Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit

Several physiological changes occur during fruit storage, which include the regulation of genes, metabolisms and transcription factors. In this study, we compared ‘JF308’ (a normal tomato cultivar) and ‘YS006’ (a storable tomato cultivar) to determine the difference in accumulated metabolites, gene...

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Main Authors: Susu Guo, Yanhai Ji, Yanyan Zheng, Christopher B. Watkins, Lili Ma, Qing Wang, Hao Liang, Chunmei Bai, Anzhen Fu, Ling Li, Demei Meng, Mingchi Liu, Jinhua Zuo
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1142913/full
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author Susu Guo
Susu Guo
Susu Guo
Susu Guo
Susu Guo
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Christopher B. Watkins
Lili Ma
Qing Wang
Qing Wang
Qing Wang
Qing Wang
Hao Liang
Hao Liang
Hao Liang
Hao Liang
Chunmei Bai
Chunmei Bai
Chunmei Bai
Chunmei Bai
Anzhen Fu
Anzhen Fu
Anzhen Fu
Anzhen Fu
Ling Li
Demei Meng
Mingchi Liu
Mingchi Liu
Mingchi Liu
Mingchi Liu
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
author_facet Susu Guo
Susu Guo
Susu Guo
Susu Guo
Susu Guo
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Christopher B. Watkins
Lili Ma
Qing Wang
Qing Wang
Qing Wang
Qing Wang
Hao Liang
Hao Liang
Hao Liang
Hao Liang
Chunmei Bai
Chunmei Bai
Chunmei Bai
Chunmei Bai
Anzhen Fu
Anzhen Fu
Anzhen Fu
Anzhen Fu
Ling Li
Demei Meng
Mingchi Liu
Mingchi Liu
Mingchi Liu
Mingchi Liu
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
author_sort Susu Guo
collection DOAJ
description Several physiological changes occur during fruit storage, which include the regulation of genes, metabolisms and transcription factors. In this study, we compared ‘JF308’ (a normal tomato cultivar) and ‘YS006’ (a storable tomato cultivar) to determine the difference in accumulated metabolites, gene expression, and accessible chromatin regions through metabolome, transcriptome, and ATAC-seq analysis. A total of 1006 metabolites were identified in two cultivars. During storage time, sugars, alcohols and flavonoids were found to be more abundant in ‘YS006’ compared to ‘JF308’ on day 7, 14, and 21, respectively. Differentially expressed genes, which involved in starch and sucrose biosynthesis were observed higher in ‘YS006’. ‘YS006’ had lower expression levels of CesA (cellulose synthase), PL (pectate lyase), EXPA (expansin) and XTH (xyglucan endoglutransglucosylase/hydrolase) than ‘JF308’. The results showed that phenylpropanoid pathway, carbohydrate metabolism and cell wall metabolism play important roles in prolonging the shelf life of tomato (Solanum lycopersicum) fruit. The ATAC-seq analysis revealed that the most significantly up-regulated transcription factors during storage were TCP 2,3,4,5, and 24 in ‘YS006’ compared to ‘JF308’ on day 21. This information on the molecular regulatory mechanisms and metabolic pathways of post-harvest quality changes in tomato fruit provides a theoretical foundation for slowing post-harvest decay and loss, and has theoretical importance and application value in breeding for longer shelf life cultivars.
