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. 2018 Nov 1;11(3):180049. doi: 10.3835/plantgenome2018.07.0049

Domestication of Temperate and Coastal Hybrids with Distinct Ancestral Gene Selection in Octoploid Strawberry

Michael A Hardigan 1,✉, Thomas J Poorten 1, Charlotte B Acharya 1, Glenn S Cole 1, Kim E Hummer 2, Nahla Bassil 2, Patrick P Edger 3, Steven J Knapp 1,✉
PMCID: PMC12810100  PMID: 30512037

Abstract

Garden strawberry (Fragaria × ananassa Duchesne ex Rozier) arose from spontaneous hybridization of distinct octoploid species 300 yr ago. Since its discovery in the 1700s, migration and selection restructured the genetic diversity of early hybrids to produce elite fruit‐bearing groups. Breeders’ understanding of the genetic architecture of domesticated populations is incomplete. To resolve the impacts of domestication on strawberry genetic diversity, we analyzed genome‐wide DNA profiles of 1300 octoploid individuals (1814–present), including wild species, historic varieties, and the University of California germplasm collection. Commercially important California genotypes, adapted to mild coastal climates and accounting for a large fraction of global production, have diverged from temperate cultivars originating in eastern North America and Europe. Whereas temperate cultivars were shown to have selected North American Fragaria virginiana Miller ssp. virginiana ancestral diversity at higher frequencies, coastal breeding increased selection of Fragaria chiloensis (L.) Miller (beach strawberry) alleles in F. × ananassa, in addition to photoperiod‐insensitive flowering alleles from nonancestral F. virginiana (S.Watson) Staudt ssp. glauca, underscoring the role of continued adaptive introgressions in the domestication of artificial hybrids. Selection for mass production traits in coastal climates over the last 20 to 30 yr has restructured domesticated strawberry diversity on a scale similar to the first 200 yr of breeding; coastal F. × ananassa has diverged further from temperate F. × ananassa than the latter from their wild progenitors. Selection signatures indicate that strawberry domestication targeted genes regulating hormone‐mediated fruit expansion, providing a blueprint for genetic factors underlying elite phenotypes.

Abbreviations

π

marker diversity

CC‐F×a

California coastal Fragaria × ananassa

FST

population genetics F‐statistic

GO

Gene Ontology

QTL

quantitative trait locus

SNP

single nucleotide polymorphism

TM‐F×a

temperate Fragaria × ananassa

UCD

University of California Davis

Core Ideas

  • Genetic restructuring yielded distinct temperate and coastal‐adapted subpopulations.

  • Ancestral species selection bias was discovered in temperate and coastal octoploids.

  • Flowering and fruit development genes targeted during strawberry domestication were identified.

Garden strawberry (Fragaria × ananassa) began its domestication as an interspecies hybrid approximately 300 yr ago (Hancock et al., 2008). Forgoing the dominant crop model involving millennia of selection and expansion from a geographic origin of diversity (Meyer and Purugganan, 2013), F. × ananassa domestication arose from a chance cross in an artificial European environment, the gardens at the Palace of Versailles, between nonsympatric New World octoploids: F. chiloensis ssp. chiloensis from Chile and F. virginiana ssp. virginiana from the eastern United States and Canada (Duchesne, 1766). European F. × ananassa hybrids were introduced to North America in the 1800s, where native populations of both parent species provided additional genetic diversity in the form of subspecific ecotypes adapted to a wide range of environments (Darrow, 1966; Fletcher, 1917; Stauct, 1989). Strawberry breeders exploited these wild populations to further improve the performance of cultivated F. × ananassa hybrids (Darrow, 1966; Fletcher, 1917; Hummer and Hancock, 2009).

From historical records (Darrow, 1966; Hancock et al., 2008, 2010; Harrison et al., 1997), the F. × ananassa genome represents an artificial complex of haplotypes from wild octoploids of diverse geographic and subspecific origins. Three centuries of hybridization, migration, and selection have produced distinct but poorly understood group structures. Since the 1950s, breeding at the University of California, Davis (UCD) founded a commercially important F. × ananassa population, accounting for a large fraction of U.S. production (Bennett and Carriere, 2007). Unlike more historic F. × ananassa genotypes grown under temperate conditions [temperate F. × ananassa (TM‐F×a)], California coastal F. × ananassa (CC‐F×a) have been adapted to ocean‐buffered environments with extended growing seasons and mild winters. Genes targeted by selection for high yield and marketable fruit quality (firmness, extended shelf‐life) in the CC‐F×a population have not been identified. Historically, the octoploid strawberry genome has complicated the study of underlying genetic diversity on a genome‐wide scale (Chandler et al., 2012; Shulaev et al., 2008), obscuring patterns of selection and substructuring that arose during domestication (Sjulin and Dale, 1987). To address this, we performed a study of wild progenitor ecotypes and available cultivated octoploids selected in the last 200 yr, a period spanning the majority of F. × ananassa domestication history (Darrow, 1966).

