Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties

Soluble sugars and organic acids constitute the primary flavor determinants in fruits and elucidating their metabolic mechanisms provides crucial theoretical foundations for fruit breeding practices and food industry development. Through integrated physiological and transcriptomic analysis of pomegr...

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Main Authors: Ding Ke, Yilong Zhang, Yingfen Teng, Xueqing Zhao
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Foods
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Online Access:https://www.mdpi.com/2304-8158/14/10/1755
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author Ding Ke
Yilong Zhang
Yingfen Teng
Xueqing Zhao
author_facet Ding Ke
Yilong Zhang
Yingfen Teng
Xueqing Zhao
author_sort Ding Ke
collection DOAJ
description Soluble sugars and organic acids constitute the primary flavor determinants in fruits and elucidating their metabolic mechanisms provides crucial theoretical foundations for fruit breeding practices and food industry development. Through integrated physiological and transcriptomic analysis of pomegranate varieties ‘Sharp Velvet’ with high acid content and ‘Azadi’ with low acid content, this study demonstrated that the differences in flavor between the two varieties were mainly caused by differences in citric acid content rather than in soluble sugar content. Transcriptome profiling identified 11 candidate genes involved in sugar and acid metabolism, including three genes associated with soluble sugar metabolism (<i>FBA1</i>, <i>SS</i>, and <i>SWEET16</i>) and eight genes linked to organic acid metabolism (<i>ADH1</i>, <i>GABP1</i>, <i>GABP2</i>, <i>GABP3</i>, <i>GABP4</i>, <i>ICL</i>, <i>ME1</i>, and <i>PDC4</i>). These data indicated that differences in citric acid content between the two varieties mainly stemmed from differences in the regulation of the citric acid degradation pathway, which relies mainly on the γ-aminobutyric acid (GABA) branch rather than the isocitric acid lyase (ICL) pathway. Citric acid accumulation in pomegranate fruit was driven by metabolic fluxes rather than vesicular storage capacity. Weighted gene co-expression network analysis (WGCNA) uncovered a significant citric acid content associated module (r = −0.72) and predicted six core transcriptional regulators (<i>bHLH42</i>, <i>ERF4</i>, <i>ERF062</i>, <i>WRKY6</i>, <i>WRKY23</i>, and <i>WRKY28</i>) within this network. Notably, <i>bHLH42</i>, <i>ERF4</i>, and <i>WRKY28</i> showed significant positive correlations with citric acid content, whereas <i>ERF062</i>, <i>WRKY6</i>, and <i>WRKY23</i> demonstrated significant negative correlations. Our findings provide comprehensive insights into the genetic architecture governing soluble sugars and organic acids homeostasis in pomegranate, offering both a novel mechanistic understanding of fruit acidity regulation and valuable molecular targets for precision breeding of fruit quality traits.
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spelling doaj-art-734ec8e5f3ab4d99a0726827eb7653df2025-08-20T03:48:01ZengMDPI AGFoods2304-81582025-05-011410175510.3390/foods14101755Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) VarietiesDing Ke0Yilong Zhang1Yingfen Teng2Xueqing Zhao3Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaSoluble sugars and organic acids constitute the primary flavor determinants in fruits and elucidating their metabolic mechanisms provides crucial theoretical foundations for fruit breeding practices and food industry development. Through integrated physiological and transcriptomic analysis of pomegranate varieties ‘Sharp Velvet’ with high acid content and ‘Azadi’ with low acid content, this study demonstrated that the differences in flavor between the two varieties were mainly caused by differences in citric acid content rather than in soluble sugar content. Transcriptome profiling identified 11 candidate genes involved in sugar and acid metabolism, including three genes associated with soluble sugar metabolism (<i>FBA1</i>, <i>SS</i>, and <i>SWEET16</i>) and eight genes linked to organic acid metabolism (<i>ADH1</i>, <i>GABP1</i>, <i>GABP2</i>, <i>GABP3</i>, <i>GABP4</i>, <i>ICL</i>, <i>ME1</i>, and <i>PDC4</i>). These data indicated that differences in citric acid content between the two varieties mainly stemmed from differences in the regulation of the citric acid degradation pathway, which relies mainly on the γ-aminobutyric acid (GABA) branch rather than the isocitric acid lyase (ICL) pathway. Citric acid accumulation in pomegranate fruit was driven by metabolic fluxes rather than vesicular storage capacity. Weighted gene co-expression network analysis (WGCNA) uncovered a significant citric acid content associated module (r = −0.72) and predicted six core transcriptional regulators (<i>bHLH42</i>, <i>ERF4</i>, <i>ERF062</i>, <i>WRKY6</i>, <i>WRKY23</i>, and <i>WRKY28</i>) within this network. Notably, <i>bHLH42</i>, <i>ERF4</i>, and <i>WRKY28</i> showed significant positive correlations with citric acid content, whereas <i>ERF062</i>, <i>WRKY6</i>, and <i>WRKY23</i> demonstrated significant negative correlations. Our findings provide comprehensive insights into the genetic architecture governing soluble sugars and organic acids homeostasis in pomegranate, offering both a novel mechanistic understanding of fruit acidity regulation and valuable molecular targets for precision breeding of fruit quality traits.https://www.mdpi.com/2304-8158/14/10/1755pomegranatesoluble sugarsorganic acidstranscriptomic profiledifferentially expressed genestranscription factor
spellingShingle Ding Ke
Yilong Zhang
Yingfen Teng
Xueqing Zhao
Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
Foods
pomegranate
soluble sugars
organic acids
transcriptomic profile
differentially expressed genes
transcription factor
title Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
title_full Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
title_fullStr Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
title_full_unstemmed Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
title_short Transcriptomic Profiling Uncovers Molecular Basis for Sugar and Acid Metabolism in Two Pomegranate (<i>Punica granatum</i>) Varieties
title_sort transcriptomic profiling uncovers molecular basis for sugar and acid metabolism in two pomegranate i punica granatum i varieties
topic pomegranate
soluble sugars
organic acids
transcriptomic profile
differentially expressed genes
transcription factor
url https://www.mdpi.com/2304-8158/14/10/1755
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AT yilongzhang transcriptomicprofilinguncoversmolecularbasisforsugarandacidmetabolismintwopomegranateipunicagranatumivarieties
AT yingfenteng transcriptomicprofilinguncoversmolecularbasisforsugarandacidmetabolismintwopomegranateipunicagranatumivarieties
AT xueqingzhao transcriptomicprofilinguncoversmolecularbasisforsugarandacidmetabolismintwopomegranateipunicagranatumivarieties