马铃薯块茎膨大过程中代谢和转录动态变化的多组学分析

doi:10.1016/j.jia.2025.12.070

Journal of Integrative Agriculture ›› 2026, Vol. 25 ›› Issue (8): 3282-3294.DOI: 10.1016/j.jia.2025.12.070

马铃薯块茎膨大过程中代谢和转录动态变化的多组学分析

收稿日期:2025-04-01 修回日期:2025-12-31 接受日期:2025-09-25 出版日期:2026-08-20 发布日期:2026-07-08

Multi-omics analysis reveals dynamic metabolic and transcriptomic changes during potato tuber swelling

Jiangyue Long^1*, Wei Tan^1*, Chunzhi Zhang², Guangtao Zhu^1#, Zhong Zhang^{2, 1#}

¹Yunnan Key Laboratory of Potato Biology/Engineering Research Center for Valorization of Unique Bio-Resources in Yunnan of Ministry of Education, School of Life Sciences, Yunnan Normal University/Southwest United Graduate School, Kunming 650500, China
²State Key Laboratory of Genome and Multi-omics Technologies/Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture/Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs/Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China

Received:2025-04-01 Revised:2025-12-31 Accepted:2025-09-25 Online:2026-08-20 Published:2026-07-08
About author:Jiangyue Long, E-mail: 2223120031@ynnu.edu.cn, Wei Tan, E-mail: 2223120009@ynnu.edu.cn; #Correspondence Guangtao Zhu, Tel: +86-871-65941387, E-mail: zhuguangtao@ynnu.edu.cn; Zhong Zhang, Tel: +86-755-23250158, E-mail: zhangzhong@caas.cn *These authors contributed equally to this study.
Supported by:
This work was financially supported by the Guangdong Major Project of Basic and Applied Basic Research, China (2021B03
01030004), the National Natural Science Foundation of China (32272725, 32488302), and the China Postdoctoral Science Foundation (2022M723463).

摘要/Abstract

摘要：

马铃薯作为全球重要的粮食作物，为人类提供关键的膳食能量与营养。然而，块茎发育过程中的代谢动态变化及其潜在的转录调控机制尚未明确。本研究整合野生与栽培马铃薯块茎的时序代谢组和转录组分析，鉴定出 849 种代谢物呈现 10 种不同的时序积累模式，其中 6 种为两种基因型共有的积累模式，4 种为基因型特异模式。野生种质块茎膨大早期脂质含量显著减少，后期酚酸含量显著增加；栽培种质则在膨大早期酚酸含量显著增加，后期酚酸、氨基酸及类黄酮含量显著减少。代谢物差异比较分析进一步显示，与野生种质相比，栽培种质块茎的甾体糖苷生物碱（SGA）含量显著降低，类黄酮含量显著提高，这与栽培种质苦味减轻、薯肉着色增强的性状表现一致。共表达网络分析鉴定出 35 个与 SGA 含量、57 个与苯丙烷类代谢物含量高度相关的候选基因。转基因功能验证表明，候选转录因子 MYB113 可通过调控关键合成基因（PAL、C3H 和 HCT）的表达，促进块茎中酚酸的生物合成。本研究阐明了块茎发育过程中的代谢与转录动态规律，为通过分子育种改良块茎代谢品质提供了理论依据。

Abstract:

Potato is a vital global food source, yet the metabolic and transcriptional regulation governing tuber development and quality remains poorly understood. Here, we performed integrated metabolomic and transcriptomic analyses in wild and cultivated potato tubers, revealing dynamic and distinct metabolic accumulation patterns. The 849 metabolites exhibited 10 distinct temporal accumulation patterns, including six shared patterns between accessions and four genotype-specific patterns. The wild genotype exhibited an early decrease in lipids, followed by an increase in phenolic acids, whereas the cultivated genotype displayed an early increase in phenolic acids, accompanied by a decrease in some phenolic acids, amino acids, and flavonoids. A comparative analysis highlighted the cultivated genotype exhibited significantly lower levels of bitter steroidal glycoalkaloids (SGAs) but higher levels of beneficial flavonoids compared with its wild relative. Co-expression network analysis revealed 35 SGA-related and 57 phenylpropanoid-related genes that underlie metabolite dynamics. Notably, we functionally validated that the transcription factor StMYB113 plays a previously unknown role in positively regulating phenolic acid biosynthesis in tuber flesh. Our work provides a comprehensive map of tuber metabolism and a valuable resource for accelerating the genetic improvement of key potato quality traits.

