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The genome of homosporous maidenhair fern sheds light on the euphyllophyte evolution and defences

Nature Plants volume 8, pages 1024–1037 (2022)Cite this article

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Abstract

Euphyllophytes encompass almost all extant plants, including two sister clades, ferns and seed plants. Decoding genomes of ferns is the key to deep insight into the origin of euphyllophytes and the evolution of seed plants. Here we report a chromosome-level genome assembly of Adiantum capillus-veneris L., a model homosporous fern. This fern genome comprises 30 pseudochromosomes with a size of 4.8-gigabase and a contig N50 length of 16.22 Mb. Gene co-expression network analysis uncovered that homospore development in ferns has relatively high genetic similarities with that of the pollen in seed plants. Analysing fern defence response expands understanding of evolution and diversity in endogenous bioactive jasmonates in plants. Moreover, comparing fern genomes with those of other land plants reveals changes in gene families important for the evolutionary novelties within the euphyllophyte clade. These results lay a foundation for studies on fern genome evolution and function, as well as the origin and evolution of euphyllophytes.

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Fig. 1: Life cycle and intra-gametophytic selfing of A. capillus-veneris.
Fig. 2: A. capillus-veneris de novo genome assembly.
Fig. 3: Expression profile and gene network analysis during homosporangium development.
Fig. 4: JA biosynthesis pathway and defence-related metabolites in A. capillus-veneris.
Fig. 5: Gene family dynamics enabling adaptive features in euphyllophytes.
Fig. 6: BRI1-BRL gene family evolution.

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Data availability

The A. capillus-veneris genome assembly, genome annotation and all the raw sequencing data have been deposited at NCBI, under the BioProject accession number PRJNA593372 (genome assembly and annotation) and PRJNA593361 (transcriptome raw sequence data). The CDS and peptide files are available from https://figshare.com/s/47be9fe90124b22d3c0e. The referenced dataset for Arabidopsis LEC1 co-expression analysis is under the accessions: https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE12404 (DOI: 10.1073/pnas.1707957114). 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

We thank X. Zhang (Institute of Botany, Chinese Academy of Sciences) for providing helpful advice and suggestions, G. Rao (Peking University) for providing the homozygous A. capillus-veneris plant and DNA sequencing sample, Y. Wu (AGIS, CAAS) for providing the lncRNA determination pipeline, J. Zhao (Boyce Thompson Institute) for converting the references to a uniform format, and W. Wang and L. Xu (Tsinghua University) for assistance with phytohormone and metabolites detection. This work was supported by the National Key Research and Development Program of China (grant no. 2019YFA0906200 to S.H.); Science, Technology and Innovation Commission of Shenzhen Municipality (grant no. ZDSYS20200811142605017 to J.Y.); the Elite Young Scientists Program of CAAS (to J.Y.); the Agricultural Science and Technology Innovation Program (to J.Y.); the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant no. 833522 to Y.V.d.P.); Methusalem funding from Ghent University (grant no. BOF.MET.2021.0005.01 to Y.V.d.P.); a postdoctoral fellowship from the Special Research Fund of Ghent University (grant no. BOFPDO2018001701 to Z.L.); and the Research Foundation – Flanders (FWO) (grant no. 3G032219 to H.C.).

Author information

Author notes

  1. These authors contributed equally: Yuhan Fang, Xing Qin, Qinggang Liao, Ran Du.

Authors and Affiliations

  1. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Yuhan Fang, Xing Qin, Qinggang Liao, Ran Du, Xizhi Luo, Qian Zhou, Pengbo Sun, Li Wang, Shifeng Cheng, Xingtan Zhang, William John Lucas, Sanwen Huang & Jianbin Yan

  2. Peng Cheng Laboratory, Artificial Intelligence Research Center, Shenzhen, China

    Qian Zhou

  3. Department of Plant Biotechnology and Bioinformatics, Ghent University and VIB Center for Plant Systems Biology, Ghent, Belgium

    Zhen Li, Hengchi Chen & Yves Van de Peer

  4. State Key Laboratory of Protein and Plant Gene Research, Quantitative Biology Center, College of Life Sciences, Peking University, Beijing, China

