[en] [en] INTRODUCTION: Commercial spring maize germplasm in northern China has been shaped by five decades of intensive breeding and the continual incorporation of elite domestic and introduced germplasm, but its genetic diversity, pedigree structure, and genomic signatures of selection remain incompletely characterized.
METHODS: We re-sequenced 108 representative inbred lines from China's commercial spring maize germplasm and combined them with 14 previously published key inbred lines. Population structure, genetic diversity, identity-by-descent, selective sweeps, and haplotype-trait associations were analyzed across seven heterotic groups.
RESULTS: The 122 inbred lines represented nearly five decades of elite maize germplasm in northern China. Modern breeding materials showed reduced nucleotide diversity, with π decreasing from 1.58 × 10-3 to 1.34 × 10-3, and an increased deleterious mutation burden. We identified 275 Mb of high-impact IBD regions shared among elite germplasm, containing genes associated with flowering, plant architecture, photosynthesis, and grain quality. Selective sweep analyses detected genomic regions associated with agronomic traits including grain quality and floral organ development. Haplotype analyses further revealed natural alleles related to tassel structure, with differential allele frequencies between the SS and TSPT heterotic groups.
DISCUSSION: These findings provide a genomic resource for northern Chinese commercial maize germplasm and support future heterotic group optimization, marker-assisted breeding, and genomic selection.
Disciplines :
Agriculture & agronomy
Author, co-author :
Song, Yuhan ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Nong, Hongsen; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China ; College of Agriculture, South China Agricultural University, Guangzhou, Guandong, China
Liao, Zhenyang; Spice and Beverage Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wanning, Hainan, China
Wang, Yanyan; College of Agriculture, South China Agricultural University, Guangzhou, Guandong, China
Yu, Hongying; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Du, Guohua; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Chang, Yuxiao; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Tan, Cong; State Key Laboratory of Agricultural Genomics, Key Laboratory of Genomics, Ministry of Agriculture, BGI Research, Shenzhen, China
Zhang, Xingtan; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Lu, Hong; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China
Language :
English
Title :
Genetic characterization of commercial spring maize germplasm in Northern China for hybrid breeding and trait improvement.
The author(s) declared that financial support was received for this work and/or its publication. This study was supported by the Shenzhen Science and Technology Program (KQTD20230301092839007) and the Shenzhen Science and Technology Key Project (KJZD20230923114103007).
Alleman M., Sidorenko L., McGinnis K., Seshadri V., Dorweiler J. E., White J., et al. (2006). An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295–298. doi: 10.1038/nature04884, 16855589.
Anzala F., Morere-Le Paven M.-C., Fournier S., Rondeau D., Limami A. M., (2006). Physiological and molecular aspects of aspartate-derived amino acid metabolism during germination and post-germination growth in two maize genotypes differing in germination efficiency. J. Exp. Bot. 57, 645–653. doi: 10.1093/jxb/erj054, 16415333.
Bairoch A., Apweiler R., (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28, 45–48. doi: 10.1093/nar/28.1.45, 10592178.
Bastian M., Heymann S., Jacomy M., (2009). “ Gephi: an open source software for exploring and manipulating networks”, in: Proceedings ofthe international AAAI conference on web and social media (Menlo Park, CA: AAAI Press), 361–362. doi: 10.1609/icwsm.v3i1.13937.
Becraft P. W., Stinard P. S., McCarty D. R., (1996). CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273, 1406–1409. doi: 10.1126/science.273.5280.1406, 8703079.
Bomblies K., Wang R.-L., Ambrose B. A., Schmidt R. J., Meeley R. B., Doebley J., (2003). Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130, 2385–2395. doi: 10.1242/dev.00457.
Browning B. L., Browning S. R., (2013). Detecting identity by descent and estimating genotype error rates in sequence data. Am. J. Hum. Genet. 93, 840–851. doi: 10.1016/j.ajhg.2013.09.014, 24207118.
