A multi‐omics framework reveals strawberry flavor genes and their regulatory elements

Abstract

Summary 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.

Strawberry breeding for improved flavor

“…Importantly, QTL mapping led to the characterization of FaOMT, an essential gene for the production of mesifurane (Zorrilla-Fontanesi et al, 2012). Results of GWAS studies from Florida breeding lines revealed the same QTL locations for many volatiles (Barbey et al, 2021;Fan et al, 2022). These association mapping studies uncovered genetic control of mesifurane but not furaneol.…”

“…Mesifurane abundance is dependent on an o‐methyl transferase gene ( FaOMT ) that has been functionally validated and mapped to chromosome 7D (Barbey et al., 2021; Zorrilla‑Fontanesi et al., 2012). Nonfunctional alleles are characterized by a 28 bp indel in the first exon that causes premature termination of transcription (Fan et al., 2022). There is also evidence that the locus discovered for furaneol on chromosome 1C also modulates mesifurane content (Barbey et al., 2021).…”

“…Recently, Fan et al built an eQTL map using 200 elite breeding lines from the two largest public breeding programs in the United States, identifying eQTL for half of fruit expressed genes. Integration with GWAS results allowed identification of anthranilate synthase alpha subunit (FaASa1) as another gene influencing MA abundance (Fan et al, 2022). As a tool for investigating genes that affect flavor compounds, eQTLs for markers that are associated with phenotypes provide robust expression evidence for uncovering candidate genes.…”

“…Sucrose, glucose, and fructose comprise 99% of sugars while citric and malic acid are the main acids (Montero et al., 1996). Narrow sense SNP‐based heritabilities from a genome‐wide association study (GWAS) population with many segregating volatiles averaged 0.660, indicating strong genetic control of most aromatic compounds in strawberry (Fan et al., 2022). Despite this fact, relatively few genes have been confirmed to underlie the natural variation observed for important volatile compounds in breeding programs.…”

Advances in genomics for diversity studies and trait improvement in temperate fruit and nut crops under changing climatic scenarios

“…A transcriptome analysis of Chinese pear showed high variation of gene expressions during the developmental phase of tissues and fruits ( Xie et al., 2013 ). In strawberry, a multiomics approach revealed the association of different genes regulating volatile organic compounds behind the flavor characteristics of its berries ( Fan et al., 2022 ). A comparative transcriptome analysis among several apple verities exhibited 34 genes regulating the anthocyanin contents which are associated with preferred appearance of apples ( El-Sharkawy et al., 2015 ).…”