We investigated genetic relationships, population structure, and selected gene functions in a panel of 1300 octoploid Fragaria genotypes to understand how strawberry breeding reshaped F. × ananassa from 18th‐century hybrids. The panel included 100 F. chiloensis and F. virginiana accessions, 157 heirloom cultivars from the USDA‐ARS National Plant Germplasm System representing TM‐F×a (temperate genotypes), and the complete UCD strawberry germplasm collection representing CC‐F×a (California coastal genotypes). Analysis of octoploid DNA profiles from 16,492 subgenome‐specific variants anchored to an improved diploid reference genome (Edger et al., 2017) resolved postdomestication restructuring events and patterns of gene selection underlying modern strawberry cultivars. We discovered that breeding for temperate and coastal environments, the latter now a source of 80 to 90% of U.S. production, produced genetically distinct F. × ananassa subpopulations with increased frequencies of alleles inherited from different ancestral species (F. virginiana and F. chiloensis). Divergence of the coastal and temperate domesticated populations exceeded the divergence of temperate F. × ananassa from the wild octoploid progenitor species. This may be partly adaptive, as coastal genotypes have overaccumulated F. chiloensis alleles as they diverged from heirloom temperate genotypes showing nearly exclusive selection of F. virginiana alleles. We show that introgression of the day‐neutral flowering trait from nonancestral F. virginiana ssp. glauca (Ahmadi et al., 1990; Bringhurst and Voth, 1980) into CC‐F×a promoted a transition to a different single‐locus source of late‐season flowering. Selection signatures were analyzed against genes regulating flowering, fruit quality, hormone‐induced ripening, and volatile biosynthesis, as well as flower and fruit developmental transcriptomes (Hollender et al., 2014; Kang et al., 2013), identifying candidate gene functions controlling elite traits in modern cultivars.

Postdomestication introgressions from additional octoploid subspecies helped catalyze the formation of a distinct coastal F. × ananassa population. Our findings support ancestral species adaptation as a determinant of allelic selection during this process. This study provides a genomic framework for understanding the evolution of F. × ananassa, a recently domesticated artificial hybrid, and identifies gene functions that are important for breeding elite fruit‐bearing cultivars.

MATERIALS AND METHODS

Genotyping the Octoploid Diversity Panel

The diversity panel contained 1300 octoploid genotypes including wild accessions and clonally preserved F. × ananassa genotypes. Wild accessions included ecotypes of South American F. chiloensis ssp. chiloensis, North American F. chiloensis (ssp. lucida and pacifica) and F. virginiana (ssp. glauca, grayana, platypetala, and virginiana) (Supplemental Table S1). Cultivated genotypes included the complete strawberry collection housed at UCD up to 2011, and a diversity panel from the USDA germplasm repository (Corvallis, OR) containing heirloom cultivars and genotypes from 20th‐century U.S., Canadian, and European breeding programs. University of California germplasm represented CC‐F×a, genotypes grown for California coastal production, whereas cultivars obtained from the USDA germplasm repository represented TM‐F×a, the majority being older 19th‐ and 20th‐century varieties developed by breeders in Europe, Canada, and the northern United States. DNA samples were obtained from immature leaf tissue with an E‐Z 96 Plant DNA Kit (Omega Bio‐Tek, Norcross, GA). The protocol was modified to include the use of Proteinase K, a separate RNase treatment and additional spin, and heated incubation steps during elution. Variants primarily consisting of single nucleotide polymorphisms (SNPs) were assayed on the Axiom IStraw35 array (Affymetrix Inc., Santa Clara, CA) (Verma et al., 2016) and processed with the Axiom Analysis Suite (Affymetrix Inc.), identifying 16,492 polymorphic and subgenome‐specific markers (Supplemental File S1).

Population Structure and Diversity Estimates

Markers were analyzed in the R package SNPRelate (Zheng et al., 2012) for estimating FST, linkage disequilibrium, linkage disequilibrium‐pruning, and principal component analysis. Linkage disequilibrium‐pruning was used to subsample 3780 markers (R 2 < 0.50) with reduced linkage. Linkage disequilibrium‐pruned markers were used to evaluate population structuring via principal component analysis (SNPRelate) and STRUCTURE version 2.3.4 (https://web.stanford.edu/group/pritchardlab/structure_software/release_versions/v2.3.4/html/structure.html, accessed 3 Oct. 2018), testing K = 2 to 14 with an admixture model (20,000 burn‐in steps, 50,000 Markov chain Monte Carlo steps), performing 10 replicates per K‐value. The most likely number of populations was determined with STRUCTURE HARVESTER (version 0.6.94), as described in Evanno et al. (2005), with sample orders calculated with CLUMPP version 1.1.2 (https://rosenberglab.stanford.edu/clumpp.html, accessed 3 Oct. 2018). Marker diversity (π) was estimated with TASSEL version 5.2.39 (http://www.maizegenetics.net/tassel, accessed 3 Oct. 2018).

Phylogenetic Analysis

Genotypes were converted to gene frequency format for analysis in PHYLIP version 3.696 (http://evolution.genetics.washington.edu/phylip/, accessed 3 Oct. 2018). Genetic distance matrices and corresponding neighbor‐joining trees were calculated via 1000 bootstrap replicates to produce a consensus tree structure. Trees were rooted and visualized with the Interactive Tree of Life tool (itol.embl.de, accessed 19 Sept. 2018).

Flowering Time Genome‐Wide Association Studies

Flowering time phenotypes were collected in 2016 at the Wolfskill experiment station located in Winters, CA. The trait was measured categorically by the presence or absence of flowering and fruit production in fall months, with genotypes flowering in September and November scored as day‐neutral. Genome‐wide association was tested across 14,606 markers with TASSEL (version 5.2.39) via a mixed linear model accounting for population structure and kinship. Marker significance was determined from a Bonferroni‐corrected p‐value (P < 3.423 × 10–6).

