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Article|18 Apr 2020|OPEN
A key ‘foxy’ aroma gene is regulated by homology-induced promoter indels in the iconic juice grape ‘Concord’
Yingzhen Yang1, Jose Cuenca1,2, Nian Wang1,3, Zhenchang Liang4, Honghe Sun5, Benjamin Gutierrez6, Xiaojun Xi6,7, Jie Arro6, Yi Wang4,8, Peige Fan4, Jason Londo1, Peter Cousins9, Shaohua Li4, Zhangjun Fei5,10 & Gan-Yuan Zhong1,
1US Department of Agriculture-Agricultural Research Service, Grape Genetics Research Unit, Geneva, NY, USA
2Present address: Centro de Citricultura y Producción Vegetal. Instituto Valenciano de Investigaciones Agrarias, Moncada, Valencia, Spain
3Present address: College of Horticulture and Forestry, Huazhong Agricultural University, Wuhan, Hubei, China
4Beijing Key Laboratory of Grape Sciences and Enology, Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, China
5Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY, USA
6US Department of Agriculture-Agricultural Research Service, Plant Genetic Resources Unit, Geneva, NY, USA
7Forestry and Pomology Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai, China
8University of Chinese Academy of Sciences, Beijing, China
9E. & J. Gallo Winery, Modesto, CA, USA
10US Department of Agriculture–Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, NY, USA

Horticulture Research 7,
Article number: 20067 (2020)
doi: 10.1038/hortres.2020.67
Views: 555

Received: 27 Jan 2020
Revised: 19 Mar 2020
Accepted: 30 Mar 2020
Published online: 18 Apr 2020

Abstract

‘Concord’, the most well-known juice grape with a parentage of the North American grape species Vitis labrusca L., 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 species V. 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 in AMAT promoters highly associated with high levels of AMAT expression and MA accumulation in ‘Concord’ and other V. labrusca-derived grapes. These promoter variants, all with direct and inverted repeats, were further confirmed in more than 1,300 Vitis germplasm. Moreover, functional impact of these indels was validated in transgenic Arabidopsis. Superimposed on the promoter regulation, large structural changes including exonic insertion of a retrotransposon were present at the AMAT locus in some V. vinifera grapes. Elucidation of the AMAT genetic regulation advances our understanding of the ‘foxy’ aroma trait and makes it genetically trackable and amenable in grapevine breeding.