Plant of the Week – 26th April 2021 – Phaeoceros laevis (Smooth Hornwort)

Phaeoceros laevis (L.) Prosk. – Division Anthocerotopsida

The Hornworts are a sister group to the mosses and liverworts that evolved 450-500,000,000 years ago and are thus closer to the lineage that led to the vascular plants.  They illustrate morphological features that link them to their algal ancestors that are not expressed in the mosses or liverworts.  They are therefore key to the understanding of the evolution of plants on the land.

Records for Phaeoceros laevis from the Lothians, cited in Smith et al. (2002), all from the first decade of the 20th century, are now considered to be doubtful. The two for which there are herbarium specimens have been redetermined as Aneura pinguis (a liverwort), and the third was only known as a literature record. There was every reason to believe that the species would be found in the Lothians but where should one look?

As it happens it was there right under my nose. As a retired member of staff, I have traced a route for 45 years, between my residence and the herbarium, across the Edinburgh Royal Botanic Garden. In September 2014 I spotted thalli in a flower bed that looked like those of Phaeoceros laevis. However, the thalli were male only, indicating that the organism was dioecious. Therefore, the tell-tale capsules were absent. Luckily, the male antheridia were quite large, confirming that this was indeed P. laevis; for the hornworts, the size of the male sex organs really does matter.

Figure 1. Phaeoceros laevis (l.) Prosk – female.

Figure 2. P. laevis (l.) showing antheridial tubercles (upper centre)Royal Botanic Garden Edinburgh, September 2014    Photo: D.F. Chamberlain

Life History
 The general life history of the Anthocerotophyta closely resembles that of the liverworts (see Chamberlain & Chamberlain – Marchantia polymorpha blog). The haploid spores germinate to produce a protonema from which the haploid thalli arise that are either male or female. The haploid spermatozoids travel through water films to the female thalli where fertilisation occurs in the archegonia. The resulting diploid sporophyte then develops into a capsule, in which meiosis occurs to produce haploid spores sequentially as it elongates. The capsules mature through the autumn and early winter. The thalli can perennate though they are generally killed by severe frost, turning black and rotting. P. laevis can overwinter vegetatively and recolonise from tubers borne on the underside of the thallus. Thus, the best time to record Phaeoceros is in the autumn and early winter.

Annual or perennial; thalli dioicous, broad, shallowly lobed, not translucent, commensal Nostoc colonies present in thalloid cavities, tubers sometimes present on the under-surface of the lobes.  Male thalli bearing conspicuous antheridial cavities, each with several antheridia that have a body length of 120-245 µm. Female thalli bearing cylindrical involucres, from which the narrowly cylindrical capsules emerge are at maturity 10-70 mm long. As the capsule extends, it splits into two twisted valves. Spores yellow, maturing over a long period as the capsules split, ejected by the expansion of the pseudo-elaters.

Figure 3. Phaeoceros laevis (scanned from Paton, 1999, with the author’s permission).
Key: an – antheridium, ap. tu. – tuber apex, l/s. – longitudinal section, n. – Nostoc, pse. – pseudo-elaters,
sp. – spore, th. – thallus (d.e. – dorsal epidermis), t/s transverse section, v.s. tub – male tubercle, vertical section

Morphology There are two aspects of the morphology of Phaeoceros that relate to the evolution of green plants as they colonised dry land.
The most significant feature that distinguishes the hornworts from the mosses and liverworts is a basal meristem in the bulbous base of the sporophyte. This meristem produces a complex structure as the capsule elongates, resulting in a continuous production of haploid spores over a significant time interval. The continuous maturation of the capsule requires control of water loss; this is achieved by the development of stomata. These stomata are structurally homologous with those in flowering plants but differ in that, once they open, they do not close. This complex sporophyte morphology is not found in the mosses or the liverworts; similar stomata are present on moss though not liverwort capsules.
The chloroplasts are the cellular organelles containing chlorophyll that enables green plants to harness sunlight.  P. laevis is one of the hornworts in which these chloroplasts contain pyrenoids; they occur widely in the algae, but not in either the mosses or liverworts, or in any of the vascular plants. Thus, these pyrenoids provide evidence of a direct link to the algal ancestors of the hornworts that emerged early in the process of dry land colonisation by green plants. These pyrenoids contain stacks of thyalakoid membranes that are mirrored in the chloroplasts of vascular plants. Their function is to improve the efficiency of Rubisco, a key enzyme in the cascade of chemical reactions that leads to the fixation of carbon dioxide. However, it can also bind to oxygen, a biproduct of the light (Hill) reaction, during which the energy of sunlight is harnessed. This leads to a process called photo-respiration. The function of the pyrenoids is to raise the carbon dioxide concentration around the reaction sites by as much as 150 times. This increases the proportion of carbon dioxide molecules that bind with Rubisco, resulting in more efficient photosynthesis (Villarreal & Renner, 2012).

Related species in Britain
There are four species of hornworts in Britain, belonging to two different genera. All four can occur together in fallow fields.  The species in the genus Anthoceros differ from those in Phaeoceros in the more deeply incised, almost crisped thalli that have internal mucilaginous cavities. At maturity, the spores are black, and the antheridia are significantly smaller, borne in insignificant pits. Phaeoceros carolinianus is monoicous, with both sexes on the same thallus.  

Figure 4. Phaeoceros carolinianus (Michx) Prosk.,_122441-471446)_1077.JPG

Ecology and Distribution
P. laevis is a plant of moist, often shaded soil, on woodland banks, in fallow fields or on the sides of ditches. In Britain it tends to have a more western and southern distribution (NBN distribution map).  It is considered to have a world-wide distribution and can probably be characterised as cosmopolitan (Paton, 1999).

