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Chromosomal inversion at the DG1 promoter drives double-grain spikelets and enhances grain yield in sorghum

Nature Plants volume 11, pages 453–467 (2025)Cite this article

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Abstract

The phenomenon of multiple-grain spikelets is frequently observed in gramineous crops. In the case of dual-floret spikelets, the upper fertile floret develops normally to form a single grain, while the lower sterile floret undergoes abortion. Here we elucidate the role of Double-Grain 1 (DG1), a gene encoding a homeobox-domain-containing protein, in regulating the lower floret meristem activity and double-grain spikelet trait in sorghum. A 35.7-kb paracentric inversion in the DG1 promoter region leads to increased DG1 expression, probably by reducing repressive histone modifications. This increase in DG1 expression transforms the degenerated lower floret into a fertile one. The use of the superior DG1 allele results in an increase of approximately 40.7% to 46.1% in grain number per panicle and a 10.1% to 14.3% increase in overall grain yield. Our findings shed light on the sorghum double-grain spikelet characteristic, offering valuable insights for high-yield breeding designs in cereals.

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Fig. 1: Identification and map-based cloning of the DG1 locus in controlling the sorghum double-grain trait.
Fig. 2: ORF1 is the candidate gene for DG1.
Fig. 3: DG1 reduced repressive histone lysine methylation and increased gene expression.
Fig. 4: DG1 exhibits fertility of the lower floret to form double grains.
Fig. 5: The potential downstream pathways of DG1.
Fig. 6: DG1 potentially enhances grain number and grain yield.
Fig. 7: A proposed working model for the regulation of the double-grain trait by DG1 in sorghum.

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Data availability

The raw sequence data from RNA-seq reported in this paper have been deposited in the Genome Sequence Archive in the National Genomics Data Center, China National Center for Bioinformation, Chinese Academy of Sciences, under accession number CRA014887. The gene sequences and amino acid sequences used in this paper were collected from Phytozome (https://phytozome-next.jgi.doe.gov/). Source data are provided with this paper.

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (grant nos 32241038 to Q.X., 32472124 to P.X., 32201780 to P.X., 32241045 to Q.X. and 32241042 to F. Yu), the National High-Level Personnel of Special Support Program (grant no. 2024WRQB003 to P.X.), the National Key R&D Program of China (grant nos 2022YFD1500503, 2023YFD1200700 and 2023YFD1200704 to S.T.), the Shenzhen Science and Technology Program (grant no. JCYJ20240813151204006 to P.X.), the Moutai Group Research and Development Project (grant no. 2023011 to Q.X.), the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDA0440302 to Q.X.), the ShenZhen Postdoctoral Funding Project (grant no. 77000*42100029 to P.X.) and the Fundamental Research Fund for the Central Universities (grant no. 77000-12240011 to P.X.).

Author information

Author notes

  1. These authors contributed equally: Dan Zhang, Sanyuan Tang.

Authors and Affiliations

  1. Institute of Genetics and Developmental Biology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, P. R. China

    Dan Zhang, Sanyuan Tang, Kangxu Zhao, Chao Li, Ran Xia & Qi Xie

  2. State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China

    Junyu Chen & Cheng-Guo Duan

  3. Guangdong Provincial Key Laboratory of Plant Stress Biology, School of Agriculture and Biotechnology, Shenzhen Campus of Sun Yat-sen University, Sun Yat-sen University, Shenzhen, P. R. China

    Fangyuan Liu, Lu Kang, Fang Yang & Peng Xie

  4. College of Grassland Science and Technology, China Agricultural University, Beijing, China

    Feifei Yu

  5. University of Chinese Academy of Sciences, Beijing, P. R. China

    Qi Xie

  6. State Key Laboratory of Crop Germplasm Innovation and Molecular Breeding, National Center of Technology Innovation for Maize, Syngenta Group China, Beijing, China

    Qi Xie

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Contributions

Q.X. and P.X. designed this project. P.X. and D.Z. wrote the manuscript. D.Z., P.X. and S.T. performed most of the experiments. D.Z., P.X., S.T., K.Z. and F.L. constructed multiple segregated populations and evaluated the yield traits in the field. D.Z. and P.X. collected the genotyping data for the linkage map construction. D.Z., P.X. and R.X. performed the transgenic experiments in sorghum. C.-G.D. and J.C. performed the ChIP–qPCR assay. F.L., L.K. and F. Yang performed RNA in situ hybridization. P.X., D.Z., F. Yu and C.L. analysed the data. All authors have read, discussed and contributed to the manuscript.

Corresponding authors

Correspondence to Peng Xie or Qi Xie.

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Nature Plants thanks Hongning Tong and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 DG1 is a single dominant locus for double-grain trait.

a, Seed morphology at filling stage of single-grain spikelet and IDGS and EDGS. IDGS, Ineffective double-grain spikelet. EDGS, Effective double-grain spikelet. Gl, Glume. Bar = 1 mm. b, Spikelet morphology of double-grain line NSL360516 and F.R. Miller, as well as three single-grain lines SC855, KS115 and BTx399. Upper and lower bar = 1 cm and 0.5 cm, respectively. c, Ratio of double-grain spikelet in NSL360516, SC855, BTx399, KS115, F1 (NSL360516 × SC855), F1 (NSL360516 × KS115), and F1 (NSL360516 × BTx399). d, Ratio of double-grain spikelet in F.R. Miller, F1 (F.R. Miller × SC855), F1 (F.R. Miller × KS115), and F1 (F.R. Miller × BTx399). e, Genetic analysis in three F2 populations derived from F2 (NSL360516 × SC855), F2 (NSL360516 × KS115), and F2 (NSL360516 × BTx399). Data are shown as mean ± SD, n = 3 biological replicates.

Source data

Extended Data Fig. 2 Construction of the NIL lines.

a, Through molecular markers assisted selection, the NIL lines were constructed from BTx399 and NSL360516 through self-crossing several generations. b, The genetic background of NIL-dg1 and NIL-DG1 lines. The red boxes indicate that the genotypes are derived from NSL360516. The background in white means genotypes is the same between the two NILs.

Extended Data Fig. 3 A chromosomal paracentric inversion in ORF5-KO mutant.

a, The chromosomal paracentric inversion fragment is 2077 bp. It occurred between sgRNA1 and sgRNA2 targets in the homozygous ORF5-KO line. b, Schematic diagram of the peptide sequence alignment of ORF5 and ORF5-KO.

Extended Data Fig. 4 The DG1 orthologs in crops.

a, Phylogenetic analysis of DG1 and its orthologs in different species, including sorghum, maize, Setaria italica, rice and Arabidopsis thaliana. The phylogenetic tree was constructed using the maximum likelihood method. b, Protein sequence alignment of SbDG1 (Sorghum bicolor), AtWUS (Arabidopsis), and ZmWUS1 (maize). The red box indicates the homeobox domain.

Extended Data Fig. 5 Number of stamens and pistils in NIL-dg1 and NIL-DG1.

a, Number of double pistils in NIL-dg1 and NIL-DG1. b, Number of stamens in NIL-dg1 and NIL-DG1. For each line, 200 spikelets were examined.

Source data

Extended Data Fig. 6 Gene expression of SbbZIP34, SbAP2-39 and SbABCG26 in NIL-dg1 and NIL-DG1.

a, Relative expression of SbbZIP34 in the NIL-dg1 and NIL-DG1 at YP1 stage. b, Relative expression of SbAP2-39 in the NIL-dg1 and NIL-DG1 at YP1 stage. c, Relative expression of SbABCG26 in the NIL-dg1 and NIL-DG1 at YP1 stage. Three biological repeats were performed. P value was calculated by two-tailed Student’s t test, *** P < 0.001, ** P < 0.01.

Source data

Extended Data Fig. 7 DG1 enhances grain number and grain yield in 2023.

Field-yield tests were conducted in Beijing in 2023 (See Methods). a, Representative mature panicle and spikelet morphology of NIL-dg1 and NIL-DG1. Left and right bar = 3 mm and 5 cm, respectively. b-c, Grain morphology and statistics of grain length (GL), grain width (GW) and grain thickness (GW) of NIL-dg1, IDGS and EDGS of NIL-DG1. n = 3. Bar = 5 mm. d-h, Statistical analysis of thousand grain weight (n = 3), grain number per panicle (n = 3), grain weight per panicle (n = 3), grain yield per plot (n = 3; plot size: 10 meters long and 4 meters wide, with row spacing set at 50 cm and plant spacing at 20 cm) in NIL-dg1 and NIL-DG1. Data are shown as mean ± SD. P value was determined by two-tailed Student’s t test, *** P < 0.001, ** P < 0.01.

Source data

Extended Data Fig. 8 DG1 enhances grain number and grain yield in different region.

Field-yield tests were conducted in ShenZhen in 2024. a, Representative mature panicle morphology of NIL-dg1 and NIL-DG1. Bar = 5 cm. b–e, Statistical analysis of thousand grain weight (n = 10), grain number per panicle (n = 8), grain yield per panicle (n = 10), grain yield per plot (n = 3, plot size: 4 meters long and 3 meters wide, with row spacing set at 50 cm and plant spacing at 20 cm) in NIL-dg1 and NIL-DG1. Data are shown as mean ± SD. P value was determined by two-tailed Student’s t test, *** P < 0.001, ** P < 0.01, * P < 0.05, ns: no significant difference.

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Supplementary information

Reporting Summary

Supplementary Dataset 1

Downstream DEG detection for DG1.

Supplementary Dataset 2

Primers used in this study.

Source data

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Zhang, D., Tang, S., Chen, J. et al. Chromosomal inversion at the DG1 promoter drives double-grain spikelets and enhances grain yield in sorghum. Nat. Plants 11, 453–467 (2025). https://doi.org/10.1038/s41477-025-01937-7

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