, and University of California germplasm. We discovered that the globally important California strawberry population, adapted to sub-tropical coastal habitats and accounting for up to 60% worldwide consumption, is highly divergent from temperate genotypes originating in eastern North America and Europe. Whereas temperate strawberries were primarily selected from the North American Virginia strawberry, coastal habitats dramatically increased the selection of the beach strawberry, and photoperiod-insensitive flowering from a wild strawberry from mountains in Utah, highlighting the importance of adaptive selection in domestication of this artificial hybrid. Genetic narrowness resulting from selection for enhanced fruit phenotypes in subtropical climates over the last several decades restructured the strawberry genetic composition on a scale equivalent to the first 200 years of breeding. The coastal strawberry is now more diverged from temperate cultivars than the latter from their wild progenitors. We show that strawberry domestication targeted the genes that regulated hormone-mediated fruit expansion, providing a genomic blueprint for identifying genetic factors driving modern cultivars.

Technical Abstract: Garden strawberry (Fragaria × ananassa) originated as a spontaneous hybrid between distinct octoploid species 300 years ago, a uniquely short timespan for plant domestication. Since its discovery in the 1750s, migration, selection, and population bottlenecks reshaped strawberry genetic diversity to produce elite fruit-bearing groups constituting a hybrid complex. Due to polyploid genome complexity, the genetic architecture of historic and modern strawberry populations remained elusive. To resolve the impacts of domestication on strawberry genetic diversity, weanalyzed genome-wide DNA profiles of 1,300 clonally preserved octoploids (1814 - present) including wild species, historic varieties, and University of California germplasm. We discovered that the globally important California population, adapted to sub-tropical coastal habitats and accounting for up to 60% worldwide consumption, is highly divergent from temperate genotypes originating in eastern North America and Europe. Whereas temperate octoploids primarily selected North American F. virginiana subsp. virginiana ancestral diversity, coastal habitats dramatically increased selection of F. chiloensis (beach strawberry) alleles, and photoperiod-insensitive flowering from non-ancestral F. virginiana subsp. glauca, highlighting the importance of adaptive selection in domestication of this artificial hybrid. Genetic bottlenecks resulting from selection for enhanced fruit phenotypes in subtropical climates over the last several decades have restructured octoploid strawberry genetics on a scale equivalent to the first 200 years of breeding; coastal strawberry is now more diverged from temperate cultivars than the latter from their wild progenitors. We show that strawberry domestication targeted genes regulating hormone-mediated fruit expansion, providing a genomic blueprint for identifying genetic factors driving elite modern phenotypes.