Independent attempts towards an adapted terrestrial body within land plants

Increasing evidence is thus revealing that bryophyte innovations served, sometimes unexpectedly, as a basis for subsequent evolution in vascular

Fig. 1.6. Scanning electron micrograph of water-conducting cells in the simple thalloid liverwort Symphyogyna, showing the elongated pits in the thickened walls (reproduced from Ligrone et al. 2000 with permission of the authors and The Royal Society, UK).

plants. By contrast, a series of other characters thought to have first appeared in bryophytes and then to have been modified by descent in vascular plants, are now thought to have evolved repeatedly and independently in different lineages. The most striking examples concern the water-conducting structures, stomata and endosymbioses. These characters are, in fact, almost certainly not homologous between bryophytes and tracheophytes and even among the bryophyte lineages themselves. These features are now interpreted as the result of several independent attempts of land plants to adapt to their new, terrestrial condition.

Evolution of conducting structures Bryophytes are often erroneously referred to as non-vascular plants, implying that they are devoid of specialized tissue for the internal transport of water and nutrients. In fact, specialized internal conducting cells are found in some liverworts and most mosses (Ligrone et al. 2000). All bryophyte water-conducting cells are dead and lack any cytoplasmic content. Within liverworts, water-conducting cells are present in two main lineages. In some genera of simple thalloid lineages (see Section 3.1.1), water-conducting cells are elongate (8 x 300 mm) with tapering ends and thick walls perforated throughout by numerous pits (Fig. 1.6).

Fig. 1.7. Scanning electron micrograph of the end-wall of a water-conducting cell in the liverwort Haplomitrium, showing numerous, large pores (reproduced from Edwards et al. 2003 with permission of Blackwell).

In the basal liverwort and moss genera Haplomitrium and Takakia, these cells are, by contrast, similar in shape to the surrounding parenchymal cells, but are perforated by numerous pits of about 300-600 nm in the former and 120 nm in the latter (Fig. 1.7). Finally, differentiated, highly elongated cells (c. 200-1500 x 10-25 mm) called hydroids, with thin, non-perforated walls (Fig. 1.8), are present as a central strand in the stem, seta and leaf costa of most mosses (see Section 4.1).

For many decades, a possible homology between bryophyte water-conducting cells and water-conducting elements of tracheophytes figured prominently in phylogenetic speculation linking these groups. In particular, similarities between hydroids and tracheids have been emphasized to support the contention that these two cell types are homologous, i.e. have the same origin. The assumption of homology of hydroids and tracheids is fundamental to cladograms in which mosses are sister to tracheophytes (Fig. 1.4). There are, however, three main differences between hydroids and water-conducting cells of tracheophytes. First, hydroids lack secondary wall patterns such as spirals, bands or pitting that are characteristic of tracheids. Second, although lignin-like polymers have been detected in bryophytes, they are not tissue

Fig. 1.8. Scanning electron micrograph of a transverse (a) and longitudinal (b) section of a central hydroid, H, strand in the moss Dawsonia, showing the completely smooth walls and the thick-walled surrounding stereids, S (reproduced from Edwards et al. 2003 with permission of Blackwell).

specific, whereas lignin is predominantly localized in tracheids, vessels and fibres in tracheophytes (Ligrone et al. 2008). This suggests that, unlike lignins, the lignin-like polymers found in bryophytes do not fulfil specific structural functions and are more likely to be involved in protection against microorganisms (see Section 2.1). Third, as opposed to tracheids and vessels, hydroids collapse during water stress and are highly resistant to cavitation, that is the rapid formation and collapse of vapour pockets in water caused by the drop in pressure associated with desiccation (Ligrone et al. 2000). This emphasizes a major difference in the water relations between bryophytes and tracheophytes: while the former are mostly desiccation-tolerant, in other words, at equilibrium with external ambient humidity and suspend physiological activity upon drying, tracheophytes mostly tend to resist desiccation by pumping water from the soil through roots and limiting water loss by stomata and a waterproof cuticle (see Section 8.1).

Perhaps more striking is the similarity between the water-conducting cells in simple thalloid liverworts and tracheids, which both have thickened walls with helicoidally arranged pits. Such a similarity might suggest that simple thalloid water-conducting cells were the precursors of tracheids, which would definitely lend support to the hypothesis that liverworts are sister to tracheophytes (Fig. 1.5d). The pits of liverwort water-conducting cells, however, develop by removal of secondary wall material closely associated with

Fig. 1.9. Transmission electron micrographs showing cytoplasmic polarity in food-conducting cells in Mnium hornum, with the mitochondrion m, nucleus n and plastids p concentrated at the distal end of the cell (a) and details of the microtubules (arrowheads) extending from the nuclear pole into the cytoplasm (b) (reproduced from Ligrone & Duckett 1994 with permission of The New Phytologist).

