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Ginger genome reveals the SMPED1 gene causing sex-phase synchrony and outcrossing in a flowering plant

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Abstract

In many flowering plants, male and female reproductive organs mature at different times to avoid self-pollination, a phenomenon termed dichogamy. Most dichogamous species are either protandrous or protogynous, making this strategy difficult to study genetically. However, in the ginger Alpinia mutica, protandrous and protogynous floral morphs co-occur within populations, and the synchronized rhythmic movement of styles and dehiscence of stamens promotes cross-pollination between morphs. Here we demonstrate that a single Mendelian locus with a dominant allele governing protogyny controls sexual polymorphism. We used haplotype-resolved genomes and population genomics to identify the dichogamy-determining region, revealing a large deletion in the protandrous morphotype. We found that the key gene SMPED1, located adjacent to the deletion, governs the timing of anther dehiscence and style movement. SMPED1 is widespread among angiosperms and probably has conserved function. Our findings represent a new genetic characterization of a key mating system gene controlling the synchrony of sex organs in flowering plants.

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Fig. 1: Mendelian inheritance of dichogamy in Alpinia species.
Fig. 2: Identification of the DDR in the A. mutica genome.
Fig. 3: Confirmation that SMPED1 determines the sex-phase synchrony of dichogamy.
Fig. 4: Origin of the DDR in ginger and related families.
Fig. 5: Evolution of the putative DDR in angiosperms.

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Data availability

The raw sequence data reported in this paper have been deposited in the Genome Sequence Archive at the National Genomics Data Center, China National Center for Bioinformation, Beijing Institute of Genomics, Chinese Academy of Sciences and are publicly accessible at https://ngdc.cncb.ac.cn/gsa. Among them, the HiFi reads, Hi-C reads and full-length transcriptome reads can be found under accession number CRA020599 (reviewer link: https://ngdc.cncb.ac.cn/gsa/s/Su7E6mDl), and the resequencing data are under accession number CRA020857 (reviewer link: https://ngdc.cncb.ac.cn/gsa/s/Z3T7vDQ6). Transcriptome reads of different time points can be shared on request from the corresponding author J.-L.Z. because these data are under further explored. Source data are provided with this paper.

Code availability

All analysis tools used in this study are publicly available, as described in Methods and Reporting Summary.

References

  1. Harder, L. D. & Barrett, S. C. H. Ecology and Evolution of Flowers (Oxford Univ. Press, 2006).

  2. Darwin, C. The Different Forms of Flowers on Plants of the Same Species (John Murray, 1877).

  3. Barrett, S. C. H. The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274–284 (2002).

    Article  CAS  PubMed  Google Scholar 

  4. Charlesworth, D. & Charlesworth, B. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Evol. Syst. 18, 237–268 (1987).

    Article  Google Scholar 

  5. Morran, L. T., Parmenter, M. D. & Phillips, P. C. Mutation load and rapid adaptation favour outcrossing over self-fertilization. Nature 462, 350–352 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bertin, R. I. & Newman, C. M. Dichogamy in angiosperms. Bot. Rev. 59, 112–152 (1993).

    Article  Google Scholar 

  7. Lloyd, D. G. & Webb, C. J. The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. N. Z. J. Bot. 24, 135–162 (1986).

    Article  Google Scholar 

  8. Bertin, R. I. Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. Am. J. Bot. 80, 557–560 (1993).

    PubMed  Google Scholar 

  9. Darwin, C. On the Various Contrivances by Which British and Foreign Orchids Are Fertilized by Insects, and on the Good Effects of Intercrossing (John Murray, 1862).

  10. Darwin, C. The Effects of Cross- and Self-Fertilization in the Vegetable Kingdom (Murray, 1876).

  11. Renner, S. S. & Muller, N. A. Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration. Nat. Plants 392, 392–402 (2021).

    Article  Google Scholar 

  12. Boualem, A. et al. A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321, 836–838 (2008).

    Article  CAS  PubMed  Google Scholar 

  13. Huu, C. N. et al. Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses. eLife 5, e17956 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Xue, H., Gong, Y., Wright, S. I. & Barrett, S. C. H. The genomic basis of the tristylous floral polymorphism—evidence for a role of gene duplications in a region of restricted recombination. Mol. Biol. Evol. 42, msaf170 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Renner, S. S. How common is heterodichogamy?. Trends Ecol. Evol. 16, 595–597 (2001).