Browning B. L., Zhou Y., Browning S. R., (2018). A one-penny imputed genome from next-generation reference panels. Am. J. Hum. Genet. 103, 338–348. doi: 10.1016/j.ajhg.2018.07.015, 30100085.
Brutnell T. P., Sawers R. J., Mant A., Langdale J. A., (1999). BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11, 849–864. doi: 10.2307/3870819.
Bu D., Luo H., Huo P., Wang Z., Zhang S., He Z., et al. (2021). KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res. 49, W317–W325. doi: 10.1093/nar/gkab447, 34086934.
Cantalapiedra C. P., Hernández-Plaza A., Letunic I., Bork P., Huerta-Cepas J., (2021). eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829. doi: 10.1093/molbev/msab293, 34597405.
Chen H., Patterson N., Reich D., (2010). Population differentiation as a test for selective sweeps. Genome Res. 20, 393–402. doi: 10.1101/gr.100545.109, 20086244.
Chen L., Luo J., Jin M., Yang N., Liu X., Peng Y., et al. (2022). Genome sequencing reveals evidence of adaptive variation in the genus Zea. Nat. Genet. 54, 1736–1745. doi: 10.1038/s41588-022-01184-y, 36266506.
Colasanti J., Yuan Z., Sundaresan V., (1998). The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell. 93, 593–603. doi: 10.1016/s0092-8674(00)81188-5, 9604934.
Consortium (2004). The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32, D258–D261. doi: 10.1093/nar/gkh036, 14681407.
Cui X., Wise R. P., Schnable P. S., (1996). The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272, 1334–1336. doi: 10.1126/science.272.5266.1334, 8650543.
Damkjær J. T., Kereïche S., Johnson M. P., Kovacs L., Kiss A. Z., Boekema E. J., et al. (2009). The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis. Plant Cell 21, 3245–3256. doi: 10.1105/tpc.108.064006.
Danecek P., Auton A., Abecasis G., Albers C. A., Banks E., DePristo M. A., et al. (2011). The variant call format and VCFtools. Bioinformatics 27, 2156–2158. doi: 10.1093/bioinformatics/btr330, 21653522.
Danecek P., Bonfield J. K., Liddle J., Marshall J., Ohan V., Pollard M. O., et al. (2021). Twelve years of SAMtools and BCFtools. GigaScience 10, giab008. doi: 10.1093/gigascience/giab008, 33590861.
FAO. Food and Agriculture Organization of the United Nations (2024). Faostat Statistical Database. Available online at: https://www.fao.org/faostat/en/#home (Accessed June 29, 2026.).
Feng J.-W., Han L., Liu H., Xie W.-Z., Liu H., Li L., et al. (2023). MaizeNetome: A multi-omics network database for functional genomics in maize. Mol. Plant 16, 1229–1231. doi: 10.1016/j.molp.2023.08.002, 37553832.
Fu Z., Chai Y., Zhou Y., Yang X., Warburton M. L., Xu S., et al. (2013). Natural variation in the sequence of PSY1 and frequency of favorable polymorphisms among tropical and temperate maize germplasm. Theor. Appl. Genet. 126, 923–935. doi: 10.1007/s00122-012-2026-0, 23238762.
Gao M., Wanat J., Stinard P. S., James M. G., Myers A. M., (1998). Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10, 399–412. doi: 10.2307/3870597.
Hallauer A. R., Carena M. J., (2009). “ Maize, ” in Cereals, vol. 3 . Ed. Carena M., ( Springer, New York, NY).
Hao Z., Lv D., Ge Y., Shi J., Weijers D., Yu G., et al. (2020). RIdeogram: drawing SVG graphics to visualize and map genome-wide data on the idiograms. PeerJ Comput. Sci. 6, e251. doi: 10.32614/cran.package.rideogram.
Harjes C. E., Rocheford T. R., Bai L., Brutnell T. P., Kandianis C. B., Sowinski S. G., et al. (2008). Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319, 330–333. doi: 10.1126/science.1150255.
