{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,20]],"date-time":"2026-04-20T13:55:34Z","timestamp":1776693334015,"version":"3.51.2"},"reference-count":45,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T00:00:00Z","timestamp":1763942400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100009329","name":"Scientific Research and Technology Development Program of Guangxi Zhuang Autonomous Region","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009329","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>\n                    Maize kernel hardness, largely determined by the structural and compositional characteristics of the endosperm, is a key trait affecting grain quality, milling performance, and storage stability. Although vitreous and starchy endosperms exhibit markedly different physical properties, the underlying metabolic and transcriptional mechanisms\u2014particularly the crosstalk between primary and specialized metabolic pathways\u2014remain insufficiently understood. In this study, we conducted integrated metabolomic and transcriptomic analyses, along with cytological observations, to investigate these mechanisms using two contrasting maize inbred lines (D003, vitreous; D009, starchy) at three kernel developmental stages (18, 25, and 32 days after pollination, DAP). Cytological examination revealed that D003 endosperms comprise smaller, tightly packed cells containing polygonal starch granules, whereas D009 endosperms consist of larger, irregular cells with loosely arranged spherical starch granules. Metabolomic profiling revealed significantly higher levels of carotenoids\u2014including carotenes (\u03b1-carotene, \u03b2-carotene) and xanthophylls (zeaxanthin, lutein)\u2014in D003 kernels across all stages, implicating carotenoid biosynthesis in contributing to kernel hardness. Transcriptomic analysis identified starch and sucrose metabolism as the most significantly enriched pathway among differentially expressed genes (DEGs), with qRT-PCR validation confirming the downregulation of a key sucrose synthase gene (\n                    <jats:italic>Zm00001eb313170<\/jats:italic>\n                    ). We propose a synergistic model in which transcriptional regulation of starch and sucrose metabolism\u2014particularly reduced sucrose synthase activity\u2014promotes the formation of a compact endosperm structure characterized by polygonal starch granules, while enhanced carotenoid accumulation reinforces cellular interfaces, collectively enhancing kernel hardness. These findings offer novel molecular targets for breeding strategies aimed at improving maize kernel quality.\n                  <\/jats:p>","DOI":"10.3389\/fpls.2025.1688375","type":"journal-article","created":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T06:29:39Z","timestamp":1763965779000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":2,"title":["Integrated metabolomic and transcriptomic analyses reveal that starch and sucrose metabolism regulate maize kernel hardness"],"prefix":"10.3389","volume":"16","author":[{"given":"Haiyu","family":"Zhou","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaodong","family":"Xie","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hexia","family":"Xie","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lanqiu","family":"Qin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuxin","family":"Xie","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiang","family":"Yang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bujin","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jingdan","family":"He","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bingwei","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chengqiao","family":"Shi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juzhi","family":"Lv","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xianjie","family":"Tan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinguo","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Weidong","family":"Cheng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yufeng","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2025,11,24]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.1105\/tpc.7.7.1027","article-title":"Plant carotenoids: pigments for photoprotection, visual attraction, and human health","volume":"7","author":"Bartley","year":"1995","journal-title":"Plant Cell."},{"key":"B2","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1016\/j.jcs.2019.04.019","article-title":"Role of yield genetic progress on the biochemical determinants of maize kernel hardness","volume":"87","author":"Caballero-Rothar","year":"2019","journal-title":"J. Cereal Science."},{"key":"B3","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1023\/a:1014457901992","article-title":"Gene expression studies on developing kernels of maize sucrose synthase (susy) mutants show evidence for a third susy gene","volume":"49","author":"Carlson","year":"2002","journal-title":"Plant Mol. Biol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"2003","DOI":"10.1105\/tpc.8.11.2003","article-title":"Ef-1[alpha] is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells","volume":"8","author":"Clore","year":"1996","journal-title":"Plant Cell."},{"key":"B5","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1111\/jipb.13069","article-title":"Maize endosperm development","volume":"63","author":"Dai","year":"2021","journal-title":"J. Integr. Plant Biol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1897","DOI":"10.1111\/pbi.13349","article-title":"Transactivation of sus1 and sus2 by opaque2 is an essential supplement to sucrose synthase-mediated endosperm filling in maize","volume":"18","author":"Deng","year":"2020","journal-title":"Plant Biotechnol. J."},{"key":"B7","doi-asserted-by":"publisher","first-page":"818","DOI":"10.2135\/cropsci2003.8180","article-title":"Combining ability of maize inbreds for carotenoids and tocopherols","volume":"43","author":"Egesel","year":"2003","journal-title":"Crop Science."},{"key":"B8","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.abb.2018.06.001","article-title":"Carotenoids in human nutrition and health","volume":"652","author":"Eggersdorfer","year":"2018","journal-title":"Arch. Biochem. Biophys."},{"key":"B9","doi-asserted-by":"publisher","first-page":"5647","DOI":"10.1021\/jf900623w","article-title":"Hardness methods for testing maize kernels","volume":"57","author":"Fox","year":"2009","journal-title":"J. Agric. Food. Chem."},{"key":"B10","doi-asserted-by":"publisher","first-page":"760","DOI":"10.1007\/s12155-017-9837-4","article-title":"Maize kernel hardness, endosperm zein profiles, and ethanol production","volume":"10","author":"Gerde","year":"2017","journal-title":"Bioenerg. Res."},{"key":"B11","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1016\/j.tig.2005.02.009","article-title":"Molecular genetic approaches to developing quality protein maize","volume":"21","author":"Gibbon","year":"2005","journal-title":"Trends Genet."},{"key":"B12","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1111\/j.1365-3040.2005.01492.x","article-title":"Carotenoid accumulation and function in seeds and non-green tissues","volume":"29","author":"Howitt","year":"2006","journal-title":"Plant Cell Environ."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1016\/j.xplc.2021.100237","article-title":"Starch biosynthesis in cereal endosperms: an updated review over the last decade","volume":"2","author":"Huang","year":"2021","journal-title":"Plant Commun."},{"key":"B14","doi-asserted-by":"publisher","first-page":"812","DOI":"10.1016\/j.jpba.2008.04.001","article-title":"Determination of carotenoids and their esters in fruits of lycium barbarum linnaeus by hplc-dad-apci-ms","volume":"47","author":"Inbaraj","year":"2008","journal-title":"J. Pharm. Biomed. Anal."},{"key":"B15","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1016\/j.plaphy.2010.03.006","article-title":"Starch biosynthesis in cereal endosperm","volume":"48","author":"Jeon","year":"2010","journal-title":"Plant Physiol. Biochem."},{"key":"B16","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.jcs.2013.12.004","article-title":"Reflectance colorimetry as a simple method for estimating carotenoid content in maize grain","volume":"59","author":"Kljak","year":"2014","journal-title":"J. Cereal Science."},{"key":"B17","doi-asserted-by":"publisher","first-page":"412","DOI":"10.1016\/j.plaphy.2016.08.001","article-title":"Carotenoid profiling, in silico analysis and transcript profiling of mirnas targeting carotenoid biosynthetic pathway genes in different developmental tissues of tomato","volume":"108","author":"Koul","year":"2016","journal-title":"Plant Physiol. Biochem."},{"key":"B18","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1093\/pcp\/pcs180","article-title":"Enhancing sucrose synthase activity results in increased levels of starch and adp-glucose in maize (zea mays l.) Seed endosperms","volume":"54","author":"Li","year":"2013","journal-title":"Plant Cell Physiol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"581","DOI":"10.1007\/s11248-007-9111-1","article-title":"Metabolic engineering of carotenoid accumulation by creating a metabolic sink","volume":"16","author":"Li","year":"2007","journal-title":"Transgenic Res."},{"key":"B20","doi-asserted-by":"publisher","first-page":"385","DOI":"10.1016\/j.ifset.2007.03.015","article-title":"Physical properties and carotenoid content of maize kernels and its nixtamalized snacks","volume":"8","author":"Lozano-Alejo","year":"2007","journal-title":"Innovative Food Sci. Emerging Technologies."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1203284","article-title":"Integrative transcriptome and metabolome analysis reveals the mechanisms of light-induced pigmentation in purple waxy maize","volume":"14","author":"Lu","year":"2023","journal-title":"Front. Plant Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"e1801045","DOI":"10.1002\/mnfr.201801045","article-title":"An overview of carotenoids, apocarotenoids, and vitamin a in agro-food, nutrition, health, and disease","volume":"63","author":"Melendez-Martinez","year":"2019","journal-title":"Mol. Nutr. Food Res."},{"key":"B23","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1016\/j.foodchem.2013.01.014","article-title":"Distribution of carotenoids in endosperm, germ, and aleurone fractions of cereal grain kernels","volume":"139","author":"Ndolo","year":"2013","journal-title":"Food Chem."},{"key":"B24","doi-asserted-by":"publisher","first-page":"10862","DOI":"10.1021\/acs.jafc.3c09309","article-title":"Integrated transcriptomic and metabolomic analysis reveal the dynamic process of bama hemp seed development and the accumulation mechanism of alpha-linolenic acid and linoleic acid","volume":"72","author":"Nie","year":"2024","journal-title":"J. Agric. Food. Chem."},{"key":"B25","doi-asserted-by":"publisher","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":"B26","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1111\/nyas.12396","article-title":"Global maize production, utilization, and consumption","volume":"1312","author":"Ranum","year":"2014","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1016\/j.jcs.2019.102901","article-title":"Maize kernel color depends on the interaction between hardness and carotenoid concentration","volume":"91","author":"Saenz","year":"2020","journal-title":"J. Cereal Science."