    Article  Google Scholar 

  16. Gleeson, S. K. Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36, 892–902 (1982).

    Article  PubMed  Google Scholar 

  17. Groh, J. S. et al. Ancient structural variants control sex-specific flowering time morphs in walnuts and hickories. Science 387, eado5578 (2025).

    Article  CAS  PubMed  Google Scholar 

  18. Li, Q.-J. et al. Flexible style that encourages outcrossing. Nature 410, 432 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Li, Q.-J. et al. Study on the flexistyly pollination mechanism in Alpinia plants (Zingiberaceae). Acta Bot. Sin. 43, 364–369 (2001).

    Google Scholar 

  20. Cui, X., Wei, R. & Huang, R. A preliminary study on the genetic system of Amomum tsao-ko. J. Yunnan Univ. 17, 290–297 (1995).

    Google Scholar 

  21. Li, Q.-J. et al. Mating system and stigmatic behaviour during flowering of Alpinia kwangsiensis (Zingiberaceae). Plant Syst. Evol. 232, 123–132 (2002).

    Article  Google Scholar 

  22. Liu, M., Sun, S. & Li, Q. The relation between stigma position and receptivity in two flexistylous gingers. Biodivers. Sci. 15, 639–644 (2007).

    Article  Google Scholar 

  23. Chen, S. et al. Genetic and genomic insights into dichogamy in Zingiberaceae. Plant Commun. 6, 101352 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Thompson, T. E. & Romberg, L. D. Inheritance of heterodichogamy in pecan. J. Hered. 76, 456–458 (1985).

    Article  Google Scholar 

  25. Huang, J. et al. Stigma receptors control intraspecies and interspecies barriers in Brassicaceae. Nature 614, 303–308 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang, L. et al. FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa. Curr. Biol. 31, 3004–3016 (2021).

    Article  CAS  PubMed  Google Scholar 

  27. Sass, C., Iles, W. J. D., Barrett, C. F., Smith, S. Y. & Specht, C. D. Revisiting the Zingiberales: using multiplexed exon capture to resolve ancient and recent phylogenetic splits in a charismatic plant lineage. PeerJ 4, e1584 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Carlsen, M. M. et al. Resolving the rapid plant radiation of early diverging lineages in the tropical Zingiberales: pushing the limits of genomic data. Mol. Phylogenet. Evol. 128, 55–68 (2018).

    Article  PubMed  Google Scholar 

  29. Cheng, S. P. et al. Haplotype-resolved genome assembly and allele-specific gene expression in cultivated ginger. Hortic. Res. 8, 188 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. D’Hont, A. et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213–217 (2012).

    Article  PubMed  Google Scholar 

  31. Li, H.-T. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5, 461–470 (2019).

    Article  PubMed  Google Scholar 

  32. Willemstein, S. C. An Evolutionary Basis for Pollination Ecology Leiden Botanical Series 10 (Brill, 1987).

  33. Routley, M. B., Bertin, R. I. & Husband, B. C. Correlated evolution of dichogamy and self-incompatibility: a phylogenetic perspective. Int. J. Plant Sci. 165, 983–993 (2004).

    Article  Google Scholar 

  34. Charlesworth, B. & Charlesworth, D. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112, 975–997 (1978).

    Article  Google Scholar 

  35. Harkess, A. et al. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat. Commun. 8, 1279 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kappel, C., Huu, C. N. & Lenhard, M. A short story gets longer: recent insights into the molecular basis of heterostyly. J. Exp. Bot. 68, 5719–5730 (2017).

    Article  CAS  PubMed  Google Scholar 

  37. Haldane, J. B. S. A mathematical theory of natural and artificial selection. Math. Proc. Camb. 23, 363–372 (2008).

    Article  Google Scholar 

  38. Orr, H. A. & Betancourt, A. J. Haldane’s sieve and adaptation from the standing genetic variation. Genetics 157, 875–884 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Maydeu-Olivares, A. & García-Forero, C. in International Encyclopedia of Education 3rd edn (eds Peterson, P. et al.) 190–196 (Elsevier, 2010).

