Skip to main content
Log in

Unique genetic architecture of prolificacy in ‘Sikkim Primitive’ maize unraveled through whole-genome resequencing-based DNA polymorphism

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

‘Sikkim Primitive’ maize landrace, unique for prolificacy (7–9 ears per plant) possesses unique genomic architecture in branching and inflorescence-related gene(s), and locus Zm00001eb365210 encoding glycosyltransferases was identified as the putative candidate gene underlying QTL (qProl-SP-8.05) for prolificacy. The genotype possesses immense usage in breeding high-yielding baby-corn genotypes.

Abstract

‘Sikkim Primitive’ is a native landrace of North Eastern Himalayas, and is characterized by having 7–9 ears per plant compared to 1–2 ears in normal maize. Though ‘Sikkim Primitive’ was identified in the 1960s, it has not been characterized at a whole-genome scale. Here, we sequenced the entire genome of an inbred (MGUSP101) derived from ‘Sikkim Primitive’ along with three non-prolific (HKI1128, UMI1200, and HKI1105) and three prolific (CM150Q, CM151Q and HKI323) inbreds. A total of 942,417 SNPs, 24,160 insertions, and 27,600 deletions were identified in ‘Sikkim Primitive’. The gene-specific functional mutations in ‘Sikkim Primitive’ were classified as 10,847 missense (54.36%), 402 non-sense (2.015%), and 8,705 silent (43.625%) mutations. The number of transitions and transversions specific to ‘Sikkim Primitive’ were 666,021 and 279,950, respectively. Among all base changes, (G to A) was the most frequent (215,772), while (C to G) was the rarest (22,520). Polygalacturonate 4-α-galacturonosyltransferase enzyme involved in pectin biosynthesis, cell-wall organization, nucleotide sugar, and amino-sugar metabolism was found to have unique alleles in ‘Sikkim Primitive’. The analysis further revealed the Zm00001eb365210 gene encoding glycosyltransferases as the putative candidate underlying QTL (qProl-SP-8.05) for prolificacy in ‘Sikkim Primitive’. High-impact nucleotide variations were found in ramosa3 (Zm00001eb327910) and zeaxanthin epoxidase1 (Zm00001eb081460) genes having a role in branching and inflorescence development in ‘Sikkim Primitive’. The information generated unraveled the genetic architecture and identified key genes/alleles unique to the ‘Sikkim Primitive’ genome. This is the first report of whole-genome characterization of the ‘Sikkim Primitive’ landrace unique for its high prolificacy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available in the NCBI Sequence Read Archives (SRA) repository with BioProject number PRJNA1078761.

References

  • Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA (2019) An update on the signals controlling shoot branching. Trends Plant Sci 24(3):220–236

    Article  CAS  PubMed  Google Scholar 

  • Bayer PE, Golicz AA, Scheben A, Batley J, Edwards D (2020) Plant pan-genomes are the new reference. Nat Plants 6(8):914–920

    Article  PubMed  Google Scholar 

  • Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6(2):80–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38(5):594–597

    Article  CAS  PubMed  Google Scholar 

  • Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danecek P, Bonfield JK, Liddle J et al (2021) Twelve years of SAMtools and BCFtools. Gigascience 10(2):giab008

    Article  PubMed  PubMed Central  Google Scholar 

  • Demesa-Arevalo E, Abraham-Juarez MJ, Xu X, Bartlett M, Jackson D (2021) Maize RAMOSA3 accumulates in nuclear condensates enriched in RNA POLYMERASE II isoforms during the establishment of axillary meristem determinacy. Preprint bioRxiv. https://doi.org/10.1101/2021.04.06.438639

    Article  Google Scholar 

  • DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhawan NL (1964) Primitive maize in Sikkim. Maize Genet Coop News Lett 38:69–70

    Google Scholar 

  • Doebley J, Stec A, Gustus C (1995) teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141(1):333–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Z, Xiao Y, Govindarajulu R, Feil R, Siddoway ML, Nielsen T, Lunn JE, Hawkins J, Whipple C, Chuck G (2019) The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression. Nat Commun 10(1):1–15