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spelling doaj.art-aa343f431c614f93bc02bfa03628cf232023-03-08T15:11:26ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-03-011410.3389/fpls.2023.11429131142913Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruitSusu Guo0Susu Guo1Susu Guo2Susu Guo3Susu Guo4Yanhai Ji5Yanhai Ji6Yanhai Ji7Yanhai Ji8Yanyan Zheng9Yanyan Zheng10Yanyan Zheng11Yanyan Zheng12Christopher B. Watkins13Lili Ma14Qing Wang15Qing Wang16Qing Wang17Qing Wang18Hao Liang19Hao Liang20Hao Liang21Hao Liang22Chunmei Bai23Chunmei Bai24Chunmei Bai25Chunmei Bai26Anzhen Fu27Anzhen Fu28Anzhen Fu29Anzhen Fu30Ling Li31Demei Meng32Mingchi Liu33Mingchi Liu34Mingchi Liu35Mingchi Liu36Jinhua Zuo37Jinhua Zuo38Jinhua Zuo39Jinhua Zuo40State Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaSchool of Integrative Plant Science, Horticulture Section, College of Agriculture and Life Science, Cornell University, NY, Ithaca, United StatesCollege of Food Science and Biotechnology, Tianjin Agricultural University, Tianjin, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaCollege of Food Science and Biotechnology, Tianjin Agricultural University, Tianjin, ChinaState Key Laboratory of Food Nutrition and Safety, College of Food Science and Engineering, Tianjin University of Science & Technology, Tianjin, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Vegetable Postharvest Processing, Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaBeijing Key Laboratory of Fruits and Vegetable Storage and Processing, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China) of Ministry of Agriculture, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaKey Laboratory of Urban Agriculture (North) of Ministry of Agriculture, Beijing Vegetable Research Center, Institute of Agri-Products Processing and Food Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing, ChinaSeveral physiological changes occur during fruit storage, which include the regulation of genes, metabolisms and transcription factors. In this study, we compared ‘JF308’ (a normal tomato cultivar) and ‘YS006’ (a storable tomato cultivar) to determine the difference in accumulated metabolites, gene expression, and accessible chromatin regions through metabolome, transcriptome, and ATAC-seq analysis. A total of 1006 metabolites were identified in two cultivars. During storage time, sugars, alcohols and flavonoids were found to be more abundant in ‘YS006’ compared to ‘JF308’ on day 7, 14, and 21, respectively. Differentially expressed genes, which involved in starch and sucrose biosynthesis were observed higher in ‘YS006’. ‘YS006’ had lower expression levels of CesA (cellulose synthase), PL (pectate lyase), EXPA (expansin) and XTH (xyglucan endoglutransglucosylase/hydrolase) than ‘JF308’. The results showed that phenylpropanoid pathway, carbohydrate metabolism and cell wall metabolism play important roles in prolonging the shelf life of tomato (Solanum lycopersicum) fruit. The ATAC-seq analysis revealed that the most significantly up-regulated transcription factors during storage were TCP 2,3,4,5, and 24 in ‘YS006’ compared to ‘JF308’ on day 21. This information on the molecular regulatory mechanisms and metabolic pathways of post-harvest quality changes in tomato fruit provides a theoretical foundation for slowing post-harvest decay and loss, and has theoretical importance and application value in breeding for longer shelf life cultivars.https://www.frontiersin.org/articles/10.3389/fpls.2023.1142913/fullstoragetomatotranscriptomemetabolomeATAC-seqtranscription factor
spellingShingle Susu Guo
Susu Guo
Susu Guo
Susu Guo
Susu Guo
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanhai Ji
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Yanyan Zheng
Christopher B. Watkins
Lili Ma
Qing Wang
Qing Wang
Qing Wang
Qing Wang
Hao Liang
Hao Liang
Hao Liang
Hao Liang
Chunmei Bai
Chunmei Bai
Chunmei Bai
Chunmei Bai
Anzhen Fu
Anzhen Fu
Anzhen Fu
Anzhen Fu
Ling Li
Demei Meng
Mingchi Liu
Mingchi Liu
Mingchi Liu
Mingchi Liu
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
Jinhua Zuo
Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
Frontiers in Plant Science
storage
tomato
transcriptome
metabolome
ATAC-seq
transcription factor
title Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
title_full Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
title_fullStr Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
title_full_unstemmed Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
title_short Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit
title_sort transcriptomic metabolomic and atac seq analysis reveal the regulatory mechanism of senescence of post harvest tomato fruit
topic storage
tomato
transcriptome
metabolome
ATAC-seq
transcription factor
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1142913/full
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