Huang M., Slewinski T. L., Baker R. F., Janick-Buckner D., Buckner B., Johal G. S., et al. (2009). Camouflage patterning in maize leaves results from a defect in porphobilinogen deaminase. Mol. Plant 2, 773–789. doi: 10.1093/mp/ssp029, 19825655.
Huang X., Huang S., Han B., Li J., (2022a). The integrated genomics of crop domestication and breeding. Cell. 185, 2828–2839. doi: 10.1016/j.cell.2022.04.036, 35643084.
Huang Y., Wang H., Zhu Y., Huang X., Li S., Wu X., et al. (2022b). THP9 enhances seed protein content and nitrogen-use efficiency in maize. Nature 612, 292–300. doi: 10.1038/s41586-022-05441-2, 36385527.
Hufford M. B., Xu X., Van Heerwaarden J., Pyhäjärvi T., Chia J.-M., Cartwright R. A., et al. (2012). Comparative population genomics of maize domestication and improvement. Nat. Genet. 44, 808–811. doi: 10.1038/ng.2309, 22660546.
James M. G., Robertson D. S., Myers A. M., (1995). Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7, 417–429. doi: 10.2307/3870080.
Juarez M. T., Kui J. S., Thomas J., Heller B. A., Timmermans M. C., (2004a). microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88. doi: 10.1038/nature02363, 14999285.
Juarez M. T., Twigg R. W., Timmermans M. C., (2004b). Specification of adaxial cell fate during maize leaf development. doi: 10.1242/dev.01328.
Kanehisa M., Furumichi M., Tanabe M., Sato Y., Morishima K., (2017). KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45, D353–D361. doi: 10.1093/nar/gkw1092, 27899662.
Keith C. S., Hoang D. O., Barrett B. M., Feigelman B., Nelson M. C., Thai H., et al. (1993). Partial sequence analysis of 130 randomly selected maize cDNA clones. Plant Physiol. 101, 329–332. doi: 10.1104/pp.101.1.329, 8278499.
Knight M. E., Harn C., Lilley C. E., Guan H., Singletary G. W., Mu‐Forster C., et al. (1998). Molecular cloning of starch synthase I from maize (W64) endosperm and expression in Escherichia coli. Plant J. 14, 613–622. doi: 10.1046/j.1365-313x.1998.00150.x, 9675904.
Letunic I., Bork P., (2024). Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Res. 52, W78–W82. doi: 10.1093/nar/gkae268, 38613393.
Li C., Guan H., Jing X., Li Y., Wang B., Li Y., et al. (2022). Genomic insights into historical improvement of heterotic groups during modern hybrid maize breeding. Nat. Plants 8, 750–763. doi: 10.1038/s41477-022-01190-2, 35851624.
Liu J., Fernie A. R., Yan J., (2020). The past, present, and future of maize improvement: domestication, genomics, and functional genomic routes toward crop enhancement. Plant Commun. 1, 100010. doi: 10.1016/j.xplc.2019.100010, 33404535.
Mace E. S., Tai S., Gilding E. K., Li Y., Prentis P. J., Bian L., et al. (2013). Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat. Commun. 4, 2320. doi: 10.1038/ncomms3320, 23982223.
Martin A., Lee J., Kichey T., Gerentes D., Zivy M., Tatout C., et al. (2006). Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18, 3252–3274. doi: 10.1105/tpc.106.042689, 17138698.
Minh B. Q., Schmidt H. A., Chernomor O., Schrempf D., Woodhams M. D., Von Haeseler A., et al. (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534. doi: 10.1093/molbev/msaa015, 32011700.
Moreno M. A., Harper L. C., Krueger R. W., Dellaporta S. L., Freeling M., (1997). liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev. 11, 616–628. doi: 10.1101/gad.11.5.616, 9119226.
Okonechnikov K., Conesa A., García-Alcalde F., (2016). Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32, 292–294. doi: 10.1093/bioinformatics/btv566, 26428292.
