{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T11:00:06Z","timestamp":1789988406616,"version":"4.0.1"},"reference-count":32,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T00:00:00Z","timestamp":1789689600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100011501","name":"Leading Scientist Project of Qinghai Province \u201cCapacity Improvement of Innovation System of Potato Breeding and Seed Industry Production in Plateau\u201d","doi-asserted-by":"publisher","award":["2023-NK-146"],"award-info":[{"award-number":["2023-NK-146"]}],"id":[{"id":"10.13039\/501100011501","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Potato tubers exhibit prominent spatial heterogeneity in starch accumulation across distinct anatomical zones, yet the underlying transcriptional and metabolic regulatory mechanisms remain unclear, especially the molecular basis for divergent starch deposition between high- and low-starch tetraploid cultivars. In this study, the high-starch cultivar Atlantic (DX) and low-starch cultivar Dingshu No. 1 (D) were used as experimental materials. Dynamic starch contents of the tuber cortex (CR), perimedullary region (PMR), and inner medullary region (IMR) were measured throughout starch biosynthetic stages. Integrated untargeted metabolomics and RNA-seq transcriptomics were performed to compare transcriptional and metabolic differentiation between CR and IMR with the largest starch gap, followed by qRT-PCR verification of hub genes. Physiological results showed that starch content in both cultivars followed the gradient CR &gt; PMR &gt; IMR, and inter-regional starch disparities expanded continuously with tuber development; low-starch D had lower overall starch levels and milder tissue differences than DX. Transcriptomic analysis revealed massive transcriptional activation in the cortex of both cultivars, while D displayed far more dramatic transcriptional divergence between CR and IMR than DX. Core transcription factors including AP2\/ERF, bHLH and MYB were identified to mediate tissue-specific starch synthesis. Metabolomic data demonstrated severe carbon metabolic polarization in D (hyperactive cortex, weak inner medulla), whereas DX maintained balanced sugar metabolism across whole tuber tissues. Integrated multi-omics analysis of the starch and sucrose pathway (ko00500) screened 18 key structural genes. High-starch DX upregulated starch synthetic and sugar transport genes while repressing starch hydrolysis and carbon diversion genes, realizing coordinated whole-tuber carbon flux toward starch production. In contrast, D showed disrupted regulatory networks, excessive carbon shunting to secondary metabolism and aggravated starch degradation, limiting starch accumulation. Three conserved negative regulatory candidate genes, LOC102593331 (TPS), LOC102584887 (AMY), and LOC102580651 (EN), were characterized via tissue expression profiling: TPS dominates upstream carbon flux allocation, EN competes for starch precursors during cell wall synthesis, and AMY accelerates starch breakdown. This study systematically uncovered the molecular framework of spatial starch heterogeneity in tetraploid potato tubers, clarified the essential distinctions in carbon partitioning strategies between high- and low-starch cultivars, and provided valuable gene resources and theoretical support for high-starch potato molecular design breeding.<\/jats:p>","DOI":"10.3390\/biology15181655","type":"journal-article","created":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T09:01:38Z","timestamp":1789981298000},"page":"1655","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Integrated Transcriptomic and Metabolomic Analysis of Starch Biosynthesis in Different Spatial Regions of Tetraploid Potato Tubers"],"prefix":"10.3390","volume":"15","author":[{"given":"Huanhuan","family":"Lian","sequence":"first","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Chao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"conceptualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"}]},{"given":"Guangji","family":"Ye","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Wang","family":"Su","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"supervision","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"conceptualization","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-5423-1296","authenticated-orcid":false,"given":"Shenglong","family":"Yang","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"resources","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]},{"given":"Yun","family":"Zhou","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"resources","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"}]},{"given":"Yongzhen","family":"Ma","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Jian","family":"Wang","sequence":"additional","affiliation":[{"name":"Academy of Agriculture and Forestry Sciences, Qinghai University, Xining 