Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry

Strawberry (<i>Fragaria ananassa</i>) is a widely grown horticultural crop, which exists in red, yellow, and white varieties. In recent years, the white-fleshed strawberry variety is gaining more attention from consumers for its unique taste and appearance, but a comprehensive understand...

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Main Authors: Linlin Xu, Xiaodong Chen, Qinglian Wang, Mizhen Zhao, Yushan Qiao, Zhaobiao Xie, Chuanwen Sun, Miao Sun, Weijian Cai
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Agronomy
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Online Access:https://www.mdpi.com/2073-4395/14/12/2860
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author Linlin Xu
Xiaodong Chen
Qinglian Wang
Mizhen Zhao
Yushan Qiao
Zhaobiao Xie
Chuanwen Sun
Miao Sun
Weijian Cai
author_facet Linlin Xu
Xiaodong Chen
Qinglian Wang
Mizhen Zhao
Yushan Qiao
Zhaobiao Xie
Chuanwen Sun
Miao Sun
Weijian Cai
author_sort Linlin Xu
collection DOAJ
description Strawberry (<i>Fragaria ananassa</i>) is a widely grown horticultural crop, which exists in red, yellow, and white varieties. In recent years, the white-fleshed strawberry variety is gaining more attention from consumers for its unique taste and appearance, but a comprehensive understanding of the molecular processes governing the ripening of white-fleshed strawberry remains undisclosed. In this study, based on the joint analysis of physiology, metabolome, and transcriptome, we screened and identified the key metabolites that were highly correlated to the maturation of white-fleshed strawberry (cv. ‘snow white’, SW for short) fruits. In contrast to red-fleshed strawberries, SW fruits exhibited three main ripening stages during the maturation, accompanied by the increases in total soluble solid and total sugar and the declines in total anthocyanin and total acid. Metabolomic analysis identified 832 differential accumulated metabolites (DAMs) at the secondary level of LC-MS/MS, and further investigations suggested that the increase in sucrose, citric acid, and epicatechin levels potentially play a role in the ripening process of SW fruits. Furthermore, abscisic acid and methyl jasmonate were recognized as the primary phytohormones involved in the production of these metabolites. The enrichment analysis of RNA-Seq data revealed that the differential expressed genes (DEGs) were primarily attributed to the pathways of ‘Starch and sucrose metabolism’ and ‘Plant hormone signal transduction’ but were undetected in ‘Flavonoid biosynthesis’ at the late ripening stage. Moreover, the de novo biosynthesis pathway, WGCNA, and Pearson correlation analysis indicated a direct relationship between <i>FaSPS1</i>, <i>FaSPP1</i>, and <i>FaSPP2</i> with sucrose, <i>FaPEPC1</i>, <i>FaV</i>-<i>PPase2</i>, and <i>FaV</i>-<i>PPase3</i> with citric acid, and <i>Fa4CL2</i>, <i>Fa4CL3</i>, and <i>FaANR1</i> with anthocyanin. Further analysis revealed a co-expression of MYBs, bHLHs, NACs, and WRKYs with the structural genes mentioned. Overall, our findings uncovered a molecular mechanism regulating the maturation of white-fleshed strawberry, providing valuable insights for enhancing the flavor of white-fleshed strawberry through the gene-editing technique.
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spelling doaj-art-a33c3812e71d45e0a60d37fa3fdb1ca32025-08-20T02:56:03ZengMDPI AGAgronomy2073-43952024-11-011412286010.3390/agronomy14122860Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed StrawberryLinlin Xu0Xiaodong Chen1Qinglian Wang2Mizhen Zhao3Yushan Qiao4Zhaobiao Xie5Chuanwen Sun6Miao Sun7Weijian Cai8Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaJiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaJiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaJiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaJiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaAgricultural Technology Extension Center of Yandu District, Yancheng 224002, ChinaAgricultural Technology Extension Center of Yandu District, Yancheng 224002, ChinaCollege of Marine and Biological Engineering, Yancheng Teachers University, Yancheng 224002, ChinaJiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Pomology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, ChinaStrawberry (<i>Fragaria ananassa</i>) is a widely grown horticultural crop, which exists in red, yellow, and white varieties. In recent years, the white-fleshed strawberry variety is gaining more attention from consumers for its unique taste and appearance, but a comprehensive understanding of the molecular processes governing the ripening of white-fleshed strawberry remains undisclosed. In this study, based on the joint analysis of physiology, metabolome, and transcriptome, we screened and identified the key metabolites that were highly correlated to the maturation of white-fleshed strawberry (cv. ‘snow white’, SW for short) fruits. In contrast to red-fleshed strawberries, SW fruits exhibited three main ripening stages during the maturation, accompanied by the increases in total soluble solid and total sugar and the declines in total anthocyanin and total acid. Metabolomic analysis identified 832 differential accumulated metabolites (DAMs) at the secondary level of LC-MS/MS, and further investigations suggested that the increase in sucrose, citric acid, and epicatechin levels potentially play a role in the ripening process of SW fruits. Furthermore, abscisic acid and methyl jasmonate were recognized as the primary phytohormones involved in the production of these metabolites. The enrichment analysis of RNA-Seq data revealed that the differential expressed genes (DEGs) were primarily attributed to the pathways of ‘Starch and sucrose metabolism’ and ‘Plant hormone signal transduction’ but were undetected in ‘Flavonoid biosynthesis’ at the late ripening stage. Moreover, the de novo biosynthesis pathway, WGCNA, and Pearson correlation analysis indicated a direct relationship between <i>FaSPS1</i>, <i>FaSPP1</i>, and <i>FaSPP2</i> with sucrose, <i>FaPEPC1</i>, <i>FaV</i>-<i>PPase2</i>, and <i>FaV</i>-<i>PPase3</i> with citric acid, and <i>Fa4CL2</i>, <i>Fa4CL3</i>, and <i>FaANR1</i> with anthocyanin. Further analysis revealed a co-expression of MYBs, bHLHs, NACs, and WRKYs with the structural genes mentioned. Overall, our findings uncovered a molecular mechanism regulating the maturation of white-fleshed strawberry, providing valuable insights for enhancing the flavor of white-fleshed strawberry through the gene-editing technique.https://www.mdpi.com/2073-4395/14/12/2860white-fleshed strawberryripeningsucrosecitric acidanthocyanin
spellingShingle Linlin Xu
Xiaodong Chen
Qinglian Wang
Mizhen Zhao
Yushan Qiao
Zhaobiao Xie
Chuanwen Sun
Miao Sun
Weijian Cai
Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
Agronomy
white-fleshed strawberry
ripening
sucrose
citric acid
anthocyanin
title Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
title_full Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
title_fullStr Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
title_full_unstemmed Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
title_short Metabolomic and Transcriptomic Analysis Revealed the Maturation Mechanism of White-Fleshed Strawberry
title_sort metabolomic and transcriptomic analysis revealed the maturation mechanism of white fleshed strawberry
topic white-fleshed strawberry
ripening
sucrose
citric acid
anthocyanin
url https://www.mdpi.com/2073-4395/14/12/2860
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