    Article  Google Scholar 

  • Duan H, Xue Z, Ju X, Yang L, Gao J, Sun L, Xu S, Li J, Xiong X, Sun Y, Wang Y, Zhang X, Ding D, Zhang X Tang J (2023) The genetic architecture of prolificacy in maize revealed by association mapping and bulk segregant analysis. Theoretical and Applied Genetics, 136(9):182

  • Du L, Zhang C, Liu Q, Zhang X, Yue B (2018) Krait: an ultrafast tool for genome-wide survey of microsatellites and primer design. Bioinformatics 34(4):681–683

    Article  CAS  PubMed  Google Scholar 

  • Du K, Zhao W, Mao Y, Lv Z, Khattak WA, Ali S, Zhou Z, Wang Y (2022) Maize ear growth is stimulated at the fourth day after pollination by cell wall remodelling and changes in lipid and hormone signalling. J Sci Food Agric 102(12):5429–5439

    Article  CAS  PubMed  Google Scholar 

  • Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:1–14

    Article  Google Scholar 

  • Gramazio P, Yan H, Hasing T, Vilanova S, Prohens J, Bombarely A (2019) Whole-Genome resequencing of seven eggplant (Solanum melongena) and one wild relative (S. incanum) accessions provides new insights and breeding tools for eggplant enhancement. Front Plant Sci 10:1220

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Colantonio V, Müller BS, Leach KA, Nanni A, Finegan C, Wang B, Baseggio M, Newton CJ, Juhl EM, Hislop L, Gonzalez JM, Rios EF, Hannah LC, Swarts K, Gore MA, Hennen-Bierwagen TA, Myers AM, Settles AM, Tracy WF, Resende MF (2021) Genome assembly and population genomic analysis provide insights into the evolution of modern sweet corn. Nat Commun 12(1):1–13

    Google Scholar 

  • Hufford MB, Seetharam AS, Woodhouse MR et al (2021) De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science 373(6555):655–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain F, Sarika K, Muthusamy V, Zunjare RU, Gupta HS (2019) Quality protein maize for nutritional security. Quality breeding in field crops, 217–237

  • Islam MS, Coronejo S, Subudhi PK (2020) Whole-genome sequencing reveals uniqueness of black-hulled and straw-hulled weedy rice genomes. Theor Appl Genet 133:2461–2475

    Article  CAS  PubMed  Google Scholar 

  • Jayakodi M, Padmarasu S, Haberer G et al (2020) The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 588(7837):284–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapoor C, Singh S, Avasthe RK, Raj C, Singh M, Lepcha HL (2022) Morphological description based on DUS characters and molecular characterization of ‘Sikkim Primitive’maize: an endangered unique genetic resource. Plant Genetic Resources, 20(1):69–72

  • Klein H, Gallagher J, Demesa-Arevalo E, Abraham-Juárez MJ, Heeney M, Feil R, Lunn JE, Xiao Y, Chuck G, Whipple C, Jackson D, Bartlett M (2022) Recruitment of an ancient branching program to suppress carpel development in maize flowers. Proc Natl Acad Sci USA 119(2):e2115871119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Liotenberg S, North H, Marion-Poll A (1999) Molecular biology and regulation of abscisic acid biosynthesis in plants. Plant Physiol Biochem 37(5):341–350

    Article  CAS  Google Scholar 

  • Magloire A (2000) Grep: searching for a pattern. iUniverse publishing house, Bloomington

    Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2016) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(1):200–203

    Google Scholar 

  • Mateo-Bonmatí E, Casanova-Sáez R, Simura J, Ljung K (2021) Broadening the roles of UDP-glycosyltransferases in auxin homeostasis and plant development. New Phytol 232:642–654

    Article  PubMed  Google Scholar 

  • Pal S, Zunjare RU, Muthusamy V, Duo H, Gowda MM, Bhowmick PK, Kasana R, Bhatt V, Hossain F (2020) Influence of T-, C-and S-cytoplasms on male sterility and their utilization in baby corn hybrid breeding. Euphytica 216(9):1–10

    Article  Google Scholar 

  • Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. BioSystems 109(3):397–402

    Article  CAS  PubMed  Google Scholar 

  • Pande S, Sachan JKS, Sarkar KR (1988) Knob composition in northeastern Himalayan maize. Indian J Genet Plant Breed 48(2):219–224