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.jcs.2021.103206","article-title":"Carotenoid profiles in maize genotypes with contrasting kernel hardness","volume":"99","author":"Saenz","year":"2021","journal-title":"J. Cereal Science."},{"key":"B29","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1111\/j.1365-313X.2011.04527.x","article-title":"Genome-wide atlas of transcription during maize development","volume":"66","author":"Sekhon","year":"2011","journal-title":"Plant J."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.1111\/nph.20196","article-title":"Carotenoid-carbohydrate crosstalk: evidence for genetic and physiological interactions in storage tissues across crop species","volume":"244","author":"Villwock","year":"2024","journal-title":"New Phytol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"2565","DOI":"10.1038\/s41467-024-46955-9","article-title":"An arf gene mutation creates flint kernel architecture in dent maize","volume":"15","author":"Wang","year":"2024","journal-title":"Nat. Commun."},{"key":"B32","doi-asserted-by":"publisher","first-page":"5346","DOI":"10.1038\/s41467-020-19196-9","article-title":"Carotenoids modulate kernel texture in maize by influencing amyloplast envelope integrity","volume":"11","author":"Wang","year":"2020","journal-title":"Nat. Commun."},{"key":"B33","doi-asserted-by":"publisher","first-page":"3447","DOI":"10.1105\/tpc.112.101360","article-title":"Opaque1 encodes a myosin xi motor protein that is required for endoplasmic reticulum motility and protein body formation in maize endosperm","volume":"24","author":"Wang","year":"2012","journal-title":"Plant Cell."},{"key":"B34","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/j.tplants.2019.12.021","article-title":"Prospects for carotenoid biofortification targeting retention and catabolism","volume":"25","author":"Watkins","year":"2020","journal-title":"Trends Plant Sci."},{"key":"B35","doi-asserted-by":"publisher","first-page":"2857S","DOI":"10.1093\/jn\/132.9.2857S","article-title":"Extent of vitamin a deficiency among preschool children and women of reproductive age","volume":"132","author":"West","year":"2002","journal-title":"J. Nutr."},{"key":"B36","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1093\/plphys\/kiae327","article-title":"Transcriptome and metabolome atlas reveals contributions of sphingosine and chlorogenic acid to cold tolerance in citrus","volume":"196","author":"Xiao","year":"2024","journal-title":"Plant Physiol."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1007\/s00122-024-04786-8","article-title":"A beta-ketoacyl-coa synthase encoded by ddp1 controls rice anther dehiscence and pollen fertility by maintaining lipid homeostasis in the tapetum","volume":"138","author":"Xu","year":"2024","journal-title":"Theor. Appl. Genet."},{"key":"B38","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1093\/plcell\/koaa008","article-title":"The b3 domain-containing transcription factor zmabi19 coordinates expression of key factors required for maize seed development and grain filling","volume":"33","author":"Yang","year":"2021","journal-title":"Plant Cell."},{"key":"B39","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1016\/j.molp.2024.04.004","article-title":"Sucrose-associated snrk1a1-mediated phosphorylation of opaque2 modulates endosperm filling in maize","volume":"17","author":"Yang","year":"2024","journal-title":"Mol. Plant"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1016\/j.jgg.2025.05.001","article-title":"Enhancing quality traits in staple crops: current advances and future perspectives","author":"Yang","year":"2025","journal-title":"J. Genet. Genomics"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1093\/plcell\/koac044","article-title":"Aba-induced phosphorylation of basic leucine zipper 29, abscisic acid insensitive 19, and opaque2 by snrk2.2 enhances gene transactivation for endosperm filling in maize","volume":"34","author":"Yang","year":"2022","journal-title":"Plant Cell."},{"key":"B42","doi-asserted-by":"publisher","first-page":"2312","DOI":"10.1111\/pbi.14346","article-title":"Linkage and association mapping in multi-parental populations reveal the genetic basis of carotenoid variation in maize kernels","volume":"22","author":"Yin","year":"2024","journal-title":"Plant Biotechnol. J."},{"key":"B43","doi-asserted-by":"publisher","first-page":"3198","DOI":"10.1111\/pce.14936","article-title":"Integrated physiological, transcriptomic and metabolomic analyses reveal the mechanism of peanut kernel weight reduction under waterlogging stress","volume":"47","author":"Zeng","year":"2024","journal-title":"Plant Cell Environ."},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1016\/j.plaphy.2025.109897","article-title":"Effects of blue and red led treatments on carotenoid and soluble sugar metabolism in postharvest nectarine fruit and their correlation","volume":"224","author":"Zhang","year":"2025","journal-title":"Plant Physiol. Biochem."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1016\/j.eja.2024.127325","article-title":"Developing a Deep Learning network \u201cMSCP-Net\u201d to generate stalk anatomical traits related with crop lodging and yield in maize","volume":"160","author":"Zhou","year":"2024","journal-title":"Eur. J. Agronomy."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2025.1688375\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T06:29:40Z","timestamp":1763965780000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2025.1688375\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,24]]},"references-count":45,"alternative-id":["10.3389\/fpls.2025.1688375"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2025.1688375","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,24]]},"article-number":"1688375"}}