Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis

Cold-induced sweetening (CIS) in potatoes is a significant challenge affecting the quality and marketability of processed potato products. This study aims to decipher the regulatory mechanisms underlying CIS through integrated time-course transcriptome and metabolome analysis. Freshly harvested pota...

Full description

Saved in:
Bibliographic Details
Main Authors: Guangcan Cui, Tingting Zhou, Zhongliang Liu, Ting Wang, Qingguo Wang, Tengfei Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1551265/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850200680826929152
author Guangcan Cui
Tingting Zhou
Tingting Zhou
Zhongliang Liu
Ting Wang
Qingguo Wang
Tengfei Liu
author_facet Guangcan Cui
Tingting Zhou
Tingting Zhou
Zhongliang Liu
Ting Wang
Qingguo Wang
Tengfei Liu
author_sort Guangcan Cui
collection DOAJ
description Cold-induced sweetening (CIS) in potatoes is a significant challenge affecting the quality and marketability of processed potato products. This study aims to decipher the regulatory mechanisms underlying CIS through integrated time-course transcriptome and metabolome analysis. Freshly harvested potato tubers (Solanum tuberosum L. cv. ‘Netherlands No. 15’) were stored at 4°C and 20°C for various durations. RNA sequencing and quantitative real-time PCR were employed to analyze gene expression changes, while metabolomic profiling was conducted using UHPLC-MS/MS. Our results reveal significant alterations in carbohydrate metabolism, with a marked increase in reducing sugars during cold storage. Critical enzymes involved in starch degradation, such as β-amylases (StBAM1, StBAM9), and sucrose metabolic genes (StUGPase2, StVInv) were upregulated, while starch synthesis genes were downregulated. Co-expression analysis identified potential transcription factors, including StHSFA2 and StAPRR2, which may regulate these metabolic pathways. Functional assays demonstrated that StHSFA2 significantly activates the promoters of StBAM1 and StUGPase2, while StAPRR2 shows specific activation of the StVInv enhancer. These findings suggest distinct but complementary roles for StHSFA2 and StAPRR2 in regulating starch degradation and sucrose metabolism during CIS. This comprehensive analysis provides insights into the molecular mechanisms of CIS and identifies potential targets for genetic manipulation to mitigate its effects, thereby enhancing the storage quality and processing performance of potatoes.
format Article
id doaj-art-ac2ff13d5f0a40e7a143ba714b885bdb
institution OA Journals
issn 1664-462X
language English
publishDate 2025-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj-art-ac2ff13d5f0a40e7a143ba714b885bdb2025-08-20T02:12:15ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-04-011610.3389/fpls.2025.15512651551265Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysisGuangcan Cui0Tingting Zhou1Tingting Zhou2Zhongliang Liu3Ting Wang4Qingguo Wang5Tengfei Liu6College of Food Science and Engineering, Shandong Agricultural University, Tai’an, Shandong, ChinaState Key Laboratory of Wheat Breeding, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaDepartment of Agronomy, Kansas State University, Manhattan, KS, United StatesTai’an Academy of Agricultural Sciences, Tai’an, ChinaTai’an Academy of Agricultural Sciences, Tai’an, ChinaCollege of Food Science and Engineering, Shandong Agricultural University, Tai’an, Shandong, ChinaCollege of Food Science and Engineering, Shandong Agricultural University, Tai’an, Shandong, ChinaCold-induced sweetening (CIS) in potatoes is a significant challenge affecting the quality and marketability of processed potato products. This study aims to decipher the regulatory mechanisms underlying CIS through integrated time-course transcriptome and metabolome analysis. Freshly harvested potato tubers (Solanum tuberosum L. cv. ‘Netherlands No. 15’) were stored at 4°C and 20°C for various durations. RNA sequencing and quantitative real-time PCR were employed to analyze gene expression changes, while metabolomic profiling was conducted using UHPLC-MS/MS. Our results reveal significant alterations in carbohydrate metabolism, with a marked increase in reducing sugars during cold storage. Critical enzymes involved in starch degradation, such as β-amylases (StBAM1, StBAM9), and sucrose metabolic genes (StUGPase2, StVInv) were upregulated, while starch synthesis genes were downregulated. Co-expression analysis identified potential transcription factors, including StHSFA2 and StAPRR2, which may regulate these metabolic pathways. Functional assays demonstrated that StHSFA2 significantly activates the promoters of StBAM1 and StUGPase2, while StAPRR2 shows specific activation of the StVInv enhancer. These findings suggest distinct but complementary roles for StHSFA2 and StAPRR2 in regulating starch degradation and sucrose metabolism during CIS. This comprehensive analysis provides insights into the molecular mechanisms of CIS and identifies potential targets for genetic manipulation to mitigate its effects, thereby enhancing the storage quality and processing performance of potatoes.https://www.frontiersin.org/articles/10.3389/fpls.2025.1551265/fullpotatocold-induced sweeteningprocessing qualitytranscriptomeco-expression analysis
spellingShingle Guangcan Cui
Tingting Zhou
Tingting Zhou
Zhongliang Liu
Ting Wang
Qingguo Wang
Tengfei Liu
Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
Frontiers in Plant Science
potato
cold-induced sweetening
processing quality
transcriptome
co-expression analysis
title Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
title_full Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
title_fullStr Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
title_full_unstemmed Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
title_short Deciphering the regulatory mechanisms of potato cold-induced sweetening via integrated time-course transcriptome and metabolome analysis
title_sort deciphering the regulatory mechanisms of potato cold induced sweetening via integrated time course transcriptome and metabolome analysis
topic potato
cold-induced sweetening
processing quality
transcriptome
co-expression analysis
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1551265/full
work_keys_str_mv AT guangcancui decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT tingtingzhou decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT tingtingzhou decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT zhongliangliu decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT tingwang decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT qingguowang decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis
AT tengfeiliu decipheringtheregulatorymechanismsofpotatocoldinducedsweeteningviaintegratedtimecoursetranscriptomeandmetabolomeanalysis