Key words: potato , multi-omics , steroidal glycoalkaloid , phenylpropanoid , transcriptional regulation

Jiangyue Long, Wei Tan, Chunzhi Zhang, Guangtao Zhu, Zhong Zhang. 马铃薯块茎膨大过程中代谢和转录动态变化的多组学分析[J]. Journal of Integrative Agriculture, 2026, 25(8): 3282-3294.

Jiangyue Long, Wei Tan, Chunzhi Zhang, Guangtao Zhu, Zhong Zhang. Multi-omics analysis reveals dynamic metabolic and transcriptomic changes during potato tuber swelling[J]. Journal of Integrative Agriculture, 2026, 25(8): 3282-3294.

参考文献

Afnan Saleem A, Akhtar M F, Sharif A, Akhtar B, Siddique R, Ashraf G M, Alghamdi B S, Alharthy S A. 2022. Anticancer, cardio-protective and anti-inflammatory potential of natural-sources-derived phenolic acids. Molecules, 27, 7286.

Akiyama R, Umemoto N, Mizutani M. 2023. Recent advances in steroidal glycoalkaloid biosynthesis in the genus Solanum. Plant Biotechnology, 40, 185–191.

Al-Khayri J M, Sahana G R, Nagella P, Joseph B V, Alessa F M, Al-Mssallem M Q. 2022. Flavonoids as potential anti-inflammatory molecules: A review. Molecules, 27, 2901.

Ali U, Li H, Wang X, Guo L. 2018. Emerging roles of sphingolipid signaling in plant response to biotic and abiotic stresses. Molecular Plant, 11, 1328–1343.

Bao H, Yuan L, Luo Y, Jing X, Zhang Z, Wang J, Zhu G. 2024. A freezing responsive UDP-glycosyltransferase improves potato freezing tolerance via modifying flavonoid metabolism. Horticultural Plant Journal, 11, 1595–1606.

Cai J, Aharoni A. 2022. Amino acids and their derivatives mediating defense priming and growth tradeoff. Current Opinion in Plant Biology, 69, 102288.

Cárdenas P D, Sonawane P D, Heinig U, Jozwiak A, Panda S, Abebie B, Kazachkova Y, Pliner M, Unger T, Wolf D, Ofner I, Vilaprinyo E, Meir S, Davydov O, Gal-on A, Burdman S, Giri A, Zamir D, Scherf T, Szymanski J, et al. 2019. Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases. Nature Communications, 10, 5169.

Cárdenas P D, Sonawane P D, Pollier J, Vanden Bossche R, Dewangan V, Weithorn E, Tal L, Meir S, Rogachev I, Malitsky S, Giri A P, Goossens A, Burdman S, Aharoni A. 2016. GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nature Communications, 7, 10654.

Cenzano A, Cantoro R, Racagni G, De Los Santos-Briones C, Hernández-Sotomayor T, Abdala G. 2008. Phospholipid and phospholipase changes by jasmonic acid during stolon to tuber transition of potato. Plant Growth Regulation, 56, 307–316.

D’Amelia V, Aversano R, Batelli G, Caruso I, Castellano Moreno M, Castro-Sanz A B, Chiaiese P, Fasano C, Palomba F, Carputo D. 2014. High AN1 variability and interaction with basic helix-loop-helix co-factors related to anthocyanin biosynthesis in potato leaves. The Plant Journal, 80, 527–540.

Deng Y, Lu S. 2017. Biosynthesis and regulation of phenylpropanoids in plants. Critical Reviews in Plant Sciences, 36, 257–290.

