The hornwort genome and early land plant evolution

doi:10.1038/s41477-019-0588-4

. 2020 Feb;6(2):107-118.

doi: 10.1038/s41477-019-0588-4. Epub 2020 Feb 10.

The hornwort genome and early land plant evolution

Jian Zhang^#¹, Xin-Xing Fu^#^{1

2}, Rui-Qi Li^#¹, Xiang Zhao^#³, Yang Liu^#^{4

5}, Ming-He Li^#⁶, Arthur Zwaenepoel^#^{7

8}, Hong Ma⁹, Bernard Goffinet¹⁰, Yan-Long Guan¹¹, Jia-Yu Xue¹², Yi-Ying Liao^{4

13}, Qing-Feng Wang¹³, Qing-Hua Wang¹, Jie-Yu Wang^{6

14}, Guo-Qiang Zhang⁶, Zhi-Wen Wang³, Yu Jia¹, Mei-Zhi Wang¹, Shan-Shan Dong⁴, Jian-Fen Yang⁴, Yuan-Nian Jiao¹, Ya-Long Guo¹, Hong-Zhi Kong¹, An-Ming Lu¹, Huan-Ming Yang⁵, Shou-Zhou Zhang¹⁵, Yves Van de Peer^{16

17

18

19}, Zhong-Jian Liu^{20

21

22}, Zhi-Duan Chen^{23

24}

Affiliations

¹ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.
² University of Chinese Academy of Sciences, Beijing, China.
³ PubBio-Tech Services Corporation, Wuhan, China.
⁴ Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Science, Shenzhen, China.
⁵ BGI-Shenzhen, Shenzhen, China.
⁶ Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, China.
⁷ Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
⁸ VIB Center for Plant Systems Biology, Ghent, Belgium.
⁹ Department of Biology, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, USA.
¹⁰ Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA.
¹¹ Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China.
¹² Center for Plant Diversity and Systematics, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, China.
¹³ Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, China.
¹⁴ College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, China.
¹⁵ Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Science, Shenzhen, China. shouzhouz@126.com.
¹⁶ Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium. yves.vandepeer@psb.vib-ugent.be.
¹⁷ VIB Center for Plant Systems Biology, Ghent, Belgium. yves.vandepeer@psb.vib-ugent.be.
¹⁸ Center for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, Pretoria, South Africa. yves.vandepeer@psb.vib-ugent.be.
¹⁹ College of Horticulture, Nanjing Agricultural University, Nanjing, China. yves.vandepeer@psb.vib-ugent.be.
²⁰ Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, China. zjliu@fafu.edu.cn.
²¹ College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, China. zjliu@fafu.edu.cn.
²² Fujian Colleges and Universities Engineering Research Institute of Conservation and Utilization of Natural Bioresources, College of Forestry, Fujian Agriculture and Forestry University, Fuzhou, China. zjliu@fafu.edu.cn.
²³ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China. zhiduan@ibcas.ac.cn.
²⁴ Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, China. zhiduan@ibcas.ac.cn.

^# Contributed equally.

PMID: 32042158
PMCID: PMC7027989
DOI: 10.1038/s41477-019-0588-4

The hornwort genome and early land plant evolution

Jian Zhang et al. Nat Plants. 2020 Feb.

. 2020 Feb;6(2):107-118.

doi: 10.1038/s41477-019-0588-4. Epub 2020 Feb 10.

Authors

Affiliations

¹ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China.
² University of Chinese Academy of Sciences, Beijing, China.
³ PubBio-Tech Services Corporation, Wuhan, China.
⁴ Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Science, Shenzhen, China.
⁵ BGI-Shenzhen, Shenzhen, China.
⁶ Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, China.
⁷ Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
⁸ VIB Center for Plant Systems Biology, Ghent, Belgium.
⁹ Department of Biology, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, USA.
¹⁰ Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA.
¹¹ Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China.
¹² Center for Plant Diversity and Systematics, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, China.
¹³ Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, China.
¹⁴ College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, China.
¹⁵ Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Science, Shenzhen, China. shouzhouz@126.com.
¹⁶ Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium. yves.vandepeer@psb.vib-ugent.be.
¹⁷ VIB Center for Plant Systems Biology, Ghent, Belgium. yves.vandepeer@psb.vib-ugent.be.
¹⁸ Center for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, Pretoria, South Africa. yves.vandepeer@psb.vib-ugent.be.
¹⁹ College of Horticulture, Nanjing Agricultural University, Nanjing, China. yves.vandepeer@psb.vib-ugent.be.
²⁰ Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, China. zjliu@fafu.edu.cn.
²¹ College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, China. zjliu@fafu.edu.cn.
²² Fujian Colleges and Universities Engineering Research Institute of Conservation and Utilization of Natural Bioresources, College of Forestry, Fujian Agriculture and Forestry University, Fuzhou, China. zjliu@fafu.edu.cn.
²³ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China. zhiduan@ibcas.ac.cn.
²⁴ Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan, China. zhiduan@ibcas.ac.cn.

^# Contributed equally.

