The early evolution of land plants, from fossils to genomics: a commentary on Lang (1937) 'On the plant-remains from the Downtonian of England and Wales'

Abstract

During the 1920s, the botanist W. H. Lang set out to collect and investigate some very unpromising fossils of uncertain affinity, which predated the known geological record of life on land. His discoveries led to a landmark publication in 1937, 'On the plant-remains from the Downtonian of England and Wales', in which he revealed a diversity of small fossil organisms of great simplicity that shed light on the nature of the earliest known land plants. These and subsequent discoveries have taken on new relevance as botanists seek to understand the plant genome and the early evolution of fundamental organ systems. Also, our developing knowledge of the composition of early land-based ecosystems and the interactions among their various components is contributing to our understanding of how life on land affects key Earth Systems (e.g. carbon cycle). The emerging paradigm is one of early life on land dominated by microbes, small bryophyte-like organisms and lichens. Collectively called cryptogamic covers, these are comparable with those that dominate certain ecosystems today. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society.

Keywords: Cooksonia; Siluro-Devonian; bryophyte; cryptogamic cover; terrestrialization; tracheophyte.

Figure 1.

Stratigraphic occurrences of fossil plants mentioned in text. Ages in millions of years are taken from the International Chronographic Chart of the International Commission on Stratigraphy, 2012. All fossils mentioned are earliest occurrences (*), except for Psilophyton and Prototaxites, which indicate the age of the first specimens described by Dawson. Coloured block represents the time interval in Lang's paper: note that his ‘Downtonian′ encompasses the Pridoli Series (Grey Downtonian) and most of the Lochkovian Stage (Red Downtonian).

Figure 2.

New light micrographs of material illustrated by Lang [1]. Original number and figure numbers in brackets. (a) Cooksonia pertoni. Lectotype. Přídolí. V58011. (124 Z b; Plate 8, fig. 8). Coalified material has been removed, possibly using cellulose acetate, for further analysis. Scale bar, 2 mm. (b) Counterpart of (a). V58010. Black patches possibly of Nematothallus. Scale bar, 2 mm. (c) Cooksonia hemisphaerica. Lochkovian. V58022. (186; Plate 9, fig. 33). Scale bar, 2 mm. (d) C. hemisphaerica sporangium recovered using cellulose acetate. V54592. (1062; Plate 9, fig. 34). Scale bar, 1 mm. (e) Spore recovered from a sporangium of C. pertoni. V54995. (1105: Plate 8, fig. 11). Scale bar, 10 μm. (f) Tracheids recovered using cellulose acetate from a sterile axis, thought by Lang to belong to C. hemisphaerica. Lochkovian. V55040. (1150; Plate 9, fig. 36). Scale bar, 50 μm. (g) Banded tubes on cellulose acetate sheet. Přídolí. (962; Plate 11, fig. 60). Scale bar, 50 μm. (h) Nematothallus ‘cuticle′ on a cellulose acetate sheet. Přídolí. V54697. Scale bar, 50 μm. (i) Typical wefts of tubes assigned to Nematothallus. V54851. (Not figured, but cf. plate 11). Scale bar, 160 μm. (j) Dyad in elongate cylindrical spore mass. Přídolí. V54654. (764; Plate 13, fig. 109). Granular material probably represents condensed cell contents. Scale bar, 20 μm.

Figure 3.

All scanning electron micrographs except where stated. (a) Cooksonia pertoni subsp. apiculispora. Lochkovian. North Brown Clee Hill, Shropshire. Scale bar, 500 µm. First published in [, fig. 1a]. Museum number NMW94.60G.17. (b) C. pertoni subsp. apiculispora Lochkovian. North Brown Clee Hill, Shropshire. Scale bar, 500 µm. First published in [, plate III-1]. Museum number NMW94.60G.14. (c) Proximal (extreme right) and distal surfaces of spores of Aneurospora newportensis, isolated from sporangium in (a). Scale bar, 20 µm. From [, fig. 1d]. (d) Stoma from subtending stem in (a). Scale bar, 20 µm. From [, fig. 1b]. (e) Cast of tracheid from stem in (a); grooves indicate position of annular thickenings. From [, fig. 2a]. (f)–(j) Spores present in subspecies of C. pertoni. (f) Proximal surface of Ambitisporites sp. (subsp. pertoni), Upper Silurian. Scale bar, 10 µm. First published in [, fig. 3.1b]. V.62776. (g,h) Proximal and distal surfaces of Synorisporites verrucatus (subsp. synorispora), Upper Silurian. Scale bar, 10 µm. First published in [; plate 1, figs 3, 4]. NMW93.143G.1. (i,j) Proximal and distal surfaces of Synorisporites sp. (subsp. reticulispora), Lochkovian. Scale bar, 10 µm. First published in [, plate VI, 3, 18]. NMW2012.29G.20 and 19. (k) Light micrograph of a tubular structure (?hypha/banded tube) with internal spiral thickenings isolated from late Wenlock (Silurian), Rumney, Cardiff. Scale bar, 10 μm. First published in [, fig. 23]. MPK 6028. (l) Fractured end of banded tube, Ludlow (Upper Silurian), S. Wales. Scale bar, 5 µm. First published in [, fig. 68]. NMW77.34G.33c. (m) Fusitheca fanningiae containing permanent laevigate dyads with thin envelope. Lochkovian, Shropshire. Scale bar, 500 µm. First published in [, fig. 54]. NMW97.42G.4. (n) Light micrograph of Velatitetras rugulata, a permanent tetrad enclosed in a ‘rucked’ envelope, isolated from Wenlock rock, Shropshire. Unpublished–courtesy of Neil Burgess. Scale bar, 10 μm. (o) Tetrahedraletes medinensis, a permanent tetrad, Ordovician, Shropshire. Scale bar, 13 µm. First published in [, fig. 5A]. (p) Light micrograph of Artemopyra brevicosta, a permanent dyad, Wenlock, Shropshire. Scale bar, 10 µm. First published in [; plate 1, fig. 1]. (q) Dyadospora murusdensa, a permanent dyad, Ordovician, Shropshire. Scale bar, 10 µm. First published in [; plate 2, fig. 11]. (r,s) Fragment of Nematothallus williamii, Lochkovian, Shropshire. First published in [, fig. 1A,B]. Museum number NMW2013.39G.1. (r) Note three-layered thallus. Scale bar, 200 µm. (s) Magnification of (r) showing the surface patterning typical of the Nematothallus ‘cuticle’ and larger hyphae aligned perpendicular to the surface. Arrows indicate positions of lateral branches or areas in contact with a postulated photobiont. Scale bar, 100 µm. (t) Gametophytes and fertile sporophytes of Funaria hygrometrica. Note bifurcating seta in sporophyte on extreme left. (Courtesy of Jill Harrison, Yoan Coudart and Alison Reed, Cambridge University.)

Figure 4.

Relationships among major groups of land plants showing the hypothesized broad range of clades to which cryptophytes (extinct cryptospore-producing plants) might belong (shaded yellow oval; modified after [5,26]). As currently envisaged, cryptophytes is a grade of organization potentially encompassing plants spanning the embryophyte to vascular plant stem-groups as well as stem-group hornworts, mosses and liverworts. Some key developments discussed in the text are indicated on branches. Also indicated is a major shift in life cycle among clades from gametophyte dominated (sG) to sporophyte dominated (Sg) life cycles. The intermediate isomorphic life cycle (SG) is only known in some extinct plants. Estimated divergence times in millions of years.