Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors

Abstract Background Fruit acidity and color are important quality attributes in peaches. Although there are some exceptions, blood-fleshed peaches typically have a sour taste. However, little is known about the genetic variations linking organic acid and color regulation in peaches. Results Here, we...

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Main Authors: Wenbo Chen, Qi Xie, Jia Fu, Shaojia Li, Yanna Shi, Jiao Lu, Yuanyuan Zhang, Yingjie Zhao, Ruijuan Ma, Baijun Li, Bo Zhang, Donald Grierson, Mingliang Yu, Zhangjun Fei, Kunsong Chen
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Genome Biology
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Online Access:https://doi.org/10.1186/s13059-024-03470-w
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author Wenbo Chen
Qi Xie
Jia Fu
Shaojia Li
Yanna Shi
Jiao Lu
Yuanyuan Zhang
Yingjie Zhao
Ruijuan Ma
Baijun Li
Bo Zhang
Donald Grierson
Mingliang Yu
Zhangjun Fei
Kunsong Chen
author_facet Wenbo Chen
Qi Xie
Jia Fu
Shaojia Li
Yanna Shi
Jiao Lu
Yuanyuan Zhang
Yingjie Zhao
Ruijuan Ma
Baijun Li
Bo Zhang
Donald Grierson
Mingliang Yu
Zhangjun Fei
Kunsong Chen
author_sort Wenbo Chen
collection DOAJ
description Abstract Background Fruit acidity and color are important quality attributes in peaches. Although there are some exceptions, blood-fleshed peaches typically have a sour taste. However, little is known about the genetic variations linking organic acid and color regulation in peaches. Results Here, we report a peach graph-based pangenome constructed from sixteen individual genome assemblies, capturing abundant structural variations and 82.3 Mb of sequences absent in the reference genome. Pangenome analysis reveals a long terminal repeat retrotransposon insertion in the promoter of the NAC transcription factor (TF) PpBL in blood-fleshed peaches, which enhances PpBL expression. Genome-wide association study identifies a significant association between PpBL and malate content. Silencing PpBL in peach fruit and ectopic overexpression of PpBL in tomatoes confirm that PpBL is a positive regulator of malate accumulation. Furthermore, we demonstrate that PpBL works synergistically with another NAC TF, PpNAC1, to activate the transcription of the aluminum-activated malate transporter PpALMT4, leading to increased malate content. Conclusions These findings, along with previous research showing that PpBL and PpNAC1 also regulate anthocyanin accumulation, explain the red coloration and sour taste in blood-fleshed peach fruits.
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issn 1474-760X
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publishDate 2025-01-01
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spelling doaj-art-9fd1c11cd7d047e5a36a7f4435491ee22025-01-12T12:26:00ZengBMCGenome Biology1474-760X2025-01-0126112010.1186/s13059-024-03470-wGraph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factorsWenbo Chen0Qi Xie1Jia Fu2Shaojia Li3Yanna Shi4Jiao Lu5Yuanyuan Zhang6Yingjie Zhao7Ruijuan Ma8Baijun Li9Bo Zhang10Donald Grierson11Mingliang Yu12Zhangjun Fei13Kunsong Chen14College of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityInstitute of Pomology, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Jiangsu Academy of Agricultural SciencesCollege of Agriculture & Biotechnology, Zhejiang UniversityInstitute of Pomology, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Jiangsu Academy of Agricultural SciencesCollege of Agriculture & Biotechnology, Zhejiang UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityThe State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang UniversityInstitute of Pomology, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Jiangsu Academy of Agricultural SciencesBoyce Thompson Institute, Cornell UniversityCollege of Agriculture & Biotechnology, Zhejiang UniversityAbstract Background Fruit acidity and color are important quality attributes in peaches. Although there are some exceptions, blood-fleshed peaches typically have a sour taste. However, little is known about the genetic variations linking organic acid and color regulation in peaches. Results Here, we report a peach graph-based pangenome constructed from sixteen individual genome assemblies, capturing abundant structural variations and 82.3 Mb of sequences absent in the reference genome. Pangenome analysis reveals a long terminal repeat retrotransposon insertion in the promoter of the NAC transcription factor (TF) PpBL in blood-fleshed peaches, which enhances PpBL expression. Genome-wide association study identifies a significant association between PpBL and malate content. Silencing PpBL in peach fruit and ectopic overexpression of PpBL in tomatoes confirm that PpBL is a positive regulator of malate accumulation. Furthermore, we demonstrate that PpBL works synergistically with another NAC TF, PpNAC1, to activate the transcription of the aluminum-activated malate transporter PpALMT4, leading to increased malate content. Conclusions These findings, along with previous research showing that PpBL and PpNAC1 also regulate anthocyanin accumulation, explain the red coloration and sour taste in blood-fleshed peach fruits.https://doi.org/10.1186/s13059-024-03470-wGraph pangenomePeachMalate contentBlood-fleshedNAC
spellingShingle Wenbo Chen
Qi Xie
Jia Fu
Shaojia Li
Yanna Shi
Jiao Lu
Yuanyuan Zhang
Yingjie Zhao
Ruijuan Ma
Baijun Li
Bo Zhang
Donald Grierson
Mingliang Yu
Zhangjun Fei
Kunsong Chen
Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
Genome Biology
Graph pangenome
Peach
Malate content
Blood-fleshed
NAC
title Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
title_full Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
title_fullStr Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
title_full_unstemmed Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
title_short Graph pangenome reveals the regulation of malate content in blood-fleshed peach by NAC transcription factors
title_sort graph pangenome reveals the regulation of malate content in blood fleshed peach by nac transcription factors
topic Graph pangenome
Peach
Malate content
Blood-fleshed
NAC
url https://doi.org/10.1186/s13059-024-03470-w
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