Around Edinburgh the only certain records are from urban, built-up environments. The site in the Royal Botanic Garden is on the north side of a building, in the drip zone from the roof, and it is permanently shaded by a shrubbery composed mainly of evergreen rhododendrons. In September 2019 I visited an artificial pond in Currie, SW Edinburgh, that had been created as a memorial to the water mill heritage on the Water of Leith. Below the north face of a modern flat, I discovered a population of P. laevis.  As both sexes were present there were mature capsules, making identification certain in situ. I therefore believe that the population at the RBGE had probably not been introduced when the shrubbery was planted up. There is a striking similarity between the ecology of these two urban sites in Edinburgh. The common denominator is the open ground that is permanently moist and shaded. This is significant as Edinburgh is on the drier east side of Scotland.

Nostoc commune
The close symbiotic association of the cyno-bacterium Nostoc commune with its host is a feature of the hornworts.  The cavities that contain Nostoc can be distinguished as dark bluish-black patches on the thalli. Nostoc occurs as strings of cells that can be dispersed in water films. It transfers fixed nitrogen from the air via mucilaginous cells in the hornwort thalli (Adams & Duggan, 2008). An endosymbiotic association with Nostoc is a very rare in the liverworts. Nostoc is never endosymbiotic in the mosses but may occur on the surfaces of the leaves.

Mycorrhizal Associates
It appears that that mycorrhizal co-habitation with green land plants were present early in their progression onto dry land. This is indicated by the symbiotic mycorrhizal species that belong to the Mucoromycota, a significant number of which are associated with the hornworts, including P. laevis. This ancient group of fungal taxa were contemporaneous with the evolution of the hornworts; The Mucoromycota are hardly represented amongst the fungal mycorrhizae associated with the vascular plants (Rimington et al, 2020). Functioning DNA sequences for the genes enabling P. laevis to become a mycorrhizal host can be inserted into a mutant of the flowering plant Medicago truncatula, restoring a lost ability to form a mycorrhizal association (Wang Bin et al., 2010). Evidently, these genes have been retained over perhaps 300,000,000 years of land plant evolution.

Evolutionary history
Darwin has left us with an elegant metaphor for evolution, likening it to a discarded book, out of which most pages have been torn.  We have the clues left on the remaining pages, from which to reconstruct an evolutionary past. The problem is that mega-fossils of the bryophytes, and especially those of the hornworts, are not easily preserved.

One solution is to compare genomes across different plant groups to generate an evolutionary tree. The evidence suggests that the mosses, liverworts, and hornworts belong to a monophyletic embryophyte clade that diverged as a unit from the branch of the evolutionary tree that led to the vascular plants (Zhang & Fu, 2020; Frangedakis et al., 2021). Within this clade, the hornworts appeared first, followed by the bifurcation that separated the mosses from the liverworts. The probable range in timescales for the divergence of and within the bryophyte clade (Morris et al., 2018) are constrained by the emergence of embryophyte cryptospores in the fossil record. By inference, the hornworts are closer to the algal progenitors of this clade, and those of the vascular plants. The evidence for the nature of the organisms at the point that the ‘bryophytes’ diverged from the common ancestors of the vascular plants sits tantalisingly on one of Darwin’s lost pages.

Table 1. Estimated divergence times for the embryophytes, the hornworts and the mosses/liverworts

Edinburgh has been my home for the past fifty-four years, yet it has taken the Covid-19 lockdown to really come to appreciate the bryology of the city as I exploited my right to exercise within a five- mile radius of my home. There is something compulsive in adding crosses to a master excel spreadsheet, but that is totally pointless, unless the distributions are used to explore the bigger picture. This is the story of just two of these crosses. The hornworts give us an insight into the early evolution of plants as they colonised the land, perhaps 500,000,000 years ago. They may even provide us with the genes that could improve today’s crops by making photosynthesis more efficient. This is a story that seeks to stimulate scientific curiosity.

Adams, D.G. & Duggan, P.S. (2008). Cyanobacteria – bryophyte symbioses. Journal of Experimental Botany 59,5: 1047-1058.

Frangedakis E., Shimamura, M., Villarreal., J.C., Li, Fay-Wei, Tomaselli, M., Waller, M., Sakakibara, K.,

Renzaglia, K.S., Szövényi, P. (2021). The hornworts: morphology, evolution and development. New Phytologist 229: 735-751.

Morris, J.L., Puttick, M.N., Clark, J.L., et al. (2018). The timescale of early land plants evolution. Proc. Nat. Acad. Sciences USA 115(10) 2274-2283.

National Biodiversity Network Trust (NBN).

Paton, J.A (1999). The Liverwort Flora of the British Isles. 625pp. Harley Books, Colchester.

Rimington, W.R., Duckett, J.C., Field, K.J. et al. (2020). The distribution and evolution of fungal symbioses in ancient lineages of land plants. Mycorrhiza 30:23-49.

Smith, P.M., Dixon, R.O.D., Cochrane, M.P. (2002). Plant Life of Edinburgh and the Lothians. (Edinburgh University Press.

Vaughn, Kevin C., et al. “The Anthocerote Chloroplast: A Review.” The New Phytologist, vol. 120, no. 2, 1992, pp. 169–190. JSTOR,

Vilarreal , J.C. , Jenner, S.S. (2012). Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years. Proc. National Academy of Sciences 109 (46) 18873-18878.

Wang, Bin, Yuen, Li Huey, Xue, Jia Yu et al (2010). Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonisation of land by plants. New Phytologist 186,2: 514-525.

Zhang, J. & Fu, X.X. (2020). The hornwort genome and early plant evolution. Nature Plants 6:107-118.

David Chamberlain

Leave a Reply

Fill in your details below or click an icon to log in: Logo

You are commenting using your account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s

%d bloggers like this: