Major-effect candidate genes identified in cultivated strawberry (Fragaria × ananassa Duch.) for ellagic acid deoxyhexoside and pelargonidin-3-O-malonylglucoside biosynthesis, key polyphenolic compounds

Abstract

Strawberries are rich in polyphenols which impart health benefits when metabolized by the gut microbiome, including anti-inflammatory, neuroprotective, and antiproliferative effects. In addition, polyphenolic anthocyanins contribute to the attractive color of strawberry fruits. However, the genetic basis of polyphenol biosynthesis has not been extensively studied in strawberry. In this investigation, ripe fruits from three cultivated strawberry populations were characterized for polyphenol content using HPLC-DAD-MS n and genotyped using the iStraw35k array. GWAS and QTL analyses identified genetic loci controlling polyphenol biosynthesis. QTL were identified on four chromosomes for pelargonidin-3-O-malonylglucoside, pelargonidin-3-O-acetylglucoside, cinnamoyl glucose, and ellagic acid deoxyhexoside biosynthesis. Presence/absence of ellagic acid deoxyhexoside and pelargonidin-3-O-malonylglucoside was found to be under the control of major gene loci on LG1X2 and LG6b, respectively, on the F. × ananassa linkage maps. Interrogation of gene predictions in the F. vesca reference genome sequence identified a single candidate gene for ellagic acid deoxyhexoside biosynthesis, while seven malonyltransferase genes were identified as candidates for pelargonidin-3-O-malonylglucoside biosynthesis. Homologous malonyltransferase genes were identified in the F. × ananassa 'Camarosa' genome sequence but the candidate for ellagic acid deoxyhexoside biosynthesis was absent from the 'Camarosa' sequence. This study demonstrated that polyphenol biosynthesis in strawberry is, in some cases, under simple genetic control, supporting previous observations of the presence or absence of these compounds in strawberry fruits. It has also shed light on the mechanisms controlling polyphenol biosynthesis and enhanced the knowledge of these biosynthesis pathways in strawberry. The above findings will facilitate breeding for strawberries enriched in compounds with beneficial health effects.

Chemical Compounds of Berry-Derived Polyphenols and Their Effects on Gut Microbiota, Inflammation, and Cancer

“…This explains the capacity to accumulate high polyphenol levels in certain types of vines. The findings of this study corroborated those obtained by Davik et al [ 81 ], who identified the candidate genes controlling the biosynthesis of polyphenolic compounds in strawberries ( Fragaria × ananassa Duch.).…”

Azacytidine arrests ripening in cultivated strawberry (Fragaria × ananassa) by repressing key genes and altering hormone contents

“…Structural genes involved in the anthocyanin pathway such as FaPAL (phenylammonia lyase, FvH4_6g16060 ), Fa4CL (4-coumaryl-CoA ligase, FvH4_6g16460 ), FaDFR (dihydroflavonol reductase, FvH4_2g39530 ), FaF3H (flavone 3-hydroxylase, FvH4_1g11810 ) and FaANS (anthocyanin synthase, FvH4_5g01170 ) [ 36 ] were all downregulated in AZA treated tissues. FaGT1 , which encodes the essential anthocyanidin glucosyltransferase ( FvH4_7g33480 ) [ 37 ] and FaMT1 ( FvH4_6g46740 ) [ 38 ] –involved in the biosynthesis of pelargonidin-3-glucoside and its malonyl derivative– were expressed at low levels. By contrast, FaANR ( FvH4_3g02980 ), which encodes an anthocyanin reductase, was expressed at high levels (Additional file 4 ).…”

High Resolution Quantitative Trait Locus Mapping and Whole Genome Sequencing Enable the Design of an Anthocyanidin Reductase-Specific Homoeo-Allelic Marker for Fruit Colour Improvement in Octoploid Strawberry (Fragaria × ananassa)

“…The red fruit colour is due to the accumulation of the anthocyanin pigments, which are water-soluble flavonoids. The flavonoids detected in strawberry fruit (anthocyanins, flavonols, and flavan-3-ols) (Ring et al, 2013;Urrutia et al, 2016;Davik et al, 2020;Labadie et al, 2020;Pott et al, 2020) are derived from the phenylpropanoid pathway (Figure 1A). Flavonols and flavan-3-ols are mainly glycosides of quercetin and kaempferol as well as derivatives of catechin and epicatechin.…”

“…In a recent study of a pseudo F1 progeny of F. × ananassa using SSR markers (Labadie et al, 2020), we mapped flavonoid metabolic quantitative trait loci (mQTLs) and other colourand antioxidant-related QTLs assessed through colourimetric assays and LC-ESI-MS analysis (Ring et al, 2013;Haugeneder et al, 2018). Additional flavonoid mQTLs were identified by linkage mapping and association studies of other bi-parental populations of F. × ananassa (Davik et al, 2020;Pott et al, 2020). Interestingly, most mQTLs mapped to different genomic regions depending on the population studied, indicating that a large genetic diversity is available in strawberry to improve fruit colour, which is a complex trait.…”

“…Recent findings suggest that each subgenome is mainly derived from one of four ancestral diploid species Fragaria vesca, Fragaria iinumae, Fragaria nipponica, and Fragaria viridis with intrachromosomal patterns of mixed ancestral DNA variation (Edger et al, 2019;Hardigan et al, 2021a). The current resolution offered by the high-density strawberry SNP genotyping arrays (Bassil et al, 2015;Hardigan et al, 2020) now makes it possible to narrow a mQTL down to a small chromosomal region specific to a given subgenome (Hardigan et al, 2020(Hardigan et al, , 2021a, as done for the identification of several malonyltransferase candidate genes underlying pelargonidin-3-O-malonylglucoside QTLs (Davik et al, 2020). Thanks to the availability of high quality genome sequences of the diploid woodland strawberry F. vesca (Shulaev et al, 2011;Edger et al, 2018) and octoploid F. × ananassa (Edger et al, 2019;Liston et al, 2020;Hardigan et al, 2021a) and progress in sequencing, it is now possible to obtain whole genome sequences (WGS) of the parents of the population studied, compare them to reference genomes, identify polymorphism in candidate genes and design specific markers for MAS.…”