  40. Tarailo-Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinform. 25, 4.10.11–14.10.14 (2009).

    Article  Google Scholar 

  41. Jurka, J. et al. Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467 (2005).

    Article  CAS  PubMed  Google Scholar 

  42. Ou, S. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Brůna, T., Hoff, K. J., Lomsadze, A., Stanke, M. & Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom. Bioinform. 3, lqaa108 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Li, H. L. et al. Haplotype-resolved genome of diploid ginger (Zingiber officinale) and its unique gingerol biosynthetic pathway. Hortic. Res. 8, 189 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gabriel, L., Hoff, K. J., Bruna, T., Borodovsky, M. & Stanke, M. TSEBRA: transcript selector for BRAKER. BMC Bioinform. 22, 566 (2021).

    Article  CAS  Google Scholar 

  49. Aramaki, T. et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 36, 2251–2252 (2020).

    Article  CAS  PubMed  Google Scholar 

  50. Zdobnov, E. M. & Apweiler, R. InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847–848 (2001).

    Article  CAS  PubMed  Google Scholar 

  51. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

    Article  Google Scholar 

  52. Shang, L. et al. A complete assembly of the rice Nipponbare reference genome. Mol. Plant 16, 1232–1236 (2023).

    Article  CAS  PubMed  Google Scholar 

  53. Wang, Z. et al. A chromosome-level reference genome of Ensete glaucum gives insight into diversity and chromosomal and repetitive sequence evolution in the Musaceae. GigaScience 11, giac027 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Droc, G. et al. The banana genome hub: a community database for genomics in the Musaceae. Hortic. Res. 9, uhac221 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Martin, G. et al. Improvement of the banana “Musa acuminata” reference sequence using NGS data and semi-automated bioinformatics methods. BMC Genom. 17, 243 (2016).

    Article  Google Scholar 

  56. Wang, Z. et al. Musa balbisiana genome reveals subgenome evolution and functional divergence. Nat. Plants 5, 810–821 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Belser, C. et al. Chromosome-scale assemblies of plant genomes using nanopore long reads and optical maps. Nat. Plants 4, 879–887 (2018).

    Article  CAS  PubMed  Google Scholar 

  58. Li, Z. et al. The Musa troglodytarum L. genome provides insights into the mechanism of non-climacteric behaviour and enrichment of carotenoids. BMC Biol. 20, 186 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    Article  CAS  PubMed  Google Scholar 

  61. Li, L., Stoeckert, C. J. Jr. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).

    Article  Google Scholar 

  64. Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zhang, Z. et al. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom. Proteom. Bioinform. 4, 259–263 (2006).

    Article  CAS  Google Scholar 

  67. Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Vasimuddin, M., Misra, S., Li, H. & Aluru, S. Efficient architecture-aware acceleration of BWA-MEM for multicore systems. In 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS) 314–324 (IEEE, 2019).

  69. McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Zhou, X. & Stephens, M. Genome-wide efficient mixed-model analysis for association studies. Nat. Genet. 44, 821–824 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  74. Javelle, M. & Timmermans, M. C. P. In situ localization of small RNAs in plants by using LNA probes. Nat. Protoc. 7, 533–541 (2012).

    Article  CAS  PubMed  Google Scholar 

  75. Kramer, E. M. Methods for studying the evolution of plant reproductive structures: comparative gene expression techniques. Methods Enzymol. 395, 617–636 (2005).

    Article  CAS  PubMed  Google Scholar 

  76. Zhang, X., Henriques, R., Lin, S.-S., Niu, Q.-W. & Chua, N.-H. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641–646 (2006).

    Article  CAS  PubMed  Google Scholar 

  77. Peterson, R., Slovin, J. P. & Chen, C. A simplified method for differential staining of aborted and non-aborted pollen grains. Int. J. Plant Biol. 1, e13 (2010).