Du H, Zhai Z, Pu J, Liang J, Wang R, Zhang Z, Wang P, Zhu Y, Huang L, Li D, Chen K, Zhu G, Zhang C. 2025. Two tandem R2R3 MYB transcription factor genes cooperatively regulate anthocyanin accumulation in potato tuber flesh. Plant Biotechnology Journal, 23, 1521–1534.

González Moreno A, de Cózar A, Prieto P, Domínguez E, Heredia A. 2022. Radiationless mechanism of UV deactivation by cuticle phenolics in plants. Nature Communications, 13, 1786.

Hardigan M A, Laimbeer F P E, Newton L, Crisovan E, Hamilton J P, Vaillancourt B, Wiegert-Rininger K, Wood J C, Douches D S, Farré E M, Veilleux R E, Buell C R. 2017. Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proceedings of the National Academy of Sciences of the United States of America, 114, E9999–E10008.

Häusler R E, Ludewig F, Krueger S. 2014. Amino acids - A life between metabolism and signaling. Plant Science, 229, 225–237.

Jia H, Xu Y, Deng Y, Xie Y, Gao Z, Lang Z, Niu Q. 2024. Key transcription factors regulate fruit ripening and metabolite accumulation in tomato. Plant Physiology, 195, 2256–2273.

Johns T, Alonso J G. 1990. Glycoalkaloid change during the domestication of the potato, Solanum section Petota. Euphytica, 50, 203–210.

Kang S, Wang F. 2024. Key players in plant defense: How scaffold protein GAME15 orchestrates the biosynthesis of steroidal defense metabolite. Advanced Agrochem, 4, 10–12.

Kim D, Paggi J M, Park C, Bennett C, Salzberg S L. 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907–915.

Kimura S, Chikagawa Y, Kato M, Maeda K, Ozeki Y. 2008. Upregulation of the promoter activity of the carrot (Daucus carota) phenylalanine ammonia-lyase gene (DcPAL3) is caused by new members of the transcriptional regulatory proteins, DcRERF1 and DcERF2, which bind to the GCC-box homolog and act as an activator to the DcPAL3 promoter. Journal of Plant Research, 121, 499–508.

Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.

Li Y, Chen Y, Zhou L, You S, Deng H, Chen Y, Alseekh S, Yuan Y, Fu R, Zhang Z, Su D, Fernie A R, Bouzayen M, Ma T, Liu M, Zhang Y. 2020. MicroTom metabolic network: Rewiring tomato metabolic regulatory network throughout the growth cycle. Molecular Plant, 13, 1203–1218.

Liu Y, Li Y, Liu Z, Wang L, Lin-Wang K, Zhu J, Bi Z, Sun C, Zhang J, Bai J. 2023. Integrative analysis of metabolome and transcriptome reveals a dynamic regulatory network of potato tuber pigmentation. iScience, 26, 105903.

Liu Y, Kui L W, Espley R V, Wang L, Yang H, Yu B, Dare A, Varkonyi-Gasic E, Wang J, Zhang J, Wang D, Allan A C. 2016. Functional diversification of the potato R2R3 MYB anthocyanin activators AN1, MYBA1, and MYB113 and their interaction with basic helix-loop-helix cofactors. Journal of Experimental Botany, 67, 2159–2176.

Lucier R, Kamileen M O, Nakamura Y, Serediuk S, Barbole R, Wurlitzer J, Kunert M, Heinicke S, O’Connor S E, Sonawane P D. 2024. Steroidal scaffold decorations in Solanum alkaloid biosynthesis. Molecular Plant, 17, 1236–1254.

Luo J, He C, Yan S, Jiang C, Chen A, Li K, Zhu Y, Gui S, Yang N, Xiao Y, Wu S, Zhang F, Liu T, Wang J, Huang W, Yang Y, Wang H, Yang W, Li W, Zhuo L, et al. 2024. A metabolic roadmap of waxy corn flavor. Molecular Plant, 17, 1883–1898.