    Wanting Jin, Yaning Yuan & Shunong Bai

  5. Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, China

    Rui Zhang & Jiao Zhang

  6. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China

    Xueyong Yang & Zhonghua Zhang

  7. The Orchid Conservation and Research Centre of Shenzhen, Shenzhen, China

    Yuehong Yan

  8. College of Horticulture, Qingdao Agricultural University, Qingdao, China

    Zhonghua Zhang

  9. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, China

    Yves Van de Peer

  10. Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa

    Yves Van de Peer

  11. Department of Plant Biology, College of Biological Sciences, University of California, Davis, CA, USA

    William John Lucas

Authors
  1. Yuhan Fang
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  2. Xing Qin
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  3. Qinggang Liao
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  4. Ran Du
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  5. Xizhi Luo
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  6. Qian Zhou
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  7. Zhen Li
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  8. Hengchi Chen
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  9. Wanting Jin
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  10. Yaning Yuan
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  11. Pengbo Sun
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  12. Rui Zhang
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  13. Jiao Zhang
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  14. Li Wang
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  15. Shifeng Cheng
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  16. Xueyong Yang
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  17. Yuehong Yan
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  18. Xingtan Zhang
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  19. Zhonghua Zhang
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  20. Shunong Bai
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  21. Yves Van de Peer
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  22. William John Lucas
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  23. Sanwen Huang
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  24. Jianbin Yan
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Contributions

S.H., S.B., Y.F. and J.Y. conceived the study. Y.F. and J.Y. designed and managed the major scientific objectives. S.H., Y.F., W.J.L. and J.Y. coordinated the project. Y.F., W.J., Y. Yuan, L.W., X.Y. and X.Q. managed the plant materials. Q.Z. and P.S. assembled the genome and estimated the genome size. Y.F., Q.L., X.L., X.Q., Q.Z., P.S., L.W. and Z.Z. annotated the genomes. H.C., Z.L. and Y.V.d.P performed the WGD calling. Y.F., Q.L. and X.L. identified the repetitive elements, non-coding RNAs and lncRNAs. Y.F., Q.L., Y. Yan, R.Z., J.Z. and S.C. clustered the gene families and conducted the related phylogenetic analysis. Y.F. and Q.L. constructed the co-expression network of AdcLEC1. Y.F., Q.L., X.Q. and X.L. carried out the RNA-seq analysis on homosporous development and jasmonate biosynthesis genes. J.Y. and R.D. performed the jasmonate biosynthesis and signalling analyses. R.D., Y.F., W.J. and Y. Yuan contributed to hormone and metabolome sample preparation. R.D. carried out metabolome detection and characterized the function of coronatine-inducible metabolites. Y.F. and J.Y. led the article preparation, together with S.H., W.J.L., Y.V.d.P., Q.L., R.D., Z.L., X.Q., X.L. and X.Z. All authors read and approved the final article.

Corresponding authors

Correspondence to Yuhan Fang or Jianbin Yan.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Yuannian Jiao, Fay-Wei Li and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Analyses of whole genome duplication (WGD) events.

a, Self-alignment dot plot based on paralogous pairs in collinear blocks. b, The distribution of KS of the whole paranome in A. capillus-veneris. c, The distribution of KS of the syntenic paralogous pairs in A. capillus-veneris. d, The analysis of ksrates for the whole paranome of A. capillus-veneris before rate adjustment. Light grey histogram and kernel density estimation (KDE) curve are plotted for the whole paranome KS distribution. The estimated mean mode and standard deviation from 200 bootstrapped KDEs of each orthologous distribution between A. capillus-veneris and other species is shown as dashed red lines and boxes with corresponding KS values denoted in the legend. e, The analysis of ksrates for the whole paranome of A. capillus-veneris after rate adjustment. The whole paranome KS distributions are overlaid with rate-adjusted divergence events in coloured vertical lines and boxes. The overall mixture model in the dark solid KDE curve consists of an exponential component in dotted grey curve and optimized log-normal components in dashed grey curves. Each log-normal component is labelled with a letter, shown as vertical dashed grey lines with circular labels. Rate-adjusted mode estimates of orthologous KS distributions between A. capillus-veneris and other species, representing speciation events, are drawn as numbered vertical long-dashed lines and associated coloured boxes showing the mean and the standard deviation. Lines representing the same speciation event in the phylogeny share colour and numbering while here only one speciation event is involved with A. capillus-veneris. Horizontal arrows in figure legends ‘divergence with’ part indicate the KS shifts resulted from the substitution rate adjustments. f, The analysis of ksrates for anchor pairs of A. capillus-veneris after rate adjustment. The KS distributions of two anchor pair clusters, namely a and b in filled blue and red KDE curves with associated peak, derived from the lognormal mixture modeling of median KS values for the collinear segment pairs, are shown as a grey histogram. Rate-adjusted mode estimates of orthologous KS distributions between A. capillus-veneris and other species, representing speciation events, are drawn as numbered vertical long-dashed lines, and associated coloured boxes showing the mean and the standard deviation. Lines representing the same speciation event in the phylogeny share colour and numbering while here only one speciation event is involved with A. capillus-veneris. Horizontal arrows in figure legends ‘divergence with’ part indicate the KS shifts resulted from the substitution rate adjustments.

