Resistant tissues of modern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils

Abstract

Absence of a substantial pretracheophyte fossil record for bryophytes (otherwise predicted by molecular systematics) poses a major problem in our understanding of earliest land-plant structure. In contrast, there exist enigmatic Cambrian-Devonian microfossils (aggregations of tubes or sheets of cells or possibly a combination of both) controversially interpreted as an extinct group of early land plants known as nematophytes. We used an innovative approach to explore these issues: comparison of tube and cell-sheet microfossils with experimentally degraded modern liverworts as analogues of ancient early land plants. Lower epidermal surface tissues, including rhizoids, of Marchantia polymorpha and Conocephalum conicum were resistant to breakdown after rotting for extended periods or high-temperature acid treatment (acetolysis), suggesting fossilization potential. Cell-sheet and rhizoid remains occurred separately or together depending on the degree of body degradation. Rhizoid break-off at the lower epidermal surface left rimmed pores at the centers of cell rosettes; these were similar in structure, diameter, and distribution to pores characterizing nematophyte cell-sheet microfossils known as Cosmochlaina. The range of Marchantia rhizoid diameters overlapped that of Cosmochlaina pores. Approximately 14% of dry biomass of Marchantia vegetative thalli and 40% of gametangiophores was resistant to acetolysis. Pre-and posttreatment cell-wall autofluorescence suggested the presence of phenolic compounds that likely protect lower epidermal tissues from soil microbe attack and provide dimensional stability to gametangiophores. Our results suggest that at least some microfossils identified as nematophytes may be the remains of early marchantioid liverworts similar in some ways to modern Marchantia and Conocephalum.

Fungal symbioses in bryophytes: New insights in the Twenty First Century

“…These are based on a new look at the enigmatic Late Silurian to Late Devonian fossil Protaxites variously interpreted previously as a giant alga, fungus or lichen (Selosse 2002). Building on their earlier study (Graham et al 2004) Graham et al (2010a) suggest that Prototaxites was formed from partially degraded wind-, gravity-or water-rolled mats of mixotrophic liverworts having fungal and cyanobacterial associates much like Marchantia. They go on to argue that Prototaxites was derived from degradation-resistant rhizoids of marchantioid liverworts intermixed with tubular microbial elements, that liverworts were important components of Devonian ecosystems and that fossils previously attributed to nematophytes actually represent the remains of thalloid liverworts.…”

The Early Cretaceous Apple Bay flora of Vancouver Island: a hotspot of fossil bryophyte diversity

“…Pre-Cenozoic bryophyte scarcity has been traditionally attributed to a hypothesized low preservation potential of these plants (Stewart and Rothwell 1993;Hemsley 2001;Hübers and Kerp 2012). However, this hypothesis is rejected by the mechanical strength and chemical resilience of bryophytes, as demonstrated by experiments that simulate fossilization conditions (Kroken et al 1996;Hemsley 2001;Kodner and Graham 2001;Graham et al 2004), and by instances of exquisite preservation of even seemingly delicate bryophyte structures (Harris 1939;Smoot and Taylor 1986;VanAller et al 2008). Indeed, when discovered and carefully studied, pre-Cenozoic bryophyte fossils reveal morphology and anatomy in tremendous detail, such as minute and ephemeral reproductive structures (Harris 1939;Konopka et al 1997;Shelton et al 2015).…”

Superhydrophobic hierarchically structured surfaces in biology: evolution, structural principles and biomimetic applications

“…Although the systematic nature of these organisms that may have formed a cuticle or a similar extracellular covering is controversial, they may have played an important role in the transition from water to land. One of these groups is Nematophytes, puzzling organisms with a tubular organization of uncertain affinities [152][153][154][155]. However, recent investigations have led to the hypothesis that at least some fossil remnants assigned to Nematophytes are in fact Marchantiophyta [153].…”