Fig. 1.9. Transmission electron micrographs showing cytoplasmic polarity in food-conducting cells in Mnium hornum, with the mitochondrion m, nucleus n and plastids p concentrated at the distal end of the cell (a) and details of the microtubules (arrowheads) extending from the nuclear pole into the cytoplasm (b) (reproduced from Ligrone & Duckett 1994 with permission of The New Phytologist).

modified plasmodesmata, whereas in tracheophytes they arise from the lysis of primary unlignified walls with no direct link to plasmodesmata. The two cell types, therefore, have sharply different developmental designs, making homology between them highly unlikely.

Indirect support for the notion of an independent origin for hydroids and tracheids also comes from studies of photosynthate-conducting cells (the sieve cells in tracheophytes) in mosses (Ligrone et al. 2000). In mosses, photo-synthate-conducting cells exhibit a distinctly asymmetric cytoplasmic organization in longitudinal section, with many organelles and the nucleus close to one end and much less dense cytoplasm at the opposite end (Ligrone & Duckett 1994). This condition establishes two clearly different poles at the end of the longitudinal axis and is therefore referred to as cytoplasmic polarity (Fig. 1.9). From the nuclear pole, microtubules extend as parallel arrays. From these,

Fig. 1.10. Details of food-conducting cells under light microscopy: transverse section of the stem of Polytrichum commune (a) and detail showing leptoids, l, and associated parenchyma cells, p, sheathing around hydroids, h (b) (reproduced from Ligrone & Duckett 1994 with permission of The New Phytologist).

Fig. 1.10. Details of food-conducting cells under light microscopy: transverse section of the stem of Polytrichum commune (a) and detail showing leptoids, l, and associated parenchyma cells, p, sheathing around hydroids, h (b) (reproduced from Ligrone & Duckett 1994 with permission of The New Phytologist).

single microtubules diverge for a considerable distance in the cytoplasm, sometimes to both ends of the cell. This organization facilitates food conduction, either by movement along stationary microtubules or by microtubule-microtubule sliding. It is best developed in the order Polytrichales (see Section 4.1), wherein highly specialized cells, referred to as leptoids, are intermingled with parenchyma cells and form a wide irregular sheath around the water conducting strands of hydroids (Fig. 1.10) to function in long distance transport of organic nutrients. The sieve cells of tracheophytes, by contrast, are not polarized and microtubules do not persist after maturation of the cell (see Pressel et al. 2008b for further details). The two cell types are therefore unlikely to be homologous. The striking similarity between leptoids and sieve cells is probably an instance of homoplasy related to the relatively large sizes attained by Polytrichales and consequent evolutionary pressure for a more efficient transport of photosynthates. A similar example of homoplasy is found in the brown algae, notably the Laminariales, which also contain highly specialized photosynthate-conducting cells bearing striking similarity to sieve elements.

Thus, the hypothesis of multiple evolutionary origins of water-conducting cells in mosses, liverworts and tracheophytes is now strongly supported (Renzaglia et al. 2007). Making holes in the walls by disruption of plasmo-desmata, together with total loss of cytoplasmic content, is perhaps the easiest way to form a water-conducting cell under selective pressure for more efficient water transport. This suggests that the water-conducting cells that we observe in extant bryophytes correspond to multiple, independent attempts

Fig. 1.11. Stoma in sporophyte epidermis of the hornwort Leiosporoceros showing two guard cells surrounding a median pore (reproduced from Renzaglia et al. 2009 with permission of Cambridge University Press).

by land plants to adapt to their terrestrial environments and that they cannot be considered as the precursors of the tracheids and vessels of tracheophytes (Ligrone et al. 2000). The fact that hornworts, which are the only bryophyte lineage lacking water-conducting cells, are now considered to be sister to tracheophytes, is consistent with such an interpretation.

Evolution of stomata Stomata in bryophytes typically exhibit the same morphology as in tracheophytes: two guard cells surrounding a pore (Fig. 1.11). They are present in the sporophyte of most mosses and hornworts, but are absent from liverworts. Although it is not contested that bryophyte stomata facilitate gas exchange, the homology and function of these structures has been questioned. A major difference between bryophytes and tracheophytes is that the latter tend to resist desiccation by maintaining a high cell water content even when atmospheric humidity is low. In this case, the function of stomata is to maximize CO2 exchange while minimizing water loss by evaporation and successive opening and closing therefore follows diurnal cycling.

Fig. 1.12. Fungal associations in bryophytes: swollen-tipped rhizoids of the liverwort Cephalozia connivens after experimental inoculation with mycorrhizal fungi found on Ericaceae (a) (reproduced from Read et al. 2000 with permission of the authors and The Royal Society, UK) and scanning electron photomicrograph of fungus arbuscules in a cross-section of the thallus of the liverwort Marchantia foliacea (b) (reproduced from Russell & Bulman 2005 with permission of The New Phytologist).