Fruit Quality Gene Candidates

Markers yielding the top 5% values for two‐population FST estimates or progenitor–descendant nucleotide diversity ratios (πP:πD) were categorized under putative selection. Markers in the top percentile with a population genetics F‐statistic (FST) of <0.20 and a relative diversity of <2.0 were treated as nonsignificant and excluded from analysis of local gene function. Because of a high frequency of monomorphic variant sites in post‐2000 CC‐F×a, markers with nucleotide diversity below 0.20 in this group were not used to test for selection between day‐neutral and short‐day genotypes. Similarly, markers with low nucleotide diversity (π < 0.10) in the wild progenitors were excluded from domestication‐related selection tests. For analysis of local candidate gene functions, IStraw35 probe sequences (Affymetrix Inc.) were anchored to an improved diploid Fragaria vesca L. reference genome (FvH4.1) (Edger et al., 2017) via BLAST (Supplemental Table S2). Genes within 10 to 20 kb of selected markers were screened as candidates for selected gene functions.

Fragaria vesca Candidate Genes

Candidate genes controlling plant flowering and maturity pathways, fruit ripening and quality, hormone‐induced ripening, and volatile biosynthesis genes were compiled from published literature. Candidate gene protein sequences from the original F. vesca version 1.0 reference annotation (Shulaev et al., 2011) were aligned to the F. vesca FvH4.1 proteome (Edger et al., 2017) with BLAST, and used to identify genes in the newer assembly representing best‐hit loci or alternate genes with significant homology (e‐value < 1 × 10–50). Enrichment of specific Gene Ontology (GO) functions among selected gene candidates was determined via Fisher's Exact Test.

Reproductive Tissue Expression

Reproductive gene expression categories were obtained from Kang et al. (2013) and Hollender et al. (2014), based on flower and fruit transcriptome studies that identified genes as demonstrating tissue‐ and stage‐specific expression within strawberry reproductive organs, or comprising expression modules associated with reproductive development. Gene IDs from the original diploid reference annotation (version 1.0) were replaced by their best‐match in the FvH4.1 annotation. Enrichment of reproductive expression groups in selected gene sets was determined via Fisher's Exact Test.

RESULTS AND DISCUSSION

Genetic Restructuring of Coastal F. × ananassa

We evaluated restructuring of genetic diversity in the F. × ananassa hybrid complex following strawberry domestication. Neighbor‐joining analysis of octoploid Fragaria samples distinguished hybrid progenitor species F. chiloensis from TM‐F×a genotypes, whereas the hybrid progenitor F. virginiana was resolved as a distinct branch inside the TM‐F×a clade (Fig. 1). Genetic distances supported an allelic bias toward F. virginiana among TM‐F×a genotypes (Supplemental Table S3). Early F. × ananassa breeding in the United States and England frequently used F. virginiana ecotypes because of geographic availability and better adaptation to northern climates (Bunyard, 1915; Darrow, 1966; Fletcher, 1917). Recurrent use of northern‐adapted hybrids probably produced the larger F. virginiana genetic footprint observed in the broader TM‐F×a group. The abundance of F. virginiana ssp. virginiana populations in the eastern United States allows for bidirectional gene flow as a contributing factor for TM‐F×a genotypes. Octoploid trees based on the full strawberry panel (Fig. 1) and a subpanel (n = 418) with equal numbers of genotypes from the TM‐F×a and CC‐F×a populations (Supplemental Fig. S1A) indicated that they began diverging as early as the 1950s, separating coastal‐adapted genotypes from their older North American and European founders.

Fig. 1.

Fig. 1

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Neighbor‐joining tree of 1300 octoploid strawberry genotypes. Tree topology is a consensus of 1000 bootstrap datasets estimated from 16,492 markers.

Population stratification in the subpanel (optimal group [K] = 6) (Supplemental Fig. S1C) revealed F. virginiana admixture in TM‐F×a and clearly demonstrated the restructuring of CC‐F×a from TM‐F×a following the 1950s, with no evidence of CC‐F×a admixture by the 21st century. Principal component clustering of genotypes from the full octoploid panel (Fig. 2) showed a limited convergence of post‐1970 CC‐F×a and TM‐F×a genotypes, with greater separation from TM‐F×a and progressively tighter CC‐F×a clustering over time, suggesting that a genetic bottleneck coincided with branching of the California coastal lineage in the late 1900s. Average nucleotide diversity within CC‐F×a has decreased over time (πCC>2000:πCC<1970 = 0.796), as well as CC‐F×a diversity relative to TM‐F×a (πCC>2000:πTM = 0.787) (Supplemental Fig. S2A); however these values did not support a large population bottleneck during coastal F. × ananassa restructuring. It is notable that the genetic diversity of early CC‐F×a germplasm (pre‐1970) was equal to TM‐F×a (πCC<1970:πTM = 0.988), particularly because the CC‐F×a germplasm represents a single breeding program (UCD), whereas TM‐F×a represents genotypes from numerous programs across Europe, Canada, and the United States (Supplemental Table S1). Despite some loss of diversity over time, CC‐F×a genotypes were generally more heterozygous than TM‐F×a genotypes, a pattern extending back to the 1960s (Supplemental Fig. S2C).

Fig. 2.

Fig. 2

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Sample clustering using variance components estimated by principal component analysis (PCA) of 1300 octoploid genotypes.

Single nucleotide polymorphism ascertainment bias is unlikely to have skewed interpretations of genetic diversity in F. × ananassa, as the majority of octoploids used to design the IStraw35 array were not CC‐F×a genotypes from UCD (Bassil et al., 2015). However, less total diversity was observed among F. chiloensis and F. virginiana ecotypes (a proxy for early‐generation F. × ananassa) than CC‐F×a or TM‐F×a (Supplemental Fig. S2A), indicating significant array bias between wild and domesticated genotypes. As a result, no inferences were made pertaining to relative total diversity between wild progenitors and F. × ananassa. Genotype clustering of F. × ananassa samples projected onto principal coordinates estimated from the wild progenitors (Supplemental Fig. S1B) offered poor resolution of TM‐F×a and CC‐F×a germplasm, despite Principal Component 1 and Principal Component 2 accounting for a large fraction of progenitor variance (45.5%). This suggests low F. × ananassa variation at loci distinguishing the wild species, although the CC‐F×a population appeared more intermediate to the progenitor species than TM‐F×a.

Estimates of pairwise FST between octoploid populations showed that the extent of F. × ananassa genetic restructuring that gave rise to CC‐F×a may have exceeded the first 200 yr of strawberry breeding (Fig. 3). The divergence of modern (post‐2000) CC‐F×a genotypes from the more historic TM‐F×a population (CC‐F×a 2000 vs TM‐F×a: FST = 0.207) exceeded the divergence of TM‐F×a from the combined F. chiloensis–F. virginiana progenitors (TM‐F×a vs. wild progenitors: FST = 0.182), with the latter estimate approximating the impact of strawberry breeding on allele frequencies of the original 18th‐century hybrids. Modern CC‐F×a divergence from the wild progenitors was twice that of TM‐F×a (post‐2000 CC‐F×a vs. wild progenitors: FST = 0.375) (Fig. 3). Moreover, CC‐F×a genotypes showed a high frequency of fixed or nearly‐fixed variant loci relative to the wild species (Supplemental Fig. S2B). Pre‐1970 CC‐F×a genotypes were closer to TM‐F×a than post‐2000 CC‐F×a genotypes (Fig. 3), indicating that F. × ananassa restructuring and formation of the California coastal subpopulation continued until the late 20th century.

Fig. 3.

Fig. 3

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Population divergence [Weir&Hill F‐statistic (FST), arrow labels) of wild progenitor species (combined South American F. chiloensis and F. virginiana), temperate F. × ananassa (TM‐F×a), California coastal (CC‐F×a) (pre‐1970), and CC‐F×a (post‐2000). Internal values reflect average marker diversity (π) within the populations.

Germplasm clustering based on population stratification in the full CC‐F×a panel showed that genetic diversity within the California coastal population has been restructured across time, with genotypes stretched from early to modern (Fig. 4A, 4C). Older CC‐F×a genotypes have diverged least from the TM‐F×a founders (Group 2; Fig. 4A), which clustered with F. virginiana, whereas North and South American F. chiloensis ecotypes collapsed into a single group (Group 1; Fig. 4A). Since the introduction of the first strongly day‐neutral cultivars (Ahmadi et al., 1990; Bringhurst and Voth, 1976; Sjulin, 2006), the frequency of day‐neutral flowering genotypes has increased dramatically in the CC‐F×a population (Fig. 4B, 4C) as the commercial importance of day‐neutral production increased in California. Population clusters corresponding to coastal California F. x ananassa genotypes (Groups 3, 4, 5, and 6; Fig. 4A) were partitioned along a time gradient, with the frequency of day‐neutral flowering increasing in the more modern groups. This supports the hypothesis that coastal breeding restructured genetic diversity in the CC‐F×a population more significantly than TM‐F×a, and that selection for day‐neutral flowering has been an important factor in restructuring of the CC‐F×a population to take advantage of an extended coastal growing season (Hancock et al., 2008; Sjulin, 2006).

Fig. 4.

Fig. 4

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Population substructuring based on 1300 octoploid strawberry genotypes. (A) Q‐sorted clustering (K = 6) of octoploid strawberry genotypes into subpopulations. (B) Summary of germplasm composition, University of California Davis (UCD) contribution, cultivar contribution, and frequency of day‐neutral flowering in octoploid subpopulations. (C) Distribution of release year and flowering phenotype in octoploid subpopulations.

Genetics of Day‐Neutral Flowering

To identify selected loci controlling variance for flowering time, we evaluated selective sweeps comparing short‐day flowering genotypes to pre‐1990 and modern (post‐2000) subsets of day‐neutral genotypes, and performed parallel genome‐wide association studies in the same groups. Pre‐1990 day‐neutral genotypes were developed by Royce Bringhurst, who discovered and introduced the high‐elevation F. virginiana ssp. glauca source of photoperiod‐insensitive flowering to California (Ahmadi et al., 1990; Bringhurst and Voth, 1976, 1980). Genome‐wide association of markers in the post‐2000 subset identified a haploblock of SNPs in linkage disequilibrium with a quantitative trait locus (QTL) affecting photoperiod sensitivity (Fig. 5C). The QTL mapped to the Mb 29 to 33 region of chromosome 4 (Fvb4) in the diploid genome (Edger et al., 2017). The QTL was not present in the pre‐1990 day‐neutral subset, confirming that the source of day‐neutral flowering changed as CC‐F×a was restructured over time. Putatively selected variants (top fifth percentile based on short‐day vs. day‐neutral FST) co‐localized with significant QTL variants in the Mb 29 region (Fig. 5A). This region contains numerous duplicated CYP72 family genes with close homology to PHYB ACTIVATION TAGGED SUPPRESSOR 1 (BAS1/CYP72B1) (Supplemental Table S4). The BAS1 gene has been shown to modulate photomorphogenic traits, including floral induction, by interacting with PHYTOCHROME B to regulate brassinosteroid‐mediated phase transition in the apical meristem (Sandhu et al., 2012; Turk et al., 2005). Disruption of PHYTOCHROME B light‐sensing and signaling in rice (Oryza sativa L., se5 mutant) has been shown to result in day‐neutral flowering (Izawa et al., 2000; Osugi et al., 2011). Neither pre‐1990 nor modern QTL regions for day‐neutrality corresponded to the TERMINAL FLOWERING1 locus controlling the trait in diploid ancestor F. vesca (Iwata et al., 2012, Koskela et al., 2012).

