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The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution

Nature Plants volume 7, pages 748–756 (2021)Cite this article

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Abstract

Gymnosperms are a unique lineage of plants that currently lack a high-quality reference genome due to their large genome size and high repetitive sequence content. Here, we report a nearly complete genome assembly for Ginkgo biloba with a genome size of 9.87 Gb, an N50 contig size of 1.58 Mb and an N50 scaffold size of 775 Mb. We were able to accurately annotate 27,832 protein-coding genes in total, superseding the inaccurate annotation of 41,840 genes in a previous draft genome assembly. We found that expansion of the G. biloba genome, accompanied by the notable extension of introns, was mainly caused by the insertion of long terminal repeats rather than the recent occurrence of whole-genome duplication events, in contrast to the findings of a previous report. We also identified candidate genes in the central pair, intraflagellar transport and dynein protein families that are associated with the formation of the spermatophore flagellum, which has been lost in all seed plants except ginkgo and cycads. The newly obtained Ginkgo genome provides new insights into the evolution of the gymnosperm genome.

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Fig. 1: Features of 12 pseudochromosomes of G. biloba.
Fig. 2: Analyses of gene family evolution and WGD events.
Fig. 3: Analysis of genes involved in leaf polarity.

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Data availability

The G. biloba genome project has been deposited at the National Genomics Data Center under BioProject no. PRJCA001755. Whole-genome sequencing data were deposited in the Genome Sequence Archive database under accession nos. CRA002032 and CRA002041. Source data are provided with this paper.

Code availability

All custom codes are available for research purposes from the corresponding authors upon request.

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Acknowledgements

This work was funded by the Key Forestry Public Welfare Project (grant no. 201504105 to G.W.), the National Key R&D Programme of China (grant no. 2019YFA0707003 to J.R.), the Natural Science Foundation of China (grant no. 31822029 to J.R.) and the Guangdong Basic and Applied Basic Research Foundation (grant no. 2019A1515111150 to B.H.).

Author information

Author notes

  1. These authors contributed equally: Hailin Liu, Xiaobo Wang, Guibin Wang, Peng Cui.

Authors and Affiliations

  1. The Southern Modern Forestry Collaborative Innovation Center, the Key Lab of Tree Genetics and Biotechnology of Educational Department of China and the Key Lab of Tree Genetics and Silvicultural Sciences of Jiangsu Province, Nanjing Forestry University, Nanjing, China

    Hailin Liu, Guibin Wang, Nan Hu, Jing Hou, Xiaogang Dai, Tongming Yin & Fuliang Cao

  2. Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Hailin Liu, Xiaobo Wang, Peng Cui, Shigang Wu, Cheng Ai, Alun Li, Bing He, Xiujuan Shao, Zhichao Wu, Hu Feng, Yuxiao Chang, Desheng Mu & Jue Ruan

  3. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi University, Nanning, China

    Xiaobo Wang

  4. Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA

    Nan Hu

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Contributions

F.C., T.Y. and J.R. conceived this research. F.C., T.Y., J.R., G.W., P.C. and H.L. designed the experiments. H.L., G.W., N.H., J.H., B.H. and X.D. collected samples. H.L., N.H. and Y.C. performed DNA/RNA extraction. J.R. and S.W. performed genome assembly. C.A. and H.L. contributed to RNA-seq and the corresponding analysis. X.W., S.W., C.A., A.L. and Z.W. assessed the genome assembly. C.A. characterized the repeat content. X.W., C.A., X.S., H.F. and D.M. performed gene annotation. X.W. conducted gene family classification. X.W. and H.L. conducted synteny analyses. X.W. and C.A. performed analysis of LTR elements. H.L. and X.W. carried out analysis of phenotypic traits. H.L., X.W., G.W. and P.C. wrote most of the manuscript. T.Y., J.R. and F.C. organized and edited the manuscript.

Corresponding authors

Correspondence to Tongming Yin, Jue Ruan or Fuliang Cao.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Sequential inversion of a 170-Mb region at the terminus of chromosome 11 revealed by a genetic map.

The black columns represent the linkage groups of the genetic map; the grey columns represent the pseudochromosomes.

Source data

Extended Data Fig. 2 Assessment of gene set completeness by BUSCO.

The species involved were labelled along the x axis. The y axis represents the percentage of the coverage of complete gene models (pink), fragmented gene models (orange) and uncovered genes (yellow) in each species.

Extended Data Fig. 3 Self-alignment dotplot based on syntenic gene pairs.

The one-to-one syntenic blocks are highlighted with red circles. The blue shadow was used to mask the same alignment in unshadowed regions.

Extended Data Fig. 4 WGD event revealed by Bayesian inference of retention rates of plants.

Inference is based on 2,841 gene families. The q value along the x axis represents the retention rate. Based on the distribution of q values, no Ginkgo lineage-specific or gymnosperm-specific WGD was detected, while seed plant WGD (ζ WGD) was confirmed. We set the iteration value to 1,000 during the Hamiltonian Monte Carlo sampling process recommended by the developers.

Extended Data Fig. 5 Timing of LTR-RT insertions in different gymnosperms.

Insertion time was calculated based on sequence identity of LTRs identified in each genome assembly. The X-axis displays the insertion time (Mya), and the Y-axis represents the ratio of LTR elements in windows of every 4 Mya.

Supplementary information

Supplementary Information

Supplementary Tables 1–12, 14 and 15 and Figs. 1–8.

Reporting Summary

Supplementary Table 13

Ks values calculated against 25 species for homologous genes in protein categories including radial spoke proteins, central pair proteins, intraflagellar transport proteins, inner dyneins, outer dyneins and dyneins.

Source data

Source Data Fig. 2

Statistical source data for Fig. 2b.

Source Data Extended Data Fig. 1

Statistical source data for Extended Data Fig. 1.

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Liu, H., Wang, X., Wang, G. et al. The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution. Nat. Plants 7, 748–756 (2021). https://doi.org/10.1038/s41477-021-00933-x

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