Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2020 Mar;6(3):259-272.
doi: 10.1038/s41477-020-0618-2. Epub 2020 Mar 13.

Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

Fay-Wei Li  1   2 , Tomoaki Nishiyama  3 , Manuel Waller  4 , Eftychios Frangedakis  5 , Jean Keller  6 , Zheng Li  7 , Noe Fernandez-Pozo  8 , Michael S Barker  7 , Tom Bennett  9 , Miguel A Blázquez  10 , Shifeng Cheng  11 , Andrew C Cuming  9 , Jan de Vries  12 , Sophie de Vries  13 , Pierre-Marc Delaux  6 , Issa S Diop  4 , C Jill Harrison  14 , Duncan Hauser  15 , Jorge Hernández-García  10 , Alexander Kirbis  4 , John C Meeks  16 , Isabel Monte  17 , Sumanth K Mutte  18 , Anna Neubauer  4 , Dietmar Quandt  19 , Tanner Robison  15   20 , Masaki Shimamura  21 , Stefan A Rensing  8   22   23 , Juan Carlos Villarreal  24   25 , Dolf Weijers  18 , Susann Wicke  26 , Gane K-S Wong  27   28 , Keiko Sakakibara  29 , Péter Szövényi  30   31
Affiliations

Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts

Fay-Wei Li et al. Nat Plants. 2020 Mar.

Abstract

Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole-genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomatal function are conserved in Anthoceros and upregulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Genome organizations in the Anthoceros genomes.
a, Circos plot of A. agrestis Bonn showing the densities of repeats, genes and single nucleotide polymorphisms (SNPs) with the A. agrestis Oxford genomes. b–e, Anthoceros genomes lack whole genome duplication. No self-synteny can be found in the three Anthoceros genomes (A. agrestis Bonn (b), A. agrestis Oxford (c) and A. punctatus (d)) nor in M. polymorpha (e). f, P. patens, on the other hand, shows a clear 1:1 and some 1:2 syntenic relationship, suggesting paleopolyploidy. In b–f, the bar graphs show the proportion of the genome at different self syntenic levels, with the dot-plots on the right.
Fig. 2
Fig. 2. Land plant phylogeny inferred from 742 mostly single-copy genes.
The monophyly of bryophytes is supported. The topology shown here is based on the maximum likelihood tree from the concatenated amino acid dataset. Thickened branches received maximal (100) bootstrap and SH-aLRT supports from both the concatenated nucleotide and amino acid datasets, as well as maximal posterior probabilities (1.0) from the Astral species-tree analysis (based on both nucleotide and amino acid gene trees). The inset shows the quartet frequencies among the 742 gene trees supporting monophyletic bryophytes (T1) versus two alternative placements of hornworts (T2 and T3). The dotted line shows the one-third threshold.
Fig. 3
Fig. 3. TAPs and sporophyte development.
a, The Anthoceros genomes have the smallest TAP repertoire among land plants. b, Sporophytes (red arrowhead) and gametophytes (blue arrow) of A. agrestis Bonn. c, Stomata of A. agrestis Bonn. d, Gene expression profiles across different developmental stages in A. agrestis Bonn (n = 12 biologically independent samples; two-sided test for differential expression, false-discovery rate ≤0.05 and log2-fold-change ≥2). wk, week; mo, month.
Fig. 4
Fig. 4. Evolution and genetics of symbiosis in hornworts.
a, Orthologues of AMF symbiosis pathway genes can be found in hornworts, indicating their presence in the common ancestor of land plants. The asterisk indicates that the M. paleacea transcriptome was searched instead of M. polymorpha genome because the latter secondarily lost AMF. b, RAM1 is upregulated during nitrogen starvation in both A. agrestis and A. punctatus. c, Reconstituted Anthoceros–cyanobacteria symbiosis. Arrowhead points to a cyanobacteria colony. d, Transcriptomic responses to nitrogen starvation and cyanobacterial symbiosis in A. agrestis (n = 9 biologically independent samples). PC1 and PC2 refer to the first and second axes of principal component analysis on gene expression values. e, A suite of genes were highly upregulated under symbiosis in both A. agrestis and A. punctatus (two-sided test for differential expression, false-discovery rate ≤0.05 and log2-fold-change >4).
Fig. 5
Fig. 5. Relationship between LCIB and pyrenoid-based CCM.
a, Phylogeny of LCIB. Numbers above branches are bootstrap support values (branches thickened when bootstrap >70). b, Hornwort LCIBs have conserved amino acid residues at the active site. Yellow and green arrowheads point to the zinc-binding and catalytic residues, respectively. K.n., K. nitens; C.r., C. reinhardtii; O.l., Ostreococcus lucimarinus.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Morris JL, et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA. 2018;115:E2274–E2283. - PMC - PubMed
    1. Nishiyama T, et al. Chloroplast phylogeny indicates that bryophytes are monophyletic. Mol. Biol. Evol. 2004;21:1813–1819. - PubMed
    1. Wickett NJ, et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl Acad. Sci. USA. 2014;111:E4859–E4868. - PMC - PubMed
    1. Puttick MN, et al. The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 2018;28:733–745. - PubMed
    1. de Sousa F, Foster PG, Donoghue PCJ, Schneider H, Cox CJ. Nuclear protein phylogenies support the monophyly of the three bryophyte groups (Bryophyta Schimp) New Phytol. 2019;222:565–575. - PubMed

Publication types