    Article  Google Scholar 

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Acknowledgements

Q.-J.L. was the principal investigator of this project but passed away on 1 December 2022. This paper is in memory of the important contributions that he made to our understanding of the biology of gingers and the evolution of reproductive strategies in plants. This research was supported by a Joint Project between Yunnan Provincial Science and Technology Department and the ‘Double First-Class’ University Project of Yunnan University (grant no. 2019FY003001 to Q.-J.L.), the Ministry of Science and Technology of the PRC, the State Key Research Plan (grant no. 2019YFC1711100 to W.C.), the National Natural Science Foundation of China (grant no. U1602263 to Q.-J.L.; grant no. 41871047 to J.-L.Z.), a ‘Young Talent Project’ of Yunnan (grant no. YNWR-QNBJ-2019-214 to J.-L.Z.; grant no. C619300A101 to J.-J.H.) and the Postgraduate Research and Innovation Foundation of Yunnan University (grant no. 2021Z021 to A.-D.H.). We thank Y.-M. Xia, F.-C. Wu, H.-Z. Lu, H.-P. Xi, J. Gao, L.-J. Jiang and others from Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, for their kind help in collecting samples. We appreciate Q.-H. Duan and L. Yang from the College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China, for their help in the experiments on silencing by AS-ODNs. We thank D. Charlesworth, M. Lenhard and S. Wright for valuable discussions on hemizygosity.

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Author notes

  1. Deceased: Qing-Jun Li.

  2. These authors contributed equally: Jian-Li Zhao, Yang Dong, Ao-Dan Huang, Sheng-Chang Duan, Xiao-Chang Peng.

Authors and Affiliations

  1. State Key Laboratory of Vegetation Structure, Function and Construction (VegLab), Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology, and Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming, China

    Jian-Li Zhao, Ao-Dan Huang, Xiao-Chang Peng, Hong Liao, Ya-Li Wang, Wen-Jing Wang, Xin-Meng Zhu, Pei-Wen Luo, Xue Xia, Bo Li, Jia-Jia Han & Qing-Jun Li

  2. Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China

    Jian-Li Zhao, Jiang-Hua Chen & Qin-Ying Lan

  3. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Kunming, China

    Yang Dong, Sheng-Chang Duan & Wei Chen

  4. Yunnan Research Institute for Local Plateau Agriculture and Industry, Kunming, China

    Yang Dong, Sheng-Chang Duan & Wei Chen

  5. Key Laboratory of Subtropical Medicinal Edible Resources Development and Utilization in Yunnan Province, College of Biology and Chemistry, Puer University, Puer, China

    Yin-Ling Luo

  6. National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    W. John Kress

  7. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada

    Spencer C. H. Barrett

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  1. Jian-Li Zhao
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Contributions

J.-L.Z., Y.D., J.-J.H., S.C.H.B., W.C. and Q.-J.L. designed, conceived and supervised the research. A.-D.H., S.-C.D., X.-C.P., J.-L.Z., Q.-J.L., H.L., J.-H.C., Y.D., Y.-L.W., W.-J.W. and Q.-Y.L. collected the samples. J.-L.Z., Q.-J.L. and Y.-L.L. conducted the Mendelian inheritance experiments and the corresponding data analysis. S.-C.D., W.C., Y.D., X.-C.P. and J.-L.Z. performed the genome assembly, annotation, GWAS and evolutionary analysis. X.-C.P. and W.C. performed the SMPED1 protein prediction. A.-D.H., J.-J.H., X.-C.P., X.-M.Z., P.-W.L., X.X. and J.-H.C. validated SMPED1 and conducted the RT-qPCR experiments in transgenic plants. A.-D.H. and H.L. conducted the RNA in situ hybridizations. A.-D.H., X.-C.P., Y.D., J.-J.H. and J.-L.Z. conducted the experiments using AS-ODNs. J.-L.Z., A.-D.H., S.-C.D. and W.-J.W. analysed the expression data. The paper was drafted by J.-L.Z., Y.D., S.C.H.B., W.C., Q.-J.L., J.-J.H., W.J.K. and B.L. All authors contributed to the review of the paper before submission for publication and approved the final version.

Corresponding authors

Correspondence to Jian-Li Zhao, Jia-Jia Han, Spencer C. H. Barrett or Wei Chen.

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Nature Plants thanks Takashi Akagi, Roberta Bergero 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 Style and anther behavior of Alpinia mutica flowers under natural light conditions and continuous illumination.

Progression of daily flower maturation of the PG and PA morphs under natural light conditions (top) and continuous illumination (bottom). The small circles show close-up images of the stigmas (left circles) and anthers (right circles). Images at the time of anther dehiscence and style rotation are highlighted by blue borders. The scale bar is 1 cm.

Extended Data Fig. 2 Genome assembly and annotation of the PA and PG morphs in the Alpinia mutica genome.

a, Genome survey of the PA morph based on k-mer distribution of Illumina data. The k-mer distributions were constructed on the basis of 31-mers. b, Assembly and annotation pipeline of all sequencing data into the four haplotypes of the PA and PG morphs. Red-dashed square indicates the procedure of gene annotation. c, Hi-C contact map showing the 24 pseudochromosomes for the PA morph haplotype 2 (H2) genome using Hi-C reads. Numbers along diagonal line are chromosome numbers. d, Gene synteny among the four haplotypes of PA and PG morphs.

Extended Data Fig. 3 Comparison of genetic diversity (π) between the two dichogamous morphs in and around the DDR.

a, Genetic diversity (π) of PA and PG morphs across the DDR and adjacent region. Box plot in the upper right corner indicates the general π of PG is significantly lower than the π of PA with ****P < 0.0001 estimated by two-tailed Mann-Whitney U test. Number of samples are indicated on bar. The central lines within the box plots represent the medians, the box represents the interquartile range. The data are presented as the mean ± SEM and the whiskers extend to minima and maxima. b, Difference of π between PA Vs. PG. The gray vertical line indicates the position of SMPED1.

Extended Data Fig. 4 Relative expression level of AmSMPED1 and allele-specific expression analysis.

a, Relative expression level of AmSMPED1 in anthers (left) and styles (right) under natural conditions and continuous illumination (with light exposure after sunset), as determined by RT-qPCR data. The transition point of style reciprocal movement is indicated by the directional arrowheads (see temporal details in Extended Data Fig. 1). The data are presented as the mean ± SEM and the whiskers extend to minima and maxima. Biological replicates (n) of each time point are indicated. b, A synonymous mutation (T Vs. C) is the only difference between recessive allele d and dominant allele D in the coding region. RNA-seq reads are mapped to different alleles to explore the pattern of allele-specific expression of the recessive allele d and dominant allele D. Because expressions of the two alleles are extracted from the same RNA sequences (RNA-seq), the amount of gene expression can be calculated by the number of reads (counts) mapped to the reference allele. c, Allele-specific expressions of recessive allele d and dominant allele D at different times in the PA (recessive homozygosity d/d) and PG (dominant heterozygosity d/D) morphs under different illumination. Allele-specific expression of PA and PG are indicated by different colors. The recessive d and dominant allele D are represented by different dashed lines. Solid lines are the expression of recessive allele d plus dominant allele D.

Extended Data Fig. 5 Expression of other genes related to the DDR.

a, AmCOR27 expression levels in anthers and styles over the course of one day. The left/right panels are from RT-qPCR/ RNA-seq for anthers and styles, respectively. AmCOR27 was not expressed in the PA morph. b, Expression levels of other genes in the DDR. The gray shading indicates the night before sunrise at the location where the plants were cultivated. The data are presented as the mean ± SEM and the whiskers extend to minima and maxima. Biological replicates (n) of each time point are indicated.

Extended Data Fig. 6 Sequence of SMPED, overexpression/knockdown of SMPEDs in Arabidopsis thaliana and validation of promoters.

a, Sequence of AmSMPED1 and its two homologous proteins in Arabidopsis thaliana (At5g67020 and At3g50340). b, Confirmation of overexpression of AmSMPED1 (35S:AmSMPED1), AtSMPED1 (35S:AtSMPED1), and AtSMPED2 (35S:AtSMPED2), as well as simultaneous knockdown of AtSMPED1 and AtSMPED2 (ami-AtSMPED1/2) in A. thaliana. Full-length amplification of AmSMPED1 was then performed, and the results showed that, under identical starting RNA concentrations, the amplified bands from overexpression lines were notably brighter compared to those from wild-type and positive control plants, indicating successful overexpression of AmSMPED1 in the transgenic lines. Overexpression of AmSMPED1 (35S:AmSMPED1) was confirmed by RT-PCR. Total RNA from wild-type plants, positive controls, and transgenic lines was quantified and normalized to the same initial concentration. The data are presented as the mean ± SEM and the whiskers extend to minima and maxima. Biological replicates (n) of each treatment are indicated. The blank space on the bar indicates contracted bar due to large values. The asterisks denote significant differences between samples using two-sided Mann–Whitney U-test. ***, P < 0.0001. c, Validation of promoters in the DDR. The upper diagram is the location of promoters in the DDR. “ATG” is the initiation codon of AmSMPED1. The lower is a diagram for validation. LUC is luciferase and REN is Renilla luciferase. The results of validation are indicated in Fig. 3b.