810016, China"},{"name":"Qinghai Provincial Key Laboratory of Potato Breeding, Qinghai University, Xining 810016, China"},{"name":"Ministry of Education Engineering Research Center of Potato in Northwest Region, Qinghai University, Xining 810016, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"supervision","vocabulary":"credit"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Li, H., Brouwer, M., Del Pup, E., van Lieshout, N., Finkers, R., Bachem, C.W.B., and Visser, R.G.F. (2024). Allelic variation in the autotetraploid potato: Genes involved in starch and steroidal glycoalkaloid metabolism as a case study. BMC Genom., 25.","DOI":"10.1186\/s12864-024-10186-5"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/s12571-012-0220-1","article-title":"Crops that feed the world 8: Potato: Are the trends of increased global production sustainable?","volume":"4","author":"Birch","year":"2012","journal-title":"Food Secur."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s12230-018-09696-2","article-title":"Potato Starch: A Review of Physicochemical, Functional and Nutritional Properties","volume":"96","author":"Dupuis","year":"2019","journal-title":"Am. J. Potato Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1651","DOI":"10.1093\/pcp\/pcp108","article-title":"Enhancing Sucrose Synthase Activity in Transgenic Potato (Solanum tuberosum L.) Tubers Results in Increased Levels of Starch, ADPglucose and UDPglucose and Total Yield","volume":"50","author":"Montero","year":"2009","journal-title":"Plant Cell Physiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s11540-019-09434-z","article-title":"Stability Analysis of Tuber Yield and Starch Yield in Mid-Late and Late Maturing Starch Cultivars of Potato (Solanum tuberosum)","volume":"63","author":"Lenartowicz","year":"2020","journal-title":"Potato Res."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Shirani-Bidabadi, M., Nazarian-Firouzabadi, F., Sorkheh, K., and Ismaili, A. (2024). Transcriptomic analysis of potato (Solanum tuberosum L.) tuber development reveals new insights into starch biosynthesis. PLoS ONE, 19.","DOI":"10.1371\/journal.pone.0297334"},{"key":"ref_7","first-page":"57","article-title":"SnRK1 and trehalose 6-phosphate\u2014Two ancient pathways converge to regulate plant metabolism and growth","volume":"55","author":"Lunn","year":"2020","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1111\/j.1365-3040.2004.01183.x","article-title":"Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers","volume":"27","author":"Geigenberger","year":"2004","journal-title":"Plant Cell Environ."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2086","DOI":"10.1073\/pnas.0305920101","article-title":"Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers","volume":"101","author":"Bustos","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1002\/j.1460-2075.1992.tb05167.x","article-title":"Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes","volume":"11","author":"Sonnewald","year":"1992","journal-title":"EMBO J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2781","DOI":"10.1007\/s00018-016-2250-x","article-title":"Formation of starch in plant cells","volume":"73","author":"Pfister","year":"2016","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2535","DOI":"10.1105\/tpc.19.00946","article-title":"STARCH SYNTHASE5, a Noncanonical Starch Synthase-Like Protein, Promotes Starch Granule Initiation in Arabidopsis","volume":"32","author":"Abt","year":"2020","journal-title":"Plant Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1038\/nbt0897-794","article-title":"Increased potato tuber size resulting from apoplastic expression of a yeast invertase","volume":"15","author":"Sonnewald","year":"1997","journal-title":"Nat. Biotechnol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"kiaf287","DOI":"10.1093\/plphys\/kiaf287","article-title":"Dual knockout of 2 starch synthase-related genes drives sugar reprogramming via metabolic rewiring in barley","volume":"189","author":"Jiang","year":"2025","journal-title":"Plant Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3645","DOI":"10.1111\/pbi.70338","article-title":"Dual-Layer Transcriptional-Protein Regulation by HvAP2-12 Represses HvAP2-18 Activity to Fine-Tune Barley Starch Synthesis","volume":"23","author":"Ding","year":"2025","journal-title":"Plant Biotechnol. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"124167","DOI":"10.1016\/j.carbpol.2025.124167","article-title":"Ethylene-responsive factor HvERF72 regulates starch synthesis and B-type starch granules initiation in barley","volume":"424","author":"Zhou","year":"2025","journal-title":"Carbohydr. Polym."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Ding, J.J., Karim, H., Li, Y.L., Harwood, W., Guzm\u00e1n, C., Lin, N., Xu, Q., Zhang, Y., Tang, H., and Jiang, Y. (2021). Re-examination of the APETALA2\/Ethylene-Responsive Factor Gene Family in Barley (Hordeum vulgare L.) Indicates a Role in the Regulation of Starch Synthesis. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.791584"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lebot, V. (2020). Sweet Potato: Developmental Physiology. Tropical Root and Tuber Crops: Cassava, Sweet Potato, Yams and Aroids, CABI.","DOI":"10.1079\/9781789243369.0000"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/BF02852767","article-title":"Parenchyma cell growth in potato tubers II. Cell divisions vs. cell enlargement","volume":"50","author":"Reeve","year":"1973","journal-title":"Am. Potato J."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Li, S.X., Shi, Z.G., Zhu, Q.R., Tao, L., Liang, W., and Zhao, Z. (2021). Transcriptome sequencing and differential expression analysis of seed starch accumulation in Chinese chestnut Metaxenia. BMC Genom., 22.","DOI":"10.1186\/s12864-021-07923-5"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1093\/jxb\/ers396","article-title":"Metabolic Profiling Reveals Coordinated Switches in Primary Carbohydrate Metabolism in Grape Berry (Vitis vinifera L.), a Non-Climacteric Fleshy Fruit","volume":"64","author":"Dai","year":"2013","journal-title":"J. Exp. Bot."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"20364","DOI":"10.1021\/acs.jafc.5c14718","article-title":"AP2\/ERF Transcription Factors StRAP2.7a\/b Modulate trans-Zeatin Biosynthesis and StSP6A Expression to Facilitate Stolon and Tuber Formation in Potato","volume":"74","author":"Zhang","year":"2026","journal-title":"J. Agric. Food Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"8401","DOI":"10.1038\/s41467-026-75179-2","article-title":"The OsMYB4 Transcription Factor Enables Coordinated Improvement of Grain Yield and Quality in Rice","volume":"17","author":"Xu","year":"2026","journal-title":"Nat. Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/s41467-025-67200-x","article-title":"The bHLH transcription factor PIL1 orchestrates starch synthesis in key cereal crops","volume":"17","author":"Meng","year":"2026","journal-title":"Nat. Commun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e70848","DOI":"10.1111\/ppl.70848","article-title":"Eggplant AP2\/ERF transcription factor SmWIN1 promotes wax biosynthesis by activating the expression of SmKCS6 and SmLACS2","volume":"178","author":"Li","year":"2026","journal-title":"Physiol. Plant."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.1111\/nph.19426","article-title":"The tuber-specific StbHLH93 gene regulates proplastid-to-amyloplast development during stolon swelling in potato","volume":"241","author":"Yang","year":"2024","journal-title":"New Phytol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1007\/BF02853443","article-title":"Partitioning of photoassimilates by potato plants (Solanum tuberosum L.) as influenced by irradiance I. Partitioning patterns in cultivar Russet Burbank grown under high and low irradiance","volume":"66","author":"Gawronska","year":"1989","journal-title":"Am. Potato J."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4420","DOI":"10.1002\/fsn3.2415","article-title":"Study on starch content detection and visualization of potato based on hyperspectral imaging","volume":"9","author":"Wang","year":"2021","journal-title":"Food Sci. Nutr."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"153685","DOI":"10.1016\/j.jplph.2022.153685","article-title":"Adjustments of carbon allocation and stomatal dynamics by target localized strategies to increase crop productivity under changing climates","volume":"272","author":"Drincovich","year":"2022","journal-title":"J. Plant Physiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1104\/pp.111.179903","article-title":"Altering Trehalose-6-Phosphate Content in Transgenic Potato Tubers Affects Tuber Growth and Alters Responsiveness to Hormones during Sprouting","volume":"156","author":"Debast","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1111\/pbi.13367","article-title":"Non-GMO potato lines, synthesizing increased amylose and resistant starch, are mainly deficient in isoamylase debranching enzyme","volume":"18","author":"Blennow","year":"2020","journal-title":"Plant Biotechnol. J."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Deng, K., Bao, Y.T., Xu, M.H., Lv, C., Zhao, L., Wang, J., and Wang, F. (2025). GWAS-Based Prediction of Genes Regulating Trehalose and Sucrose in Potato Tubers. Horticulturae, 11.","DOI":"10.3390\/horticulturae11091033"}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/18\/1655\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T10:04:50Z","timestamp":1789985090000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/15\/18\/1655"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,18]]},"references-count":32,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["biology15181655"],"URL":"https:\/\/doi.org\/10.3390\/biology15181655","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,18]]}}}