Extended Data Fig. 2 Comparison of the genome features of A. capillus-veneris with those of A. filiculoides and S. cucullata.

a, Lengths of different repeat components in the indicated eight representative species across land plants. b, Distributions of nucleotide distance (D) calculated for LTR among three ferns, A. capillus-veneris, A. filiculoides and S. cucullata. c, Violet plot showing gene characteristics of ferns. The upper and lower edge of white frame in the violin plot represent the 75% and 25% quartiles, the central line denotes the median value, and the black square shows the mean value. The upper and lower terminal of line in the violin indicated the upper adjacent value and lower adjacent value, 1.5 × the interquartile range and outliers (solid points).

Extended Data Fig. 3 Time course of the mechanical wound-induced response of JA in Ginkgo biloba.

Leaves of G. biloba were wounded with a hemostat. Damaged leaves were harvested at the indicated time points after wounding and analysed for jasmonates (the precursor OPDA [▲], jasmonic acid (JA) [●], and JA-Ile [■]) accumulation by HPLC-MS; each data point represents the mean ± SD of five biological replicates.

Extended Data Fig. 4 The maximum-likelihood tree of the BRI1-BRL and EMS1 gene family in land plants.

The domains of BRI1-BRL (TM, LRR, ID, and KD) and its closest gene family EMS1 (TM, LRR, and KD) were identified from all main land plant groups (in different colours). Maximum-likelihood tree was constructed with parameters: WAG + F + R6 model and 1,000 bootstrap replicates. Whole genome assemblies from 24 species were used for identification of BRI1-BRL and EMS1 homologs, including 9 bryophytes (Mpo, Marchantia polymorpha; Cpl, Calohypnum plumiforme; Fan, Fontinalis antipyretica; Cpu, Ceratodon purpureus; Ppa, Physcomitrella patens; Psc, Pleurozium schreberi; Aan, Anthoceros angustus; Aag, Anthoceros agrestis; Apu, Anthoceros punctatus), 3 lycophytes (Ita, Isoetes taiwanensis; Smo, Selaginella moellendorffii; Sle, Selaginella lepidophylla), 3 ferns (Adc, Adiantum capillus-veneris; Afi, Azolla filiculoides; Scu, Salvinia cucullata), and 9 seed plants (Pab, Picea abies; Pta, Pinus taeda; Gbi, Ginkgo biloba; Ath, Arabidopsis thaliana; Atr, Amborella trichopoda; Csa, Cucumis sativus; Osa, Oryza sativa; Vvi, Vitis vinifera; Zma, Zea mays). The detailed information is provided in Supplementary Data 19.

Extended Data Fig. 5 The island domain of the BRI1-BRL gene family in land plant.

The island domains were extracted from peptide of BRI1-BRL homologues and aligned by MUSCLE. The conserved sites were indicated with red boxes.

Supplementary information

Supplementary Information

Supplementary Text, Figs. 1–5 and Tables 1–14.

Reporting Summary

Supplementary Data 1

Supplementary Data 1–20.

Source data

Source Data Fig. 3

Statistical source data for Fig. 3b,c.

Source Data Fig. 4

Statistical source data for Fig. 4d,e.

Source Data Fig. 5

Statistical source data for Fig. 5.

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Fang, Y., Qin, X., Liao, Q. et al. The genome of homosporous maidenhair fern sheds light on the euphyllophyte evolution and defences. Nat. Plants 8, 1024–1037 (2022). https://doi.org/10.1038/s41477-022-01222-x

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