PMID: 32042158
PMCID: PMC7027989
DOI: 10.1038/s41477-019-0588-4

Abstract

Hornworts, liverworts and mosses are three early diverging clades of land plants, and together comprise the bryophytes. Here, we report the draft genome sequence of the hornwort Anthoceros angustus. Phylogenomic inferences confirm the monophyly of bryophytes, with hornworts sister to liverworts and mosses. The simple morphology of hornworts correlates with low genetic redundancy in plant body plan, while the basic transcriptional regulation toolkit for plant development has already been established in this early land plant lineage. Although the Anthoceros genome is small and characterized by minimal redundancy, expansions are observed in gene families related to RNA editing, UV protection and desiccation tolerance. The genome of A. angustus bears the signatures of horizontally transferred genes from bacteria and fungi, in particular of genes operating in stress-response and metabolic pathways. Our study provides insight into the unique features of hornworts and their molecular adaptations to live on land.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Fig. 1. Comparative genomic analysis of *A. angustus* and 18 other plant species.**
a, Comparison of the number of gene families identified by OrthoMCL. The Venn diagram shows the shared and unique gene families in *A. angustus*, Setaphyta, Tracheophyta, Charophyta and Chlorophyta. The gene-family number is listed in each of the components. b, Gene-family gain (+)/loss (−) among 19 green plants. The numbers of gained (blue) and lost (red) gene families are shown above the branches. The boxed number indicates the gene-family size at each node. The number of gene families, orphans (single-copy gene families) and number of predicted genes is indicated next to each species. c, Comparison of whole paranome, anchor pair and one-to-one orthologue distribution of the number of synonymous substitutions per synonymous site (K_S) across the three bryophyte species (*P. patens*, *M. polymorpha* and *A. angustus*).

**Fig. 2. Major TFs for plant body plan and evolutionary innovations within plants.**
a, Overview for the number of major TFs for plant body plan in ten green plants. Colour key on the upper left of the heatmap denotes the TF numbers. b, Major innovations in plants and evolutionary features of three bryophyte lineages.

**Fig. 3. Expansion of *cupin* gene family in *A. angustus*.**
a, A summary of the number of *cupin* genes from nine species based on a Pfam search of cupin_1 domain (PF00190). b,c, Phylogenetic trees show *cupin* genes in nine plant genomes: *bicupins* (b) and *monocupins* (c). The colour of each branch corresponds to the background colour for each species in a. The tandem duplicated gene clusters are ordered and shown on scaffolds of the *A. angustus* genome. The scale bars in the trees show the number of amino acid substitutions per site.

**Fig. 4. Phylogenetic affinities of genes horizontally transferred to *A. angustus*.**
a, Phylogenetic tree of glyoxalase (PF13468). b, Phylogenetic tree of NAD-binding dehydrogenase (PF08635). c, Phylogenetic tree of glucuronyl hydrolase (PF07470). d, Phylogenetic tree of DNA methyltransferase (PF02870 and PF01035). The stars indicate that the *Anthoceros* sequence or bryophyte sequences formed a monophyletic clade with homologues of putative HGT donor, reflecting *Anthoceros*-specific or bryophyte-specific HGT events. Maximum-likelihood bootstrap support values ≥50% are shown above the branches. Red, hornworts and other bryophytes; cyan, green algae; grey, metazoan; orange, stramenopiles; blue, bacteria; yellow, fungi; purple, archaea. The homologues from the kingdom other than the one that HGT donors are involved in are used as the outgroup. The scale bars in the trees show the number of amino acid substitutions per site.

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References

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[1] Puttick MN, et al. The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 2018;28:733–745. doi: 10.1016/j.cub.2018.01.063. - DOI - PubMed

[2] Puttick MN, et al. The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 2018;28:733–745. doi: 10.1016/j.cub.2018.01.063. - DOI - PubMed

[3] Goffinet, B. & Buck, W. R. in The Evolution of Plant Form (eds Ambrose, B. & Purruganan, M.) 51–90 (Wiley–Blackwell, 2013).

[4] Goffinet, B. & Buck, W. R. in The Evolution of Plant Form (eds Ambrose, B. & Purruganan, M.) 51–90 (Wiley–Blackwell, 2013).

[5] von Konrat M, Shaw AJ, Renzaglia KS. A special issue of Phytotaxa dedicated to bryophytes: the closest living relatives of early land plants. Phytotaxa. 2010;9:5–10. doi: 10.11646/phytotaxa.9.1.3. - DOI

[6] von Konrat M, Shaw AJ, Renzaglia KS. A special issue of Phytotaxa dedicated to bryophytes: the closest living relatives of early land plants. Phytotaxa. 2010;9:5–10. doi: 10.11646/phytotaxa.9.1.3. - DOI

[7] Christenhusz MJM, Byng JW. The number of known plants species in the world and its annual increase. Phytotaxa. 2016;261:201–217. doi: 10.11646/phytotaxa.261.3.1. - DOI

[8] Christenhusz MJM, Byng JW. The number of known plants species in the world and its annual increase. Phytotaxa. 2016;261:201–217. doi: 10.11646/phytotaxa.261.3.1. - DOI

[9] Qiu YL, et al. The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA. 2006;103:15511–15516. doi: 10.1073/pnas.0603335103. - DOI - PMC - PubMed

[10] Qiu YL, et al. The deepest divergences in land plants inferred from phylogenomic evidence. Proc. Natl Acad. Sci. USA. 2006;103:15511–15516. doi: 10.1073/pnas.0603335103. - DOI - PMC - PubMed

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The hornwort genome and early land plant evolution

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The hornwort genome and early land plant evolution

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