Fig. 5.

Fig. 5

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Selective sweeps and genome‐wide association studies (GWAS) for day‐neutral flowering in octoploid strawberry. (A) Genome‐wide allele selection signatures (Weir&Hill F‐statistic, FST) comparing short‐day flowering octoploids with pre‐1990 and post‐2000 d‐neutral octoploids. (B) Manhattan plot of marker significance for GWAS of short‐day and pre‐1990 day‐neutral F. × ananassa genotypes. (C) Manhattan plot of marker significance for GWAS of short‐day and post‐2000 day‐neutral F. × ananassa genotypes.

Unlike modern F. × ananassa, genome‐wide association studies of pre‐1990 germplasm identified a strong QTL on chromosome 3 and several less‐significant QTLs on other chromosomes, in addition to selective sweeps on multiple chromosomes (Fig. 5A,B). Allelic selection (FST) was stronger for selective sweeps in pre‐1990 germplasm, despite having weaker QTL effects than the Fvb4:Mb29–33 QTL in modern germplasm (Fig. 5B). However, most selective sweeps in the pre‐1990 germplasm demonstrated no clear association with a QTL, probably representing other genes unrelated to flowering time that are highly structured among historic day‐neutral cultivars. Weak selective pressure around the Fvb4:Mb29–33 QTL was expected because the favorable allele is dominant (Ahmadi et al., 1990; Perrotte et al., 2016), such that the favorable allele has not been driven to fixation. Kloosterman et al. (2013) made similar observations in tetraploid potato (Solanum tuberosum L.), where heterozygous disruption of the short‐day maturity locus haplotype proved sufficient for flowering and tuberization under long days. The single modern day‐neutral QTL region (Fvb4:Mb 29–33) housed two clusters of significant markers at Mb 29 and Mb 32 to 33 (Supplemental Table S5A). Both contained loci in strong negative linkage among day‐neutral genotypes (linkage disequilibrium below ‐0.9; Supplemental Table S5A), a condition that can arise when beneficial epistatic allele combinations become fixed at interacting loci under selection (Silvela et al., 1999). Significant markers in the Fvb4:Mb 29–33 region were scanned against two octoploid F2 genetic maps from the cultivars Fronteras and Portola (Pincot et al., 2018) to address chromosomal ambiguity arising from anchoring to a diploid genome and to resolve the marker phase. This confirmed that significant markers in the modern day‐neutral QTL region are tightly linked in repulsion on a single octoploid homeolog, LG4A (Bassil et al., 2015) (Supplemental Table S5A). We assessed phase‐corrected marker genotypes in the Fvb4:Mb 29–33 region, comparing modern CC‐F×a day‐neutral genotypes (substructure Groups 5 and 6) and historic short‐day genotypes (substructure Group 2). Modern day‐neutral genotypes primarily showed retention of contiguous haplotype blocks in the respective Mb 29 and Mb 32 to 33 marker clusters, whereas short‐day flowering genotypes exhibited frequent recombination in both marker clusters (Supplemental Table S5B). These contrasting QTL profiles indicate that selection for day‐neutral flowering has strongly suppressed recombination in the Fvb4:Mb 29–33 region. We observed retention of specific Mb 29 × Mb 32 to 33 haplotype combinations among day‐neutral cultivars (Supplemental Fig. S3, Supplemental Table S5C), supporting the possibility that multiple variants in this region influenced photoperiod‐insensitive flowering in modern CC‐F×a octoploids.

Photoperiod‐insensitive flowering (day‐neutrality) enables almost year‐round strawberry production by extending fruit development into summer and fall in the mild coastal environments of central California. These results demonstrate that selection for day‐neutrality in CC‐F×a promoted a transition from older, possibly diverse mechanisms of photoperiod‐insensitivity to reliance on a newer single‐locus mechanism. The Fvb4:Mb 29–33 region corresponds to the FaPFRU locus mapped by Perrotte et al. (2016) and recently identified as the primary QTL for flowering time in U.S. breeding populations (Verma et al., 2017). Low IStraw35 marker density in the Fvb4:Mb 29–33 region did not allow testing for the FLOWERING LOCUS T gene candidate (FvH4_4g30710) postulated by Perrotte et al. (2016) (Supplemental Table S4). Future application of high‐density markers on an octoploid genome assembly will assist fine‐mapping of the candidate genes underlying this trait. Based on its impact on the restructuring of CC‐F×a genetics in recent decades and support for the dominant gene action of the underlying locus (Ahmadi et al., 1990; Bringhurst et al., 1988; Perrotte et al., 2016), this prevalent mechanism of day‐neutral flowering almost certainly descends from the ‘Wasatch source’, a Rocky Mountain ecotype of nonprogenitor F. virginiana ssp. glauca (Ahmadi et al., 1990; Bringhurst and Voth, 1976) first introduced to CC‐F×a in the 1950s. It is notable that a significant QTL signal for this now‐dominant mechanism did not emerge until half a century following its introduction; however, independent mapping of this locus by multiple research groups suggests that the original CC‐F×a mechanism has since become a prevalent source of day‐neutrality for breeders.

Genome Targets of Domestication and Breeding

To identify genomic regions that came under selection during F. × ananassa domestication, we performed two‐population selection tests comparing cultivated genotypes (TM‐F×a, pre‐1970 CC‐F×a, post‐2000 CC‐F×a, and UCD cultivars) to wild Fragaria ecotypes. We then compared TM‐F×a and CC‐F×a to identify loci that later came under selection as a result of population restructuring within F. × ananassa. Based on the IStraw35 array design with octoploid DNA variants called in F. vesca coding sequences (Bassil et al., 2015), we evaluated FvH4.1 gene annotations in close proximity (10–20 kb) to putatively selected loci as candidate functions targeted as a result of F. × ananassa breeding. Genes previously linked to strawberry reproductive traits were screened against putatively selected loci, including flowering and maturity response (Supplemental Table S6), fruit ripening and quality (Supplemental Table S7), fruit volatile biosynthesis (Supplemental Table S8), and hormone pathway genes shown to be upregulated in reproductive tissues after fertilization (Supplemental Table S9).

We found that TM‐F×a shared a limited fraction of putative domestication‐selected loci with CC‐F×a genotypes: 28.7 and 31.8% for pre‐1970 and post‐2000 CC‐F×a, respectively. These values decreased to 11.7 and 7.0% in the top percentile of selected variants. This suggested that coastal‐adapted octoploids arising from 20th‐century restructuring of F. × ananassa not only represent a distinct subpopulation but, to a certain degree, they also rely on different mechanisms for performance from their temperate founders. Within the set of candidate genes controlling hormone biosynthesis and signaling in developing reproductive tissues (Kang et al., 2013), a larger fraction was associated with loci selected in CC‐F×a (Supplemental Fig. S4) and most were exclusively selected in the coastal population (Supplemental Table S9). This could indicate that selection for mass production phenotypes in coastal environments expanded the regulation or coordination of hormone signaling pathways controlling strawberry fruit development (Kang et al., 2013).

Because of the large number of U.S. strawberries shipped from California, modern CC‐F×a genotypes have undergone intense selection to produce large, firm receptacles with extended shelf‐life and delayed postharvest deterioration. The basis of their enhanced marketable quality is uncertain, although genes encoding cell‐wall‐degrading enzymes (pectinesterase, pectate lyase, and polygalacturonase) are of interest because of their impact on fruit texture (Castillejo et al., 2004; Goulao and Oliveira, 2008; Sesmero et al., 2007). The highest number of fruit ripening and quality gene candidates colocalized with selected variants distinguishing modern CC‐F×a from TM‐F×a, its domesticated progenitor group, rather than wild species (Supplemental Fig. S4, Supplemental Table S7); however, the subset functioning specifically in cell wall metabolism did not show expanded selection in CC‐F×a. A larger number of cell‐wall metabolism candidates colocalized with TM‐F×a domestication loci (Supplemental Table S7). Evaluation of GO annotations at loci distinguishing TM‐F×a or CC‐F×a from wild ecotypes found no enrichment for enzymatic functions affecting fruit quality (Supplemental Table S10). Expansion of CC‐F×a selection signatures in proximity to genes regulating hormone biosynthesis and signaling in developing fruit suggests that higher‐level regulatory mechanisms controlling berry development may have influenced the fruit quality of modern cultivars as strongly as structural enzymes within ripening pathways.

Redirected Ancestral Selection in Hybrids

Regarding the marketable fruit quality of modern CC‐F×a, many South American F. chiloensis populations produce larger fruit with better firmness than North American F. virginiana populations due to native landrace selection (Bringhurst and Voth, 1960; Hancock et al., 1999). Genetic distances (Supplemental Table S3) and population structuring (Fig. 2, Supplemental Fig. S1) suggested that F. chiloensis contributions to F. × ananassa were less prominent following early domestication (Dale and Sjulin, 1990; Hancock et al., 1999; Hancock and Luby, 1993; Sjulin and Dale, 1987). This could relate to a low tolerance of ocean‐buffered South American F. chiloensis to the seasonal temperature extremes of breeding environments in England and the northeastern United States, where genetic gains were most rapid in the early to mid‐1800s (Darrow, 1957, 1966; Hancock et al., 1999). In the 1890s, California frontiersman Albert Etter began breeding old F. × ananassa varieties with native and South American beach strawberries (Darrow, 1966), establishing F. chiloensis haplotypes in germplasm that became UCD founder lines under breeders Harold E. Thomas and Earl V. Goldsmith (Sjulin, 2006).

We investigated whether postdomestication F. chiloensis introgressions could have influenced F. × ananassa restructuring by comparing hybrid progenitor frequencies of alleles selected in CC‐F×a and TM‐F×a. This uncovered distinct profiles of ancestral allele selection in the F. × ananassa subpopulations. Temperate F.× ananassa showed nearly exclusive targeting of F. virginiana species‐specific alleles or alleles that were more prevalent in the North American progenitor (Fig. 6). This ancestral allele profile was reversed in coastal F. × ananassa; F. virginiana‐specific alleles were largely eliminated from loci under selection in the CC‐F×a population, which instead showed an enrichment of F. chiloensis species‐specific alleles and alleles with balanced progenitor frequencies. Adapting F. × ananassa for optimized mass production traits in coastal environments has eroded the F. virginiana ancestral gene bias in older TM‐F×a genotypes, while expanding selection of F. chiloensis ancestral alleles in the California germplasm has been a source of numerous commercially important cultivars (Fig. 6).

Fig. 6.

Fig. 6

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Distribution of hybrid progenitor allele frequency (South American F. chiloensis and North American F. virginiana) for the top 5% putatively selected markers when testing the domestication of temperate F. × ananassa (TM‐F×a) from wild species and the divergence of California coastal F. × ananassa (CC‐F×a) from TM‐F×a.

