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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) 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]

Macrophomina phaseolina, the causal agent of charcoal rot, is one of the most destructive soil-borne pathogens that affect the global strawberry industry. Resistant cultivars are critical for ensuring the profitability of strawberry production without the protection historically provided by methyl bromide. Previously, three loci, namely, FaRMp1, FaRMp2, and FaRMp3, associated with quantitative resistance to Macrophomina phaseolina have been identified and validated across diverse populations and environments. Among those, the locus with the largest effect, FaRMp3, was initially detected in crosses with an exotic Fragaria xananassa selection. We introgressed the favorable FaRMp3 allele into elite germplasm in the University of Florida strawberry breeding program already segregating for FaRMp1 and FaRMp2 and confirmed its phenotypic effects across various genetic backgrounds. Subsequently, we developed a high-throughput genotyping assay to facilitate the transfer and selection of FaRMp3 in breeding populations via marker-assisted selection. Given that three quantitative trait loci (QTL) contribute to partial resistance to Macrophomina phaseolina, stacking them within a single genotype presents a potential strategy for enhancing resistance. We screened 564 individuals that segregate for favorable alleles at all three QTL to assess their effects singly and in combination across multiple genetic backgrounds and production seasons. Inoculated field trials revealed that the three QTL cumulatively enhanced resistance levels, and that two-way QTL combinations including FaRMp3 provide increased protection against the pathogen. Pyramiding all three loci achieved the strongest resistance and could provide substantial economic value to the strawberry industry. [ABSTRACT FROM AUTHOR]