Diversity in conducting cells in early land plants and comparisons with extant bryophytes

Abstract

Anatomical screening using scanning electron microscopy (SEM) of short lengths of smooth coalified axes (mesofossils) from a Lochkovian (Lower Devonian) locality in the Welsh Borderland, Shropshire has revealed extensive diversity in the architecture of centrally aggregated, elongate cells. At least 14 types have been discovered, each distinguished by variation in wall architecture and combination of the cells in the central strand. End walls have not been seen. These elongate cells may have smooth, uniformly thick or thin walls, walls with smooth projections either traversing or lining the lumen, or bilayered walls, the innermost perforated by pores of plasmodesmata dimensions. The latter type may be further divided on presence or absence of projections which may line the lumen, but usually cross it and are highly disorganized. Indeed, none of the cells shows the regularity associated with the secondary thickenings of tracheids, but the imperforate/pitted forms with projections superficially resemble the S-type tracheids of the Rhyniopsida in basic construction. Simply pitted types show greater similarity with the waterconducting cells (WCCs) of liverworts and Takakia . To facilitate direct comparison with bryophyte conducting elements, SEM studies were undertaken on the WCCs of a number of mosses and liverworts and on the leptoids of mosses, in conjunction with a range of degradation experiments designed to assess the fossilization potential of these cells. With the exception of polytrichaceous hydroids, the latter demonstrated the resilience of hydroids and leptoids to the chemical treatments. In addition, dehydration of the leptoids produced globular residues similar to those seen in some of the fossils. This combination of techniques raises the possibility that food-conducting cells might well be preserved in coalified fossils, and hence extends the interpretation of the functions of the elongate cells. Broadly speaking, imperforate bilayered examples may have been involved in water conduction, cells with globular residues with or without pitting involved in metabolite movement, and smooth walled examples with or without projections involved in support. The wider affinities of the plants which produced the axes remain equivocal and in the absence of sporangia it is impossible to assign them to a genus. However, this anatomical diversity in vegetative remains of extreme simplicity demonstrates far greater diversity in early land vegetation than is apparent from perusal of species lists. Figures 7-12. NMW99.20G.5 continued. Scale bars = 1 µ m. Figs 7,8. LS and oblique TS of micropitted elements with horizontal ridging. Note part of element with smooth projections to top of 7. Fig. 9. TS smooth walled element lacking projections. Figs 10,11. Fractured junctions between two types of element with projections. Arrow = smooth walled cell lacking projections. Fig. 12. Fragments of perforated wall layers. 302 D. EDWARDS ET AL .

Early evolution of life cycles in embryophytes: A focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity

“…Edwards et al (2003) showed the existence within those simple fossils of a previously unsuspected wide range of anatomical diversity. Some specimens were described as showing a combination of characters not present in later bryophytes or tracheophytes (Edwards et al, 2003). Similarly, the Ordovician trilete spore assemblages of Steemans et al (2009) might also represent a glimpse at a past biodiversity encompassing plants with grades of organisation intermediate between bryophytes and tracheophytes.…”

“…The biodiversity of the organisms that thrived during this period of time is largely undocumented, but a few examples suggest that plants with intermediate grades of organization might have existed. Edwards et al (2003) have studied a large collection of minute coalified axes from an Early Devonian locality in the Welsh Borderland, Shropshire. Edwards et al (2003) showed the existence within those simple fossils of a previously unsuspected wide range of anatomical diversity.…”

“…Edwards et al (2003) have studied a large collection of minute coalified axes from an Early Devonian locality in the Welsh Borderland, Shropshire. Edwards et al (2003) showed the existence within those simple fossils of a previously unsuspected wide range of anatomical diversity. Some specimens were described as showing a combination of characters Kenrick & Crane, 1997b;Karol et al, 2001;Qiu et al, 2006;Gonez & Gerrienne, 2010).…”

“…The embryophytic affinities of Late Silurian cryptospore specimens have recently been unambiguously established (Steemans et al, 2010). The Late Silurian/Early Devonian fossil record includes embryophyte extinct lineages that are considered intermediate between the bryophyte grade and vascular plants: (i) the Late Silurian/Early Devonian mesofossil record is comprised of a wide range of small axes with centrally aggregated, elongate cells that show an almost continuous variation from smooth, uniform thin walls (suggesting affinities with bryophytes) to bilayered walls, the inner with annular or spiral thickenings (suggesting affinities with vascular plants) (Edwards, 2003; Edwards et al, 2003); (ii) the protracheophyte Aglaophyton Edwards 1986 is at a polysporangiophyte grade of organization but is devoid of thickened water‐conducting cells (Kenrick & Crane, 1991, 1997a, b); (iii) the paratracheophyte Rhynia has peculiar water‐conducting cells with a very thin, apparently unlignified, decay‐resistant, inner layer covering a spongy layer (Boyce et al, 2003; Edwards, 1980; Kenrick & Crane, 1991, 1997a, b) (Fig. 1).…”

Evolution of phytolith deposition in modern bryophytes, and implications for the fossil record and influence on silica cycle in early land plant evolution

“…Given the widespread deposition of phytoliths in WCC of both bryophytes and tracheophytes, we hypothesize that the evolution of WCC within early land plant lineages may have been closely followed by production of WCC‐derived phytoliths – albeit not necessarily in high abundances (see the Discussion section above). Organic fossils of various in situ WCC from tracheophytes, bryophytes and plants of unknown affinity are known from the Silurian–early Devonian and isolated smooth and ridged tubes reminiscent of WCC appear in the late Ordovician (Hueber, ; Krassilov & Schuster, ; Edwards et al ., ; Kenrick et al ., ). Thus, we might expect to see WCC phytoliths from bryophytes as fossils by at least the Silurian, a time‐frame that is consistent with recent phylogenetic dating of crown tracheophytes (late Ordovician–late Silurian; Morris et al ., ).…”