    Google Scholar 

  • Prakash NR, Zunjare RU, Muthusamy V, Chand G, Kamboj MC, Bhat JS, Hossain F (2019) Genetic analysis of prolificacy in “Sikkim Primitive”—A prolific maize (Zea mays) landrace of North-Eastern Himalaya. Plant Breed 138(6):781–789

    Article  CAS  Google Scholar 

  • Prakash NR, Chhabra R, Zunjare RU, Muthusamy V, Hossain F (2020) Molecular characterization of teosinte branched1 gene governing branching architecture in cultivated maize and wild relatives. 3 Biotech 10(2):77

    Article  PubMed  PubMed Central  Google Scholar 

  • Prakash NR, Zunjare RU, Muthusamy V, Rai M, Kumar A, Guleria SK, Bhatt V, Choudhary JR, Chand G, Jaiswal SK, Bhat JS, Hossain F (2021) A novel quantitative trait loci governs prolificacy in ‘Sikkim Primitive’—a unique maize (Zea mays) landrace of North-Eastern Himalaya. Plant Breed 140(3):400–408

    Article  CAS  Google Scholar 

  • Prasanna BM (2010) Phenotypic and molecular diversity of maize landraces: characterization and utilization. Indian J Genet Plant Breed 70(4):315–327

    Google Scholar 

  • Prasanna BM, Sharma L (2005) The landraces of maize (Zea mays L.): diversity and utility. Ind J Plant Genet Res 18(2):155–168

    Google Scholar 

  • Rajkumar MS, Jain M, Garg R (2021) Discovery of DNA polymorphisms via whole genome resequencing and their functional relevance in salinity stress response in chickpea. Physiol Plant 173(4):1573–1586

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna G, Kaur P, Nigam D, Chaduvula PK, Yadav S, Talukdar A, Singh NK, Gaikwad K (2018) Genome-wide identification and characterization of InDels and SNPs in Glycine max and Glycine soja for contrasting seed permeability traits. BMC Plant Biol 18(1):1–15

    Article  Google Scholar 

  • Rotili DH, Abeledo LG, Larrea SM, Maddonni GÁ (2022) Grain yield and kernel setting of multiple-shoot and/or multiple-ear maize hybrids. Field Crops Res 279:108471

    Article  Google Scholar 

  • Sachan JKS, Sarkar KR (1986) Discovery of Sikkim Primitive precursor in the Americas. Maize Genet Coop News Lett 60:104–106

    Google Scholar 

  • Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441(7090):227–230

    Article  CAS  PubMed  Google Scholar 

  • Shamimuzzaman M, Gardiner JM, Walsh AT, Triant DA, Le Tourneau JJ, Tayal A, Unni RD, Nguyen HN, Portwood JL, Cannon EKS, Andorf CN, Elsik CG (2020) MaizeMine: a data mining warehouse for the maize genetics and genomics database. Front Plant Sci 11:e592730

    Article  Google Scholar 

  • Sharma L, Prasanna BM, Ramesh B (2010) Analysis of phenotypic and microsatellite-based diversity of maize landraces in India, especially from the North East Himalayan region. Genetica, 138:619–631

  • Shin Y, Chane A, Jung M, Lee Y (2021) Recent advances in understanding the roles of pectin as an active participant in plant signaling networks. Plants 10(8):1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subudhi PK, Shankar R, Jain M (2020) Whole genome sequence analysis of rice genotypes with contrasting response to salinity stress. Sci Rep 10(1):1–13

    Article  Google Scholar 

  • Sukto S, Lomthaisong K, Sanitchon J, Chankaew S, Falab S, Lübberstedt T, Lertrat K, Suriharn K (2021) Breeding for prolificacy, total carotenoids and resistance to downy mildew in small-ear waxy corn by modified mass selection. Agron 11(9):1793

    Article  CAS  Google Scholar 

  • Tao Y, Zhaom X, Macem E, Henrym R, Jordanm D (2019) Exploring and exploiting pan-genomics for crop improvement. Mol Plant 12(2):156–169

    Article  CAS  PubMed  Google Scholar 

  • Taranto F, D’Agostino N, Rodriguez M, Pavan S, Minervini AP, Pecchioni N, Papa R, De Vita P (2020) Whole genome scan reveals molecular signatures of divergence and selection related to important traits in durum wheat germplasm. Front Genet 11:217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45(W1):W122–W129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varshney RK, Saxena RK, Upadhyaya HD et al (2017) Whole-genome resequencing of 292 Pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits. Nature Genet 49(7):1082

