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.

Highlights

  • Land plants evolved from a charophycean algal ancestor 470– 515 million years ago[1] and contributed to the greening of the terrestrial environment

  • The hornwort genomes presented here offer a unique window into the biology of land plant most recent common ancestor (MRCA)

  • The Anthoceros genomes lack KNOX1, while P. patens and M. polymorpha lack YABBY genes. This suggests that the MRCA of land plants had both of these key developmental genes and independent gene losses occurred in different bryophyte lineages

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Summary

Introduction

Land plants evolved from a charophycean algal ancestor 470– 515 million years ago[1] and contributed to the greening of the terrestrial environment. The extant land plants consist of vascular plants and three bryophyte lineages—mosses, liverworts and hornworts. As the earliest diverging lineage in bryophytes, are crucial to infer character evolution and reveal the nature of the MRCA of bryophytes and that of land plants. Hornworts uniquely possess a combination of traits that connect them with both green algae and other land plant lineages[9]. Most hornworts have a single chloroplast per cell with a pyrenoid capable of carrying out a carbon-concentrating mechanism (CCM)[10]. Such pyrenoid-based CCMs cannot be found in Articles. Hornworts are among the very few plants that have a symbiotic relationship with nitrogen-fixing cyanobacteria[15] and one particular hornwort species, Anthoceros punctatus, has been used as a model system to study plant–cyanobacteria interactions[16]

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