Pont C., Leroy T., Seidel M., Tondelli A., Duchemin W., Armisen D., et al. (2019). Tracing the ancestry of modern bread wheats. Nat. Genet. 51, 905–911. doi: 10.1038/s41588-019-0393-z, 31043760.
Pruitt K. D., Tatusova T., Maglott D. R., (2007). NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35, D61–D65. doi: 10.1093/nar/gkl842, 17130148.
Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M. A., Bender D., et al. (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575. doi: 10.1086/519795, 17701901.
Quinlan A. R., Hall I. M., (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842. doi: 10.1093/bioinformatics/btq033, 20110278.
Raj A., Stephens M., Pritchard J. K., (2014). fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197, 573–589. doi: 10.1534/genetics.114.164350, 24700103.
Sakakibara H., Kawabata S., Hase T., Sugiyama T., (1992). Differential effects of nitrate and light on the expression of glutamine synthetases and ferredoxin-dependent glutamate synthase in maize. Plant Cell Physiol. 33, 1193–1198.
Schneeberger R., Tsiantis M., Freeling M., Langdale J. A., (1998). The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125, 2857–2865. doi: 10.1242/dev.125.15.2857, 9655808.
Shen W., Le S., Li Y., Hu F., (2016). SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PloS One 11, e0163962. doi: 10.1371/journal.pone.0163962, 27706213.
Shiferaw B., Prasanna B. M., Hellin J., Bänziger M., (2011). Crops that feed the world 6. Past successes and future challenges to the role played by maize in global food security. Food Secur. 3, 307–327. doi: 10.1007/s12571-011-0140-5, 30311153.
Singh M., Lewis P. E., Hardeman K., Bai L., Rose J. K., Mazourek M., et al. (2003). Activator mutagenesis of the pink scutellum1/viviparous7 locus of maize. Plant Cell 15, 874–884. doi: 10.1201/9781003245230.
Sosso D., Luo D., Li Q.-B., Sasse J., Yang J., Gendrot G., et al. (2015). Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat. Genet. 47, 1489–1493. doi: 10.1038/ng.3422, 26523777.
Sun Y., Dong L., Kang L., Zhong W., Jackson D., Yang F., (2024). Progressive meristem and single-cell transcriptomes reveal the regulatory mechanisms underlying maize inflorescence development and sex differentiation. Mol. Plant 17, 1019–1037. doi: 10.1016/j.molp.2024.06.007, 38877701.
Taguchi-Shiobara F., Yuan Z., Hake S., Jackson D., (2001). The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15, 2755–2766. doi: 10.1101/gad.208501, 11641280.
Tatusov R. L., Fedorova N. D., Jackson J. D., Jacobs A. R., Kiryutin B., Koonin E. V., et al. (2003). The COG database: an updated version includes eukaryotes. BMC Bioinf. 4, 41. doi: 10.1186/1471-2105-4-41, 12969510.
Tian F., Bradbury P. J., Brown P. J., Hung H., Sun Q., Flint-Garcia S., et al. (2011). Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat. Genet. 43, 159–162. doi: 10.1038/ng.746, 21217756.
Timmermans M. C., Schultes N. P., Jankovsky J. P., Nelson T., (1998). Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125, 2813–2823. doi: 10.1242/dev.125.15.2813, 9655804.
Uribelarrea M., Cárcova J., Otegui M., Westgate M., (2002). Pollen production, pollination dynamics, and kernel set in maize. Crop Sci. 42, 1910–1918. doi: 10.2135/cropsci2002.1910.
Veit B., Briggs S. P., Schmidt R. J., Yanofsky M. F., Hake S., (1998). Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature 393, 166–168. doi: 10.1038/30239, 9603518.
Vicente-Carbajosa J., Moose S. P., Parsons R. L., Schmidt R. J., (1997). A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc. Natl. Acad. Sci. 94, 7685–7690. doi: 10.1073/pnas.94.14.7685, 9207153.
Wagner R., Von Sydow L., Aigner H., Netotea S., Brugière S., Sjögren L., et al. (2016). Deletion of FtsH11 protease has impact on chloroplast structure and function in Arabidopsis thaliana when grown under continuous light. Plant Cell Environ. 39, 2530–2544. doi: 10.1111/pce.12808, 27479913.
Wallace J. G., Rodgers-Melnick E., Buckler E. S., (2018). On the road to breeding 4.0: unraveling the good, the bad, and the boring of crop quantitative genomics. Annu. Rev. Genet. 52, 421–444. doi: 10.1146/annurev-genet-120116-024846, 30285496.
Wang J., Eulgem T., (2023). The Arabidopsis RRM domain proteins EDM3 and IBM2 coordinate the floral transition and basal immune responses. Plant J. 116, 128–143. doi: 10.1111/tpj.16364, 37347678.
Wang K., Li M., Hakonarson H., (2010). ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164-e164. doi: 10.1093/nar/gkq603, 20601685.
Wang J., Li X., Wang Y., Lin J., Chen S., Liu H., et al. (2026). Genetic architecture of sugarcane traits in a polyploid genomics framework. Nature 654, 994–1003. doi: 10.1038/s41586-026-10576-7, 42203877.
Wang B., Lin Z., Li X., Zhao Y., Zhao B., Wu G., et al. (2020). Genome-wide selection and genetic improvement during modern maize breeding. Nat. Genet. 52, 565–571. doi: 10.1038/s41588-020-0616-3, 32341525.
Wang H., Nussbaum-Wagler T., Li B., Zhao Q., Vigouroux Y., Faller M., et al. (2005). The origin of the naked grains of maize. Nature 436, 714–719. doi: 10.1038/nature03863, 16079849.
Woo Y.-M., Hu D.-N., Larkins B. A., Jung R., (2001). Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13, 2297–2317. doi: 10.1105/tpc.13.10.2297, 37910205.
Wright A. D., Moehlenkamp C. A., Perrot G. H., Neuffer M. G., Cone K. C., (1992). The maize auxotrophic mutant orange pericarp is defective in duplicate genes for tryptophan synthase beta. Plant Cell 4, 711–719. doi: 10.1086/279436, 24690653.
Xiao Y., Jiang S., Cheng Q., Wang X., Yan J., Zhang R., et al. (2021). The genetic mechanism of heterosis utilization in maize improvement. Genome Biol. 22, 148. doi: 10.1186/s13059-021-02370-7, 33971930.
Yanagisawa S., (2000). Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J. 21, 281–288. doi: 10.1046/j.1365-313x.2000.00685.x, 10758479.
Yang Q., He Y., Kabahuma M., Chaya T., Kelly A., Borrego E., et al. (2017). A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens. Nat. Genet. 49, 1364–1372. doi: 10.1038/ng.3919, 28740263.
Yang Q., Li Z., Li W., Ku L., Wang C., Ye J., et al. (2013). CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl. Acad. Sci. 110, 16969–16974. doi: 10.1073/pnas.1310949110, 24089449.
Yang N., Liu J., Gao Q., Gui S., Chen L., Yang L., et al. (2019). Genome assembly of a tropical maize inbred line provides insights into structural variation and crop improvement. Nat. Genet. 51, 1052–1059. doi: 10.1038/s41588-019-0427-6, 31152161.
Zhang C., Dong S.-S., Xu J.-Y., He W.-M., Yang T.-L., (2019). PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786–1788. doi: 10.1093/bioinformatics/bty875, 30321304.
Zhang W. Z., Hua-Quan L., Heng-Ling L. I., Wei-Zheng G., Kui-Sen W., (2006). Application of 'Tie7922' Derived lines in maize breeding and production. Rain Fed. Crops.
Zhang R., Jia G., Diao X., (2023). geneHapR: an R package for gene haplotypic statistics and visualization. BMC Bioinf. 24, 199. doi: 10.1186/s12859-023-05318-9, 37189023.