Malacarne G, Coller E, Czemmel S, Vrhovsek U, Engelen K, Goremykin V, Bogs J, Moser C. 2016. The grapevine VvibZIPC22 transcription factor is involved in the regulation of flavonoid biosynthesis. Journal of Experimental Botany, 67, 3509–3522.

Mandal S M, Chakraborty D, Dey S. 2010. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signaling & Behavior, 5, 359–368.

Mao J, Gao Z, Wang X, Lin M, Chen L, Ning X. 2024. Combined widely targeted metabolomic, transcriptomic, and spatial metabolomic analysis reveals the potential mechanism of coloration and fruit quality formation in Actinidia chinensis cv. Hongyang. Foods, 13, 233.

Mattioli R, Francioso A, Mosca L, Silva P. 2020. Anthocyanins: A comprehensive review of their chemical properties and health effects on cardiovascular and neurodegenerative diseases. Molecules, 25, 3809.

Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S. 2009. Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant and Cell Physiology, 50, 2210–2222.

Okazaki Y, Saito K. 2014. Roles of lipids as signaling molecules and mitigators during stress response in plants. The Plant Journal, 79, 584–596.

Peng Z, Wang P, Tang D, Shang Y, Li C, Huang S, Zhang C. 2019. Inheritance of steroidal glycoalkaloids in potato tuber flesh. Journal of Integrative Agriculture, 18, 2255–2263.

Rao M J, Zheng B. 2025. The role of polyphenols in abiotic stress tolerance and their antioxidant properties to scavenge reactive oxygen species and free radicals. Antioxidants, 14, 74.

Shannon P, Markiel A, Ozier O, Baliga N S, Wang J T, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498–2504.

Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B. 2019. Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules, 24, 2452.

Shen N, Wang T, Gan Q, Liu S, Wang L, Jin B. 2022. Plant flavonoids: Classification, distribution, biosynthesis, and antioxidant activity. Food Chemistry, 383, 132531.

Sonawane P D, Gharat S A, Jozwiak A, Barbole R, Heinicke S, Almekias-Siegl E, Meir S, Rogachev I, Connor S E O, Giri A P, Aharoni A. 2023. A BAHD-type acyltransferase concludes the biosynthetic pathway of non-bitter glycoalkaloids in ripe tomato fruit. Nature Communications, 14, 4540.

Sonawane P D, Jozwiak A, Barbole R, Panda S, Abebie B, Kazachkova Y, Gharat S A, Ramot O, Unger T, Wizler G, Meir S, Rogachev I, Doron-Faigenboim A, Petreikov M, Schaffer A, Giri A P, Scherf T, Aharoni A. 2022. 2-oxoglutarate-dependent dioxygenases drive expansion of steroidal alkaloid structural diversity in the genus Solanum. New Phytologist, 234, 1394–1410.

Song Z, Xu X, Chen X, Chang J, Li J, Cheng J, Zhang B. 2024. Multi-omics analysis provides insights into the mechanism underlying fruit color formation in Capsicum. Frontiers in Plant Science, 15, 1448060.

Strygina K V, Kochetov A V, Khlestkina E K. 2019. Genetic control of anthocyanin pigmentation of potato tissues. BMC Genetics, 20, 27.

Tai H H, Worrall K, Pelletier Y, De Koeyer D, Calhoun L A. 2014. Comparative metabolite profiling of Solanum tuberosum against six wild Solanum species with colorado potato beetle resistance. Journal of Agricultural and Food Chemistry, 62, 9043–9055.

Umemoto N, Nakayasu M, Ohyama K, Yotsu-Yamashita M, Mizutani M, Seki H, Saito K, Muranaka T. 2016. Two cytochrome P450 monooxygenases catalyze early hydroxylation steps in the potato steroid glycoalkaloid biosynthetic pathway. Plant Physiology, 171, 2458–2467.

Wang C, Meng L, Gao Y, Grierson D, Fu D. 2018. Manipulation of light signal transduction factors as a means of modifying steroidal glycoalkaloids accumulation in tomato leaves. Frontiers in Plant Science, 9, 437.

