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Flavor is essential to consumer preference of foods and is an increasing focus of plant breeding programs. In fruit crops, identifying genes underlying volatile organic compounds has great promise to accelerate flavor improvement, but polyploidy and heterozygosity in many species have slowed progress. Here we use octoploid cultivated strawberry to demonstrate how genomic heterozygosity, transcriptomic intricacy and fruit metabolomic diversity can be treated as strengths and leveraged to uncover fruit flavor genes and their regulatory elements. Multi-omics datasets were generated including an expression quantitative trait loci map with 196 diverse breeding lines, haplotype-phased genomes of a highly-flavored breeding selection, a genome-wide structural variant map using five haplotypes, and volatile genome-wide association study (GWAS) with > 300 individuals. Overlaying regulatory elements, structural variants and GWAS-linked allele-specific expression of numerous genes to variation in volatile compounds important to flavor. In one example, the functional role of anthranilate synthase alpha subunit 1 in methyl anthranilate biosynthesis was supported via fruit transient gene expression assays. These results demonstrate a framework for flavor gene discovery in fruit crops and a pathway to molecular breeding of cultivars with complex and desirable flavor.

Cultivated strawberry (Fragaria × ananassa) is one of our youngest domesticates, originating in early eighteenth-century Europe from spontaneous hybrids between wild allo-octoploid species (Fragaria chiloensis and Fragaria virginiana). The improvement of horticultural traits by 300 years of breeding has enabled the global expansion of strawberry production. Here, we describe the genomic history of strawberry domestication from the earliest hybrids to modern cultivars. We observed a significant increase in heterozygosity among interspecific hybrids and a decrease in heterozygosity among domesticated descendants of those hybrids. Selective sweeps were found across the genome in early and modern phases of domestication-59-76% of the selectively swept genes originated in the three less dominant ancestral subgenomes. Contrary to the tenet that genetic diversity is limited in cultivated strawberry, we found that the octoploid species harbor massive allelic diversity and that F. × ananassa harbors as much allelic diversity as either wild founder. We identified 41.8 M subgenome-specific DNA variants among resequenced wild and domesticated individuals. Strikingly, 98% of common alleles and 73% of total alleles were shared between wild and domesticated populations. Moreover, genome-wide estimates of nucleotide diversity were virtually identical in F. chiloensis,F. virginiana, and F. × ananassa (π = 0.0059-0.0060). We found, however, that nucleotide diversity and heterozygosity were significantly lower in modern F. × ananassa populations that have experienced significant genetic gains and have produced numerous agriculturally important cultivars.

Charcoal rot caused by Macrophomina phaseolinais an increasing economic problem in annualized strawberry production systems around the world. Currently there are no effective postfumigation chemical controls for managing charcoal rot, and no information is available on the genetic architecture of resistance to M. phaseolina in strawberry (Fragaria ×ananassa). In this study, three multiparental discovery populations and two validation populations were inoculated at planting and evaluated for mortality in three consecutive growing seasons. Genome-wide SNP genotyping and pedigree-based analysis with FlexQTL™ software were performed. Two large-effect quantitative trait loci (QTL) increasing charcoal rot resistance were discovered and validated in cultivated germplasm. FaRMp1 was located on linkage group 2A in the interval 20.4to 24.9 cM, while FaRMp2 was located on linkage group 4B in the interval 41.1to 61.2 cM. Together these QTLs explained 27% and 17% of the phenotypic variance in two discovery populations consisting of elite breeding germplasm. For both QTLs, the resistant allele showed some evidence of partial dominance, but no significant interaction was detected between the two loci. As the dosage of resistant alleles increased from 0 to 4 across the two QTLs, mortality decreased regardless of the combination of alleles.A third locus, FaRMp3 on 4D, was discovered in FVC 11-58, a reconstituted F.×ananassa originating from diverse F. virginiana and F. chiloensis accessions. This locus accounted for 44% of phenotypic variation in four segregating crosses. These findings will form the basis for DNA-informed breeding for resistance to charcoal rot in cultivated strawberry.

The cultivated strawberry (Fragaria × ananassa) is an allo-octoploid species, originating nearly 300 years ago from wild progenitors from the Americas. Since that time the strawberry has become the most widely cultivated fruit crop in the world, universally appealing due to its sensory qualities and health benefits. The recent publication of the first high-quality chromosome-scale octoploid strawberry genome (cv. Camarosa) is enabling rapid advances in genetics, stimulating scientific debate and provoking new research questions. In this forward-looking review we propose avenues of research toward new biological insights and applications to agriculture. Among these are the origins of the genome, characterization of genetic variants, and big data approaches to breeding. Key areas of research in molecular biology will include the control of flowering, fruit development, fruit quality, and plant-pathogen interactions. In order to realize this potential as a global community, investments in genome resources must be continually augmented.