Gene functions associated with CC‐F×a F. chiloensis‐specific alleles support the likelihood that beach strawberry contributed variation influencing fruit quality in California germplasm. In contrast with domestication‐related loci, F. chiloensis‐specific alleles that were selected during the restructuring of CC‐F×a from TM‐F×a were associated with genes enriched for enzymatic functions affecting fruit ripening and quality (Supplemental Table S11). The top F. chiloensis‐derived functions identified in pre‐1970 CC‐F×a genotypes included pectinesterase activity (GO:0030599) and enzyme inhibitor activity (GO:0004857; P < 0.00001),which are functions associated with fruit firmness, and O‐methyltransferase activity (GO:0008171; P < 0.00001), an enzymatic step in the biosynthesis of furanones, which are important strawberry flavor volatiles (Zorrilla‐Fontanesi et al., 2012). In modern (post‐2000) CC‐F×a, the most strongly selected functions were related to oxidative stress and nucleic acid metabolism. Oxidative stress response is an important determinant of extended postharvest quality in fruit (Hodges et al., 2004).

Reproductive Expression Profiling of Domestication Genes

Given the importance of receptacle size and yield in strawberry breeding, genes controlling reproductive organ development are potential targets for domestication. Fruit yield and fresh weight are correlated with the number of initiated and fertilized flower ovules (achenes) whose development controls receptacle expansion via auxin and gibberellic acid biosynthesis (Abbott et al., 1970; Kang et al., 2013; Webb et al., 1978). We used comprehensive flower and fruit development transcriptomes from F. vesca (Hollender et al., 2014; Kang et al., 2013) to identify groups of genes with reproductive tissue‐ or stage‐specific expression or comprising expression network modules controlling reproductive organ development (Supplemental File S2). Multiple reproductive expression groups were enriched in genes associated with putative domestication loci. The four most enriched expression groups were identical in all domestication‐related selection tests (Supplemental Table S12). These included genes differentially expressed in the ghost (seed coat and endosperm) and embryo during achene development (Expression Group 112), genes downregulated in developing embryos (Expression Group 109), the subset of genes that were more abundant in the ghost than in the embryo (Expression Group 114), and genes that were differentially expressed in mature pollen and late‐stage anthers housing mature pollen (Expression Group 3). Ghost‐abundant transcription was the most significantly enriched expression group for gene candidates in every domestication test. Kang et al. (2013) demonstrated that auxin and gibberellic acid biosynthesis and signaling genes controlling fertilization‐induced receptacle enlargement were activated in the achene but expressed primarily in the ghost rather than the embryo, with many exhibiting coordinated opposite expression during achene development. Enrichment of ghost‐abundant and embryo‐downregulated expression groups shows that genes upregulated in tissues responsible for hormone‐induced fruit expansion are highly represented in genomic regions distinguishing wild and domesticated strawberry populations.

CONCLUSIONS

Our study of subgenome‐specific polymorphism in a broad cross‐section of octoploid Fragaria shows how strawberry breeding altered the genetic structure of early F. × ananassa hybrids. The first hybrids were intermediates of South American F. chiloensis and North American F. virginiana; however, by the 1900s, most F. × ananassa cultivars were more closely related to the North American parent. This preference for F. virginiana is notable because the South American F. chiloensis progenitor was a landrace cultivated by Chilean natives, with selection for agriculturally beneficial alleles predating F. × ananassa by more than 1000 yr (Finn et al., 2013; Hancock et al., 1999). The dominance of the F. virginiana parent genome among TM‐F×a genotypes suggests that the need for regionally adaptive genetic variation was important for early strawberry breeding. Breeding in the 1800s was prominent in England and the northeastern United States, where F. chiloensis ssp. chiloensis was poorly suited to colder climates.

Since the late 20th century, F. × ananassa germplasm developed in California played a major role in global strawberry production, with extensive cultivation and parentage worldwide. We show that coastal breeding restructured California octoploids from other U.S., Canadian, and European F. × ananassa germplasm to produce a separate domesticated subpopulation. Formation of the commercially important CC‐F×a population, originally derived from TM‐F×a, was influenced by postdomestication introgression of diversity from nonancestral ecotypes of F. chiloensis (most likely the pacifica subspecies from California) and F. virginiana ssp. glauca. Coastal breeding reversed the predominant selection of F. virginiana allelic diversity in TM‐F×a, increasing the selection of F. chiloensis‐specific (beach strawberry) alleles. These F. chiloensis alleles selected in CC‐F×a were linked to gene functions influencing fruit development, suggesting they contributed to the elite marketable fruit quality and mass production phenotypes of UCD cultivars. Restructuring of CC‐F×a over time was also linked to selection of day‐neutral flowering, a key trait for extending the production season in the United States and abroad. The now‐predominant source of day‐neutrality descends from a high‐elevation F. virginiana ssp. glauca ecotype that is distinct from the eastern F. virginiana ssp. virginiana progenitor. Introduction of this source appears to have shifted the genetics of day‐neutrality to a single QTL on LG4A in modern CC‐F×a, which apparently took several decades.

This work supports the theory that commercially elite CC‐F×a octoploids are not the product of a single hybrid origin but instead a complex pathway initiated by merging wild genomes, followed by migration to a coastal environment, restructuring of genetic diversity, and selection of alleles from additional wild taxa. Similar findings were reported in tetraploid potato, where it was shown that migration of wild alleles into previously domesticated Andean populations introduced adaptive variation, including alleles for long‐day flowering, giving rise to a secondary coastal group (S. tuberosum group Tuberosum) that today accounts for the majority of worldwide production (Hardigan et al., 2017). The use of coastal adapted Fragaria ecotypes for California strawberry breeding produced a genetically distinct population of F. × ananassa that is better able to take advantage of coastal environments and an extended growing season. Molecular breeding in strawberry will benefit from understanding how the infusion of alleles from wild populations impacts selection in F. × ananassa. This will require breeders to unravel a patchwork of haplotypes descending from different wild species and determine how they interact in the hybrids. Octoploid genome assemblies are needed to trace F. × ananassa haplotype origins, allowing breeders to study how directional and balancing selection among wild subspecific lineage(s) impact gene expression and fruit traits in modern hybrids.

Supplemental Information

Supplemental File S1. Marker genotypes for octoploid strawberry samples screened on the Axiom IStraw35 array.

Supplemental File S2. Strawberry reproductive gene expression groups. (A) Description and data source for reproductive expression groups. (B) Summary of genes within each reproductive expression category. (C) Summary of reproductive expression categories associated with each gene.

Supplemental Table S1. Sample information for octoploid strawberry diversity panel.

Supplemental Table S2. Affymetrix marker positions in the FvH4.1 genome assembly.

Supplemental Table S3. Matrix of pairwise genetic distance estimates (Nei's) between octoploid strawberrygenotypes.

Supplemental Table S4. Association of putatively selected variant loci from two‐population selection tests with genes in the FvH4.1 annotation. Summarized number of variants in the first to fifth percentile of selected markers within 10 to 20 kb of each gene. Population tests include wild versus domesticated (wild vs. TM‐F×A, wild vs. pre‐1970 CC‐F×A, wild vs. UC cultivars, wild vs. post‐2000 CC‐F×A), domesticated subpopulations (TM‐F×A vs. pre‐1970 CC‐F×A, TM‐F×A vs. post‐2000 CC‐F×A), and day‐neutral flowering selection (short‐day F. × ananassa vs. pre‐1990 day‐neutral F. × ananassa, short‐day F. × ananassa vs. post‐2000 day‐neutral F. × ananassa).

Supplemental Table S5. Linkage disequilibrium and genotypes of significant markers in the chr4:Mb29–33 QTL region for day‐neutral flowering. (A) Linkage disequilibrium between significant markers in the chr4:Mb29–33 QTL. (B) Marker genotypes for post‐2000 day‐neutral and short‐day flowering strawberries in the chr4:Mb29‐33 QTL. (C) Phased Mb29 × Mb32–33 marker genotype frequencies for day‐neutral and short‐day flowering strawberries.

Supplemental Table S6. Information and selection signatures for strawberry candidate genes linked to flowering and maturity response pathways.

Supplemental Table S7. Information and selection signatures for strawberry candidate genes linked to fruit ripening, firmness, and quality traits.

Supplemental Table S8. Information and selection signatures for strawberry candidate genes linked to fruit volatile biosynthesis.

Supplemental Table S9. Information and selection signatures for strawberry candidate genes linked to hormone biosynthesis and signaling pathways in reproductive tissues and differentially regulated in response to fertilization (from Kang et al., 2013).

Supplemental Table S10. Significantly enriched Gene Ontology functions associated with putatively selected strawberry genes. (A) Ranked list of terms significantly enriched among gene candidates from each two‐population selection test. (B) Significance of GO term enrichment (–log10 p‐values) for genes identified in two‐population selection tests.

Supplemental Table S11. Significantly enriched Gene Ontology functions associated with gene candidates containing F. chiloensis‐specific alleles from CC‐F×A selection analysis.

Supplemental Table S12. Strawberry reproductive expression gene groups enriched in loci under putative selection when comparing wild and domesticated genotypes.

Supplemental Fig. S1. Alternate evaluation of population structuring in a subpanel of octoploids (n = 418) containing equal TM‐F×A and CC‐F×A sample sizes. (A) Neighbor‐joining tree based on a consensus of 1000 bootstrap datasets. (B) Principal component clustering of F. × ananassa samples projected onto variance components estimated from wild species. (C) Population substructure and admixture (K = 6, 7) in wild species and TM‐F×A or CC‐F×A genotypes sorted by time. Black bars delineate the decade of release.

Supplemental Fig. S2. . Marker diversity, FST, and inbreeding in wild and cultivated strawberry. (A) Distribution of marker diversity estimates in wild (F. chiloensis, F. virginiana, combined) and F. × ananassa groups. Overhead values indicate the mean marker diversity of a population. (B) Distribution of marker allele fixation (FST) between wild and domesticated octoploids in four cultivated populations. (C) Inbreeding coefficients for F. × ananassa plotted across time.

Supplemental Fig. S3. Frequency of predicted haplotypes for modern (post‐2000) day‐neutral and short‐day flowering genotypes based on significant GWAS markers in the Fvb4:Mb29‐33 QTL region.

Supplemental Fig. S4. Number of strawberry flowering or fruit development candidate genes associated with putatively selected variants based on two‐population selection tests. (A) Candidate genes for flowering and maturity response. (B) Candidate genes for ripening and fruit quality (firmness). (C) Candidate genes for fruit volatile biosynthesis. (D) Candidate hormone pathway genes with fertilization‐responsive expression in strawberry reproductive tissues.

Conflict of Interest Disclosure

The authors declare that there is no conflict of interest.

Supporting information

Supplemental Information

Supplemental File 1

TPG2-11-180049-s001.zip (48.1MB, zip)

Acknowledgments

This research is supported by grants to S.J.K. from the USDA National Institute of Food and Agriculture Specialty Crops Research Initiative (#2017‐51181‐26833), the California Strawberry Commission, and UCD.

2018‐11‐08. The Plant Genome 3 11 November 8, 2018

Contributor Information

Michael A. Hardigan, Email: mahardigan@ucdavis.edu.

Steven J. Knapp, Email: sjknapp@ucdavis.edu.

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