Wang R, Shu P, Zhang C, Zhang J, Chen Y, Zhang Y, Du K, Xie Y, Li M, Ma T, Zhang Y, Li Z, Grierson D, Pirrello J, Chen K, Bouzayen M, Zhang B, Liu M. 2022. Integrative analyses of metabolome and genome-wide transcriptome reveal the regulatory network governing flavor formation in kiwifruit (Actinidia chinensis). New Phytologist, 233, 373–389.

Wolters P J, Wouters D, Tikunov Y M, Ayilalath S, Kodde L P, Strijker M F, Caarls L, Visser R G F, Vleeshouwers V G. 2023. Tetraose steroidal glycoalkaloids from potato provide resistance against Alternaria solani and Colorado potato beetle. eLife, 12, RP87135.

Xie Y, Xu Y, Jia H, Wang K, Chen S, Ma T, Deng Y, Lang Z, Niu Q. 2024. Tomato MADS-RIN regulates GAME5 expression to promote non-bitter glycoalkaloid biosynthesis in fruit. The Plant Journal, 120, 2500–2514.

Xu J, Yan J, Li W, Wang Q, Wang C, Guo J, Geng D, Guan Q, Ma F. 2020. Integrative analyses of widely targeted metabolic profiling and transcriptome data reveals molecular insight into metabolomic variations during apple (Malus domestica) fruit development and ripening. International Journal of Molecular Sciences, 21, 4797.

Yang X, Zhang L, Guo X, Xu J, Zhang K, Yang Y, Yang Y, Jian Y, Dong D, Huang S, Cheng F, Li G. 2023. The gap-free potato genome assembly reveals large tandem gene clusters of agronomical importance in highly repeated genomic regions. Molecular Plant, 16, 314–317.

Ye M, Peng Z, Tang D, Yang Z, Li D, Xu Y, Zhang C, Huang S. 2018. Generation of self-compatible diploid potato by knockout of S-RNase. Nature Plants, 4, 651–654.

Zhang Z, Shi Q, Wang B, Ma A, Wang Y, Xue Q, Shen B, Hamaila H, Tang T, Qi X, Fernie A R, Luo J, Li X. 2022. Jujube metabolome selection determined the edible properties acquired during domestication. The Plant Journal, 109, 1116–1133.

Zhang Z, Zhou D, Li S, Pan J, Liang J, Wu X, Wu X N, Krall L, Zhu G. 2023. Multi-omics analysis reveals the chemical and genetic bases of pigmented potato tuber. Journal of Agricultural and Food Chemistry, 71, 16402–16416.

Zhang Z, Zhou J, Zhao Y, Zhao X, Liu J, Liu J, Zhang J, Song B, Zhang H. 2024. StMYB113 promotes anthocyanin biosynthesis in potato (Solanum tuberosum L.) désirée tubers. Potato Research, 67, 307–324.

Zhao L, Zhang B, Huang H, Huang W, Zhang Z, Wang Q, Luo H, An B. 2023. Metabolomic and transcriptomic analyses provide insights into metabolic networks during cashew fruit development and ripening. Food Chemistry, 404, 134765.

Zhao X, Zhang H, Liu T, Zhao Y, Hu X, Liu S, Lin Y, Song B, He C. 2023a. Transcriptome analysis provides StMYBA1 gene that regulates potato anthocyanin biosynthesis by activating structural genes. Frontiers in Plant Science, 14, 1087121.

Zhao X, Zhang Y, Lai J, Deng Y, Hao Y, Wang S, Yang J. 2023b. The SlDOG1 affect biosynthesis of steroidal glycoalkaloids by regulating GAME expression in tomato. International Journal of Molecular Sciences, 24, 3360.

Zhu Z, Wei L, Guo L, Bao H, Wang X, Kear P, Wang Z, Zhu G. 2023. Integrated full-length transcriptome and metabolome profiling reveals flavonoid regulation in response to freezing stress in potato. Plants, 12, 2054.

马铃薯块茎膨大过程中代谢和转录动态变化的多组学分析

Multi-omics analysis reveals dynamic metabolic and transcriptomic changes during potato tuber swelling

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics