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Article|10 Feb 2023|OPEN
A 21-bp InDel in the promoter of STP1 selected during tomato improvement accounts for soluble solid content in fruits 
Ying Wang1 , Chunmei Shi1 , Pingfei Ge1 , Fangman Li1 , Lihui Zhu1 , Yaru Wang1 , Jinbao Tao1 , Xingyu Zhang1 , Haiqiang Dong1 , Wenxian Gai1 , Fei Wang1 , Zhibiao Ye1 , Donald Grierson2 , Wei Xu3 , and Yuyang Zhang,1,4 ,
1National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan 430070, China
2Plant Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK
3Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization (Xinjiang Production and Construction Crops), College of Agriculture, Shihezi University, Shihezi 832003, Xinjiang, China
4Hubei Hongshan Laboratory, Wuhan 430070, China
*Corresponding author. E-mail: xuwei0412@shzu.edu.cn,yyzhang@mail.hzau.edu.cn

Horticulture Research 10,
Article number: uhad009 (2023)
doi: https://doi.org/10.1093/hr/uhad009
Views: 447

Received: 08 Oct 2022
Accepted: 18 Jan 2023
Published online: 10 Feb 2023

Abstract

Domestication and improvement are important processes that generate the variation in genome and phonotypes underlying crop improvement. Unfortunately, during selection for certain attributes, other valuable traits may be inadvertently discarded. One example is the decline in fruit soluble solids content (SSC) during tomato breeding. Several genetic loci for SSC have been identified, but few reports on the underlying mechanisms are available. In this study we performed a genome-wide association study (GWAS) for SSC of the red-ripe fruits in a population consisting of 481 tomato accessions with large natural variations and found a new quantitative trait locus, STP1, encoding a sugar transporter protein. The causal variation of STP1, a 21-bp InDel located in the promoter region 1124 bp upstream of the start codon, alters its expression. STP1Insertion accessions with an 21-bp insertion have higher SSC than STP1Deletion accessions with the 21-bp deletion. Knockout of STP1 in TS-23 with high SSC using CRISPR/Cas9 greatly decreased SSC in fruits. In vivo and in vitro assays demonstrated that ZAT10-LIKE, a zinc finger protein transcription factor (ZFP TF), can specifically bind to the promoter of STP1Insertion to enhance STP1 expression, but not to the promoter of STP1Deletion, leading to lower fruit SSC in modern tomatoes. Diversity analysis revealed that STP1 was selected during tomato improvement. Taking these results together, we identified a naturally occurring causal variation underlying SSC in tomato, and a new role for ZFP TFs in regulating sugar transporters. The findings enrich our understanding of tomato evolution and domestication, and provide a genetic basis for genome design for improving fruit taste.