Development of water‐conducting cells in the antipodal liverwort Symphyogyna brasiliensis (Metzgeriales)

Abstract

SUMMARYThe thallus of the metzgerialean liverwort Symphyogyna brasiliensis Nees contains a strand of dead thick-walled cells with helicoidally-arranged pits that are presumably involved in water transport. During the first phase of differentiation these cells undergo a 13-16-fold elongation while remaining thin-walled and almost unchanged in diameter. During suhsequent maturation the walls hecome strongly thickened hy deposition of highly electronopaque material on extraplasmodesmal areas and of transparent material forming collars around plasmodesmata. Whilst the growing wall shows an ordered microfihrillar texture and is strongly reactive to PATAg staining for carbohydrates, the material associated with plasmodesmata is amorphous and PATAg-negative. A dense cortical array of microtohules (MTs) overlies the growing wall except in proximity to plasmodesmata, which are closely associated with tuhular endoplasmic reticulum (ER). During cellular maturation plasmodesmata undergo extensive secondary elongation hy incorporation of cortical ER supposedly continuous with desmotuhules. Quantitative analysis of plasmodesmal frequencies in relation to cellular elongation and wall thickness indicates that there is no de novo formation of plasmodesmata. Cortical MTs, wall microfibrils and secondarily-modified piasmodesmata are consistently co-aligned, all forming helices of about 45°. During maturation the Golgi apparatus proliferates and a vast number of vesicles containing PATAg-positive material are produced from a membrane domain interpreted as trans Golgi network, whilst PATAg-negative vesicles are formed along the fenestrated margins of cis and medial dictyosomal cisternae. Exocytosis of PATAg-positive vesicles is confined to extraplasmodesmal areas. In ageing cells abundant fibrillar material, also positive to PATAg-test, accumulates within pleomorphic membrane-bounded tubules. Final cytoplasmic dissolution involves the lysis of all cellular membranes and the liberation of the membrane-bounded fihrillar material, that is subsequently deposited onto the walls. The eventual dissolution of the plugs of amorphous electron-transport material results in the formation of open pits. Similarities in the cytological mechanisms underlying pore development in water-conducting cells of Symphyogvna and in the sieve elements of angiosperms are discussed.

Conducting tissues and phyletic relationships of bryophytes

“…However, pits in the former develop by removal of secondary wall material closely associated with modi¢ed plasmodesmata, while in the latter they arise from the lysis of primary unligni¢ed walls with no direct relation to plasmodesmata, albeit in both cases cortical microtubules appear to have a prominent role in morphogenesis (cf. Ligrone & Duckett 1996;McCann 1997;Cha¡ey et al 1997Cha¡ey et al , 1999Seagull & Falconer 1991). The two cell types, therefore, have sharply di¡erent developmental designs and homology between them is highly unlikely.…”

“…The pits arise from plasmodesmata (¢gure 5c,d) through a mechanism closely recalling the genesis of pores in sieve elements (Esau & Thorsh 1985;Lucas et al 1993). This process has recently been described in detail in Symphyogyna (Ligrone & Duckett 1996). Following an elongation phase that terminates when the cells have reached their de¢nitive sizes, the cell walls are thickened by deposition of electron-opaque material, on extraplasmodesmatal areas, and of electron-transparent material forming collars around plasmodesmata (¢gure 5d).…”

“…This extremely distinctive organization is found not only in the cortical cells of the leafy shoot and seta but also in other types of tissues and organs, including mature caulonemal and rhizoidal cells (Duckett et al 1998), where a need for long-distance symplasmic transport of solutes can be postulated (table 5). An experimental study (Ligrone & Duckett 1996) has shown that polarized organization is suppressed following removal of the source/sink gradient. The longitudinal alignment of the nucleus and organelles is disrupted by oryzalin, a microtubule inhibitor, while it is insensitive to cytochalasin, a drug a¡ecting the actin micro¢laments.…”

“…Following an elongation phase that terminates when the cells have reached their de¢nitive sizes, the cell walls are thickened by deposition of electron-opaque material, on extraplasmodesmatal areas, and of electron-transparent material forming collars around plasmodesmata (¢gure 5d). The newly deposited wall material di¡ers cytochemically and structurally from the original wall (Smith 1966;Ligrone & Duckett 1996) and is therefore to be considered a secondary wall. Eventually, the cells undergo cytoplasmic dissolution and the electrontransparent wall material around the plasmodesmata is removed.…”

The role of Mid-Palaeozoic mesofossils in the detection of early bryophytes

“…The Symphyogyna type has been described as most tracheid-like, in that the elongate, very narrow hydroids have walls of uneven thickness. Frey et al (1996) and Ligrone & Duckett (1996) have recently con¢rmed that the thick wall is cellulose, primary and non-layered, with pits situated at the bases of oblique, slit-shaped depressions, ca. 0.3 m m diameter, and produced around plasmodesmata.…”