Fig. 1.12. Fungal associations in bryophytes: swollen-tipped rhizoids of the liverwort Cephalozia connivens after experimental inoculation with mycorrhizal fungi found on Ericaceae (a) (reproduced from Read et al. 2000 with permission of the authors and The Royal Society, UK) and scanning electron photomicrograph of fungus arbuscules in a cross-section of the thallus of the liverwort Marchantia foliacea (b) (reproduced from Russell & Bulman 2005 with permission of The New Phytologist).

In bryophytes, stomata occur only on the sporangium of some mosses and hornworts and only in parts exposed below the calyptra or above the involucre. They are completely lacking from the vegetative gametophytes. Although the guard cells are able to open and close the stomata (Garner & Paolillo 1973), the pores seem to remain open early in the maturation of the sporangium. This pattern is inherently incompatible with a function solely of gas exchange and water retention. Renzaglia et al. (2007) hypothesized that, in bryophytes, stomata favour capsule dehydration to facilitate separation of spores, capsule dehiscence and spore release. The stomata of early polyspor-angiophytes resembled those of extant vascular plants. Unlike in bryophytes, stomata of these Silurian and Devonian plants were not restricted to the sporangial wall, in fact, they occurred on the gametophyte as well as on the sporophyte (Edwards et al. 1998). Stomata may therefore have distinct functions in modern plants. The function of stomata may thus not be homologous among land plants, but the possibility remains that the basic design may be shared and may have been fundamental for further ultrastructural and physiological modifications resulting in the complex stomata of higher plants.

Transition to land and fungal associations Most land plants (90%) establish intimate symbiotic associations with fungi in or around their roots (Wang & Qiu 2006). In bryophytes, various fungi have been reported inside the cells (endomycorrhizae) (Duckett et al. 2006a, b, Zhang & Guo 2007). Intracellular fungi have been found in rhizoids, where they induce the formation of swollen apices (Fig. 1.12a). They may also occur in the thallus, where they form ingrowth pegs into surrounding cells that much resemble the peloton structures found in the roots of angiosperms (Fig. 1.12b) (Duckett & Read 1991, Kottke et al. 2003). The absence of damage to the host cells and occurrence of the fungus within specific zones indicate a high level of compatibility between the partners (Duckett et al. 2006b).

This broad phylogenetic distribution across embryophyte lineages suggests, not surprisingly, an ancient origin of mycorrhizae in the evolutionary history of land plants. Mycorrhizae may, in fact, have been essential for the colonization of (Pirozynski & Malloch 1975) and even the morphological diversification (Brundrett 2002) on land. In a terrestrial environment, where nutrients are much less mobile than in water, the immense surface area of the hyphae increases the absorption or exchange capability necessary for efficient mining of the resources, in particular those macronutrients with low mobility in the soil (Cairney 2000). Land colonization also involved the evolution of a suite of protective mechanisms against pathogens, the development of which might be directly (through the production of antibiotics) or indirectly (by depleting the nutrient pool, or triggering plant defences) prevented by mycorrhizal fungi (Selosse et al. 2004).

For mycorrhizae to have played a determinant role in the origin of land plants, two conditions must have been met: (a) fungal partners occurred at the time of the transition to land and (b) the association is exhibited by fossils of the earliest land plants. Phylogenetic inference suggests that the Glomeromycetes, which are the most common endosymbiothic fungi found in bryophytes, originated no later than 500 mya (Berbee & Taylor 2007). Their ancestry is corroborated by fossils from the Ordovician Period (460 mya; Redecker et al. 2000). However, the origin of the mycorrhizal lineage may be much younger (Berbee & Taylor 2007), in which case the association of Glomeromycetes with extant lower land plants (Read et al. 2000) would result from recent adoption of this strategy rather than from inheritance of a deeply ancestral trait (Selosse 2005). Such an interpretation finds some support in the fact that most mycorrhizal fungi recovered from liverworts belong to a rather derived lineage of Glomus comprising species associated with vascular plants (Ligrone et al. 2007). The fungus of Marchantia foliacea, for example, arose from a group of species that form mycorrhizal associations with flowering plants (Russell & Bulman 2005). Similarly, the fungal symbiont of the hornwort Anthoceros is known primarily from associations with higher plants (SchuBler 2000).

By contrast, the fungi recently reported from mosses span a broader phylogenetic spectrum encompassing four (rather than one) families of Glomerales (Zhang & Guo 2007). This perhaps indicates a more ancient origin of the moss-fungal interaction than in the case of hornworts and liverworts. Furthermore, remarkable parallels between fungal associations in the basal liverworts genera Treubia and Haplomitrium (Section 3.1.4), as well as the very ancient pteridophyte genus Lycopodium, suggest that these associations epitomize very early stages in the evolution of glomeromycotean symbioses (Duckett et al. 2006a). Finally, fossil evidence suggests that land plants had already established fungal associations by the Devonian Period (Taylor et al. 2004, Krings et al. 2007) and, at least in one case, the association shared similarities with modern endomycorrhyzae (Remy et al. 1994). Whether this ancient interaction was indeed mutualistic can, however, not be determined.

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