A key ‘foxy’ aroma gene is regulated by homology-induced promoter indels in the iconic juice grape ‘Concord’

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Abstract ‘Concord’, the most well-known juice grape with a parentage of the North American grape speciesVitis labruscaL., possesses a special ‘foxy’ aroma predominantly resulted from the accumulation of methyl anthranilate (MA) in berries. This aroma, however, is often perceived as an undesirable attribute by wine consumers and rarely noticeable in the common table and wine grape speciesV. vinifera. Here we discovered homology-induced promoter indels as a major genetic mechanism for species-specific regulation of a key ‘foxy’ aroma gene, anthraniloyl-CoA:methanol acyltransferase (AMAT), that is responsible for MA biosynthesis. We found the absence of a 426-bp and/or a 42-bp sequence inAMATpromoters highly associated with high levels ofAMATexpression and MA accumulation in ‘Concord’ and otherV. labrusca-derived grapes. These promoter variants, all with direct and inverted repeats, were further confirmed in more than 1,300Vitisgermplasm. Moreover, functional impact of these indels was validated in transgenicArabidopsis. Superimposed on the promoter regulation, large structural changes including exonic insertion of a retrotransposon were present at theAMATlocus in someV. viniferagrapes. Elucidation of theAMATgenetic regulation advances our understanding of the ‘foxy’ aroma trait and makes it genetically trackable and amenable in grapevine breeding.