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Thudi M, Roorkiwal M et al (2019) Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nature Genet 51(5):857–864

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Roorkiwal M, Sun S et al (2021) A chickpea genetic variation map based on the sequencing of 3,366 genomes. Nature 599:622–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zhang R, Zhao Y, Yao J, Li W, Yang Z, Sun F, Yang X (2023) Identifying QTL and candidate genes for prolificacy in maize. Crop J 11(2):531–539

    Article  CAS  Google Scholar 

  • Woodhouse MR, Sen S, Schott D, Portwood JL, Freeling M, Walley JW, Andorf CM, Schnable JC (2022) qTeller: A tool for comparative multi-genomic gene expression analysis. Bioinformatics 38(1):236–242

    Article  CAS  Google Scholar 

  • Xu G, Zhang X, Chen W, Zhang R, Li Z, Wen W, Warburton ML, Li J, Li H, Yang X (2022) Population genomics of Zea species identifies selection signatures during maize domestication and adaptation. BMC Plant Boil 22(1):1–15

    CAS  Google Scholar 

  • Yang CJ, Samayoa LF, Bradbury PJ, Olukolu BA, Xue W, York AM, Tuholski MR, Wang W, Daskalska LL, Neumeyer MA, de Jesus Sanchez-Gonzalez J, Romay MC, Glaubitz JC, Sun Q, Buckler ES, Holland JB, Doebley JF (2019) The genetic architecture of teosinte catalyzed and constrained maize domestication. Proc Natl Acad Sci USA 116(12):5643–5652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Yu J, Wang Q, Wang J, Zhao G, Wu H, Zhu Y, Chu C, Fang J (2021) Overexpression of the rice ORANGE gene OsOR negatively regulates carotenoid accumulation, leads to higher tiller numbers and decreases stress tolerance in Nipponbare rice. Plant Sci 310:110962

    Article  CAS  PubMed  Google Scholar 

  • Yue L, Li G, Dai Y, Sun X, Li F, Zhang S, Zhang H, Sun R, Zhang S (2021) Gene co-expression network analysis of the heat-responsive core transcriptome identifies hub genes in Brassica rapa. Planta 253(5):1–23

    Article  Google Scholar 

  • Zhou L, Zhang J, Yan J, Song R (2011) Two transposable element insertions are causative mutations for the major domestication gene teosinte branched1 in modern maize. Cell Res 21(8):1267–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou MB, Wu JJ, Ramakrishnan M, Meng XW, Vinod KK (2019) Prospects for the study of genetic variation among Moso bamboo wild-type and variants through genome resequencing. Trees 33(2):371–381

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the financial support received from the World Bank-Indian Council of Agricultural Research funded National Agricultural Higher Education Project (NAHEP) through its Centre for Advanced Agricultural Science and Technology (CAAST) on Genomics Assisted Breeding for Crop Improvement to ICAR-IARI, New Delhi (NAHEP-CAAST 71-01). The first author grateful to Council of Scientific and Industrial Research (CSIR-India) for a fellowship (09/083(0368)/2016-EMR-I) offered during the Ph.D. programme. We also acknowledge the breeders of AICRP-Maize for sharing their inbred for analysis. Our sincere thanks to Dr. B.M. Prasanna for the collection of Sikkim Primitive (landrace) from Sikkim.

Author information

Authors and Affiliations

Authors

Contributions

Conduct of the experiment: NRP, data handling and analysis: KK, candidate gene analysis: VM and RUZ, drafting of manuscript: NRP and FH, designing of experiment: FH.

Corresponding author

Correspondence to Firoz Hossain.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

No ethical approval is required.

Additional information

Communicated by Manoj Prasad.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 107 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prakash, N.R., Kumar, K., Muthusamy, V. et al. Unique genetic architecture of prolificacy in ‘Sikkim Primitive’ maize unraveled through whole-genome resequencing-based DNA polymorphism. Plant Cell Rep 43, 134 (2024). https://doi.org/10.1007/s00299-024-03176-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-024-03176-0

Keywords

Navigation