Octoploid strawberry (Fragaria ×ananassa) is a valuable specialty crop, but profitable production and availability are threatened by many pathogens. Efforts to identify and introgress useful disease resistance genes (R-genes) in breeding programs are complicated by strawberry's complex octoploid genome. Recently-developed resources in strawberry, including a complete octoploid reference genome and high-resolution octoploid genotyping, enable new analyses in strawberry disease resistance genetics. This study characterizes the complete R-gene collection in the genomes of commercial octoploid strawberry and two diploid ancestral relatives, and introduces several new technological and data resources for strawberry disease resistance research. These include octoploid R-gene transcription profiling, dN/dS analysis, expression quantitative trait loci (eQTL) analysis and RenSeq analysis in cultivars. Octoploid fruit eQTL were identified for 76 putative R-genes. R-genes from the ancestral diploids Fragaria vesca and Fragaria iinumae were compared, revealing differential inheritance and retention of various octoploid R-gene subtypes. The mode and magnitude of natural selection of individual F. ×ananassa R-genes was also determined via dN/dS analysis. R-gene sequencing using enriched libraries (RenSeq) has been used recently for R-gene discovery in many crops, however this technique somewhat relies upon a priori knowledge of desired sequences. An octoploid strawberry capture-probe panel, derived from the results of this study, is validated in a RenSeq experiment and is presented for community use. These results give unprecedented insight into crop disease resistance genetics, and represent an advance toward exploiting variation for strawberry cultivar improvement.

Cultivated strawberry (Fragaria × ananassa) has a brief history of less than 300 yr, beginning with the hybridization of octoploids Fragaria chiloensis and Fragaria virginiana. Here we explored the genomic signatures of early domestication and subsequent diversification for different climates using whole-genome sequences of 289 wild, heirloom, and modern varieties from two major breeding programs in the United States. Four nonadmixed wild octoploid populations were identified, with recurrent introgression among the sympatric populations. The proportion of F. virginiana ancestry increased by 20% in modern varieties over initial hybrids, and the proportion of F. chiloensis subsp. pacifica rose from 0% to 3.4%. Effective population size rapidly declined during early breeding. Meanwhile, divergent selection for distinct environments reshaped wild allelic origins in 21 out of 28 chromosomes. Overlapping divergent selective sweeps in natural and domesticated populations revealed 16 convergent genomic signatures that may be important for climatic adaptation. Despite 20 breeding cycles since initial hybridization, more than half of loci underlying yield and fruit size are still not under artificial selection. These insights add clarity to the domestication and breeding history of what is now the most widely cultivated fruit in the world. Whole-genome sequences of 289 octoploid strawberry samples were used to explore the genomic signatures of domestication and subsequent diversification in different climates. [ABSTRACT FROM AUTHOR]

Strawberry (Fragaria ×ananassa Duchesne ex Rozier) is cultivated and enjoyed globally for its health properties and flavor. Improvements in agronomic performance and fruit quality attributes highlight the successes of strawberry breeding in recent decades. Nevertheless, sweetness and flavor continue to fall below the ideal for the average consumer. While flavor is an important trait of focus, it is one of many critical traits necessary for the success of a strawberry variety. In addition, the chemical complexity of flavor and the genetic complexity of octoploid strawberry have slowed the development of genomics tools for flavor improvement. Recent efforts to understand consumer preference and the chemical drivers of strawberry flavor have revealed the strong impact of sugar content and specific volatile compounds. These large‐scale sensory studies combined with multi‐omics resources have set the stage for new levels of flavor improvement. Marker‐assisted selection for volatile biosynthesis genes has begun to take place in breeding programs, along with genomic selection for increased sugar content. Enhancing levels of existing volatile compounds and targeted introgression of rare compounds using genomics tools will continue to improve flavor intensity and complexity. Core Ideas: Complex fruit chemistry and balancing many traits are challenges for improving strawberry flavor.Sensory‐chemical studies have identified volatile compounds that affect flavor and sweetness.An explosion of multi‐omics resources in strawberry is advancing the discovery of genes underlying volatiles.Marker‐assisted selection for volatiles and genomic selection for sugars forms an overall breeding strategy. [ABSTRACT FROM AUTHOR]