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Origin of angiosperms and the puzzle of the Jurassic gap

Abstract

Angiosperms are by far the most species-rich clade of land plants, but their origin and early evolutionary history remain poorly understood. We reconstructed angiosperm phylogeny based on 80 genes from 2,881 plastid genomes representing 85% of extant families and all orders. With a well-resolved plastid tree and 62 fossil calibrations, we dated the origin of the crown angiosperms to the Upper Triassic, with major angiosperm radiations occurring in the Jurassic and Lower Cretaceous. This estimated crown age is substantially earlier than that of unequivocal angiosperm fossils, and the difference is here termed the ‘Jurassic angiosperm gap’. Our time-calibrated plastid phylogenomic tree provides a highly relevant framework for future comparative studies of flowering plant evolution.

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Fig. 1: Dated phylogenetic tree showing relationships among orders of angiosperms based on a maximum likelihood partitioned analysis of 82,286 bp of DNA sequence from 80 genes of 2,881 plastomes.
Fig. 2: Angiosperm ordinal phylogenetic relationships in PPA (based on the complete 80-gene matrix) versus APG IV.
Fig. 3: Sorted ordinal and interordinal node age estimates using TreePL based on the phylogenetic trees of 80 genes of 2,881 angiosperm plastomes with maximum likelihood analysis.
Fig. 4: Dated family-level angiosperm phylogenetic tree based on 80 genes of 2,881 plastomes with maximum likelihood analysis.

Data availability

Sequence alignments underlying analyses and all trees are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.bq091cg.

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Acknowledgements

We thank the Germplasm Bank of Wild Species at the Kunming Institute of Botany (KIB) for facilitating this study; the curators and staff of the Beijing Botanical Garden (BG), Blue Mountains BG, Brisbane BG, Kunming BG, Missouri BG, Wuhan BG, Royal BG Edinburgh, RBG Kew, RBG Sydney, RBG Victoria (both Melbourne and Cranbourne), San Francisco BG, Shanghai Chenshan BG, South China BG, UC Berkeley BG, Xianhu BG Shenzhen, Xishuangbanna Tropical BG, Yinchuan BG and O. Maurin (Johannesburg, now Kew), J. R. Shevock (California), Y.-M. Shui (Kunming), and N. Zamora (Costa Rica) for samples; and S. R. Manchester (Florida) for critical discussion on fossil selection and calibration. This work was funded by the Strategic Priority Research Programme of the Chinese Academy of Sciences (CAS) (grant No. XDB31000000 to D.-Z.L.), CAS’ Large-scale Scientific Facilities (grant No. 2017-LSF-GBOWS-02 to D.-Z.L. and J.-B.Y.), KIB’s iFlora initiative (grant No. 2014-4-11 to D.-Z.L.) and the National Natural Science Foundation of China (grant No. 31570333 to H.-T.L.). P.-F.M. was supported by CAS’ Youth Innovation Promotion Association (grant No. 2015321) and P.S.S. was supported by the Ten Thousand Talents Programme of China and the Yunling International High-end Experts Programme of Yunnan Province.

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D.-Z.L, J.-B.Y., H.-T.L., T.-S.Y., D.E.S. and P.S.S. conceived the project and designed the research. T.-S.Y., T.Z., J.C., L.-M.G. and S.-D.Z. designed and carried out field collection work. Q.-F.W., J.W., P.W.F., M.v.d.B., P.M.H. and M.W.C. provided and/or collected samples. J.-B.Y., H.-T.L., Z.-R.Z., C.-N.F. and J.Y. performed DNA laboratory work. M.A.G., D.E.S. and P.S.S. prepared the OneKP dataset. H.-T.L., L.-M.G., T.-S.Y., P.-F.M., D.E.S. and P.S.S. designed and coordinated computational analyses. H.-T.L., T.Z., J.C., Y.L. and H.W. prepared the Figures and Tables. T.-S.Y., Y.L., L.-M.G., P.-F.M., D.-Z.L. and H.W. wrote the supplementary information. D.-Z.L., T.-S.Y., L.-M.G., P.-F.M. and P.W.F. wrote the first manuscript draft with input from all co-authors, particularly P.S.S., M.W.C., D.E.S. and P.M.H.

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Correspondence to Pamela S. Soltis or De-Zhu Li.

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Journal peer review information: Nature Plants thanks Jennifer Mandel and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Information

Supplementary Text and Supplementary Figures 1–6.

Reporting Summary

Supplementary Table 1

Species sampled, including 1,659 newly sequenced samples for this study.

Supplementary Table 2

The details of removal of most rapidly evolving sites using Gblocks.

Supplementary Table 3

Ordinal and interordinal node age estimates using treePL based on the phylogenetics trees of 80 plastid genes of 2,881 samples with ML analysis.

Supplementary Table 4

Familial and interfamilial node age estimates using treePL based on the phylogenetics trees of 80 plastid genes of 2,881 samples with ML analysis.

Supplementary Table 5

Families age estimates using treePL based on the phylogenetics trees of 80 plastid genes of 2,881 samples with ML analysis.

Supplementary Data

The configuration file for running the software TreePL.

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Li, HT., Yi, TS., Gao, LM. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5, 461–470 (2019). https://doi.org/10.1038/s41477-019-0421-0

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