Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)

During natural evolution and artificial selection, the fruit color of many species has been repeatedly gained or lost and is generally associated with mutations in genes encoding R2R3-MYB transcription factors, especially MYB10. In this study, we show that a heterozygous frameshift mutation (FaMYB10...

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Main Authors: Huazhao Yuan, Weijian Cai, Xiaodong Chen, Fuhua Pang, Jing Wang, Mizhen Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1027567/full
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author Huazhao Yuan
Weijian Cai
Xiaodong Chen
Fuhua Pang
Jing Wang
Mizhen Zhao
author_facet Huazhao Yuan
Weijian Cai
Xiaodong Chen
Fuhua Pang
Jing Wang
Mizhen Zhao
author_sort Huazhao Yuan
collection DOAJ
description During natural evolution and artificial selection, the fruit color of many species has been repeatedly gained or lost and is generally associated with mutations in genes encoding R2R3-MYB transcription factors, especially MYB10. In this study, we show that a heterozygous frameshift mutation (FaMYB10AG-insert/FaMYB10wild) is responsible for the loss of anthocyanins in the flesh of cultivated strawberry. Comparative transcriptomic and metabolomic analyses of red- and white-fleshed strawberry indicated that the low expression level of FaUFGT (flavonol-O-glucosyltransferases) was responsible for the loss of anthocyanins and accumulation of proanthocyanidin in the white-fleshed strawberry and was the crucial gene that encodes enzymes of the anthocyanin biosynthesis pathway. Accordingly, overexpression and silencing of FaUFGT altered anthocyanin content and changed the flesh color of strawberry fruits. Furthermore, whole-genome resequencing analyses identified an AG insertion in the FaMYB10 coding region (FaMYB10AG-insert) of white-fleshed strawberry. Y1H and EMSA assays showed that FaMYB10wild was able to bind to the promoter of the FaUFGT gene, while the FaMYB10AG-insert could not. The skin and flesh color were tightly linked to the number of fully functional FaMYB10 copies in the selfing progeny of white-fleshed strawberry. Our results suggested that heterozygous frameshift mutation of FaMYB10 resulted in the loss of the ability to activate the expression of the FaUFGT gene, was responsible for the natural formation of red and white-fleshed strawberry.
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spelling doaj.art-4fd7173ddb1644dd92885f04dce86f9a2022-12-22T02:35:44ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-10-011310.3389/fpls.2022.10275671027567Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)Huazhao YuanWeijian CaiXiaodong ChenFuhua PangJing WangMizhen ZhaoDuring natural evolution and artificial selection, the fruit color of many species has been repeatedly gained or lost and is generally associated with mutations in genes encoding R2R3-MYB transcription factors, especially MYB10. In this study, we show that a heterozygous frameshift mutation (FaMYB10AG-insert/FaMYB10wild) is responsible for the loss of anthocyanins in the flesh of cultivated strawberry. Comparative transcriptomic and metabolomic analyses of red- and white-fleshed strawberry indicated that the low expression level of FaUFGT (flavonol-O-glucosyltransferases) was responsible for the loss of anthocyanins and accumulation of proanthocyanidin in the white-fleshed strawberry and was the crucial gene that encodes enzymes of the anthocyanin biosynthesis pathway. Accordingly, overexpression and silencing of FaUFGT altered anthocyanin content and changed the flesh color of strawberry fruits. Furthermore, whole-genome resequencing analyses identified an AG insertion in the FaMYB10 coding region (FaMYB10AG-insert) of white-fleshed strawberry. Y1H and EMSA assays showed that FaMYB10wild was able to bind to the promoter of the FaUFGT gene, while the FaMYB10AG-insert could not. The skin and flesh color were tightly linked to the number of fully functional FaMYB10 copies in the selfing progeny of white-fleshed strawberry. Our results suggested that heterozygous frameshift mutation of FaMYB10 resulted in the loss of the ability to activate the expression of the FaUFGT gene, was responsible for the natural formation of red and white-fleshed strawberry.https://www.frontiersin.org/articles/10.3389/fpls.2022.1027567/fullFragaria x ananassaflesh coloranthocyaninFaMYB10AG-insertheterozygous
spellingShingle Huazhao Yuan
Weijian Cai
Xiaodong Chen
Fuhua Pang
Jing Wang
Mizhen Zhao
Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
Frontiers in Plant Science
Fragaria x ananassa
flesh color
anthocyanin
FaMYB10AG-insert
heterozygous
title Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
title_full Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
title_fullStr Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
title_full_unstemmed Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
title_short Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria x ananassa Duch)
title_sort heterozygous frameshift mutation in famyb10 is responsible for the natural formation of red and white fleshed strawberry fragaria x ananassa duch
topic Fragaria x ananassa
flesh color
anthocyanin
FaMYB10AG-insert
heterozygous
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1027567/full
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