Source data

Extended Data Fig. 7 In situ hybridization of AmSMPED1 in cross sections of anthers and styles of Alpinia mutica.

The precise localization of AmSMPED1 in the anthers and styles was detected via digoxigenin (DIG)-labeled locked nucleic acid (LNA) oligonucleotide probes. Positive in situ hybridization results are characterized by deep purple signals. The miRCURY LNA miRNA detection probe was used as a negative control. Enlarged photographs are in red-dashed square at the bottom to illustrate detail of in situ hybridization. Red arrowheads indicated localization of AmSMPED1 in the anther and style. For each time point, samples were collected three times with two samples each for a total of six biological replicates at each time point for both anthers and styles. All replicates showed similar results. Each scale bar for anthers is 1 mm and for styles is 100 µm.

Extended Data Fig. 8 Growing status of wild-type (WT) and transgenic lines of Arabidopsis thaliana.

a, Representative photographs of wild-type (WT) Arabidopsis thaliana plants and lines overexpressing or knocked down for AtSMPED1 and/or AtSMPED2 or overexpressing AmSMPED1. WT is the A. thaliana Col-0 accession, 35S:AtSMPED1/2 and 35S:AmSMPED1 are the transgenic A. thaliana plants that overexpress AtSMPED1/2 or AmSMPED1, respectively, and ami-AtSMPED1/2 is a transgenic line in which AtSMPED1 and AtSMPED2 expression levels are knocked down by artificial microRNAs. The scale bar is 1 cm. b, Leaf number on the twenty-first day and bolting rates on the twenty-eighth day. There was no significant difference between WT and transgenic plants in their vegetative traits. The data are presented as the mean ± SEM and the whiskers extend to minima and maxima. Biological replicates (n) are indicated.

Extended Data Fig. 9 Whole-genome duplication events and the phylogenetic tree of dichogamy-determining regions in ginger and related families.

a, Phylogenetic tree of Musaceae and Zingiberaceae species with Oryza sativa and A. thaliana as outgroups. The blue boxes show the divergence time frames. b, Whole-genome duplication and divergence events revealed by Ks distribution. c, Unrooted phylogenetic tree of DDRs in Musaceae and Zingiberaceae species revealing three distinctive types of DDRs.

Extended Data Fig. 10 Numbers of homologous genes in the dichogamy-determining regions (DDR) and their distributions in angiosperms.

Numbers on the outer ring represent the numbers of homologous genes in the DDR indicated in Fig. 2b. Gene symbols (COR27/28, SMPED1, EREBP-like, Unknown, Monothiol glutaredoxin, DNAJB12, Asn/Gln amidotransferase) are represented by lowercases a-h (legend on the upper left). Darker color indicates more numbers of genes (legend on the lower left). The different color on the middle ring represents different plant groups (legend on the upper right). Dots on the node represent bootstrap values and the darker color higher bootstrap values (legend on the lower right). The bolds with underline above the legends indicate where the legend are.

Supplementary information

Supplementary Information

Supplementary Figs. 1 and 2, Tables 1–9 and Methods.

Reporting Summary

Supplementary Video 1

Style movement of the PA morph in a day, related to Fig. 1.

Supplementary Video 2

Style movement of the PG morph in a day, related to Fig. 1.

Source data

Source Data Extended Data Fig. 6

Unprocessed gels for Extended Data Fig. 6b.

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Zhao, JL., Dong, Y., Huang, AD. et al. Ginger genome reveals the SMPED1 gene causing sex-phase synchrony and outcrossing in a flowering plant. Nat. Plants (2025). https://doi.org/10.1038/s41477-025-02125-3

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