Putting the fight in bryophytes
For plant biologists whose primary preoccupation is not bryophytes, it may have been possible to regard the bryophyte grade of organization as having failed to achieve the evolutionary mastery of life on land that the vascular plants have attained. Such views come from a ‘top-down’ consideration of land plants, with vascular plants, and especially seed plants, as the template for evolutionary success on land. Vegetative growth of the sporophytes of most vascular plants on land is based on the intolerance of desiccation and on an internal pathway for water from the soil to the transpiring surface – the endohydric condition. Most vascular plants are also homoiohydric, that is, transpiratory water loss is greatly restricted when the potential for evaporative water loss exceeds the rate at which water can be supplied through the xylem from the soil. Homoiohydry permits the plant to remain hydrated for varying, genotype- and environment-specific, periods of water deprivation. Photosynthetic gas exchange, with the inevitable loss of water, occurs when stomata are open and gas species within photosynthetic tissues permit CO2 distribution in the gas phase to photosynthetically active cells. When water supply from the soil is restricted, the plant takes pre-emptive action, using chemical signals from the root to the shoot, to reduce stomatal aperture and thus restrict water loss (and CO2 uptake: Davies et al., 2002; Wilkinson & Davies, 2002). With completely closed stomata the plant shoot is covered by a cuticle with low, to very low, water permeability.
No extant bryophyte is homoiohydric: they are all essentially poikilohydric, albeit in some cases with some characteristics of homoiohydry even in the gametophyte phase. Even when the sporophyte phase has an endohydric conduction pathway, intercellular gas spaces, stomata and a cuticle, it is parasitic for water and inorganic nutrient supply on the maternal gametophyte. Bryophyte gametophytes are frequently ectohydric, that is, they conduct water over the plant surface to the transpirational termini. Many terrestrial bryophytes are desiccation-tolerant in the vegetative, as well as the spore phase, of the life cycle. Such desiccation tolerance also occurs among a small minority of vascular plants. In all cases desiccation-tolerant vascular plants are of relatively small stature.
Despite not being homoiohydric, bryophytes are significant contributers to today's land flora as judged by species number, and the area of habitat in which they dominate or have a significant influence. Three papers in this issue (Proctor & Tuba, pp. 327–349; Ligrone et al. pp. 491–508; Niemi et al. pp. 509–515) contribute to our understanding of how bryophytes function at the land–air interface, and the way in which some of the components involved in their existence on land have evolved.
Homoiohydry and poikilohydry
Proctor & Tuba provide a masterly and wide-ranging review of the responses of bryophytes to the challenges to water relations of life on land, which vascular plants have largely addressed by homoiohydry and vegetative intolerance of desiccation. The review is an excellent introduction to the subject, emphasizing the quantitative rather than the qualitative nature of the distinctions between desiccation tolerance and desiccation intolerance, and between poikilohydry and homoiohydry, in both tracheophytes and bryophytes. They emphasize a point that has previously been given insufficient attention – the typical size scale of bryophytes relative to that of at least the independently growing stage (after dependence on maternally derived reserves) of vascular plant sporophytes. The typically small size of bryophytes puts them, often as dense monospecific canopies, within the diffusion boundary layer of the substratum, which can be a vascular plant, a rock or soil. The high resistance to gas exchange between a plant in this surface boundary layer and the well mixed atmosphere above means that the fixed resistance of a cuticle and, especially, the variable resistance of stomata, would have a much smaller impact on plant gas exchange than is the case for taller plants, which are more closely coupled to the bulk atmosphere. This argument provides an elegant rationale for observed gas-exchange characteristics of most bryophytes.
The nature of the substratum on the possibilities for water resupply to the transpiring surfaces of bryophytes (and tracheophytes) in the absence of rain or dew events is also covered by Proctor & Tuba. Ectohydric bryophytes on bark or rock only have extracellular reserves of water to tide them over until the next resupply of liquid water, usually with the fallback position of vegetative desiccation tolerance. Endohydry in bryophytes is often associated with rhizoids or more root-like structures (Raven & Edwards, 2001), able to abstract water from a moist porous substrate, and with a relatively water-repellent cuticle. The largest gametophytes of bryophytes (Dawsonia spp.) can be half a metre in height, and so be coupled to a relatively well mixed atmosphere for gas exchange (Proctor & Tuba). These large polytrichaceous gametophytes have a ventilation apparatus which approximates to a stomata–cuticle–intercellular gas space system typical of homoiohydric plants. This ventilation machinery consists of vertical, longitudinally arranged photosynthetic lamellae on the leaves, with the row of larger cells capping each lamella and the leaf lamina being essentially non-photosynthetic and cuticularized (Proctor & Tuba; Raven, 2002).
Proctor & Tuba make many other important points about the absence of qualitative distinctions among the means by which embryophytes balance the possibilities of death by starvation (inadequate photosynthetic uptake of atmospheric CO2) and death from thirst (greater water loss than the organism can tolerate). Their analysis applies to nonembryophytes which can grow photosynthetically on land; they specifically deal with lichens, and indicate that similar considerations apply to terrestrial algae growing on higher plants, rock, soil or buildings (Rindi et al., 1999) as well as intertidal algae subject to water loss at low tide (Raven, 1999). The points raised by Proctor & Tuba should be borne in mind by any reader (including the author) of Raven (2002).
Conduits of mosses and liverworts
The second paper on bryophytes (Ligrone et al., pp. 491–508) focuses on the water (and soil-derived solute) conduits of endohydric liverworts and mosses. The seminal paper of Ligrone et al. (2000) critically reviewed published ultrastructural evidence on the nature of endohydric conduits of liverworts and mosses, and also presented many new data on this subject. This analysis suggested that the conduits were polyphyletic in both mosses (Takakia; Bryales plus Polytrichales) and liverworts (Calobryales; Metzgeriales). Ligrone et al. (2002) extended the ultrastructural work to include immunocytochemical analysis of the carbohydrates in the walls of the conduits of four species of liverwort and eight species of moss by using a range of monoclonal antibodies to polysaccharides and glycoproteins of plant cell walls. The results support the conclusions of Ligrone et al. (2000) that the water conducting cells of Takakia, the endohydric conduits of liverworts and the hydroids of the Bryales and Polytrichales, are not homologous. Ligrone and coworkers also demonstrated very significant biochemical diversity of hydroid walls among species within the Polytrichales. This work substantially advances our understanding of the diversity of water-conducting elements in bryophytes.
The third paper on bryophytes in this issue (Niemi et al., pp. 509–515) deals with UV-B sensitivity of two species of Sphagnum (S. balticum and S. papulosum) and of Eriophorum vaginatum on a peatland in central Finland. The two Sphagnum species were more sensitive to UV-B than was the cotton grass. UV-B sensitivity is a function of a number of plant factors, including the possibility of screening of UV-B before it reaches, and damages, such essential intracellular UV-B-absorbing molecules as nucleic acids, proteins and quinines. Niemi et al. point out that the unistratose leaves of mosses such as Sphagnum do not permit the occurrence of UV-B screening compounds in epidermal cells, as is common in the leaves of many tracheophyte sporophytes. In vascular plants the epidermal cells (except for most stomatal guard cells) typically lack functional chloroplasts and the (adaxial) epidermal cells can be the sites of UV-B-absorbing phenolic compounds, such as dhurrin in Sorghum. This absence of UV-B screening compounds might be related to the greater UV-B sensitivity of the two mosses than of the higher plant (Niemi et al., 2002). However, certain bryophyte gametophytes could have the potential to mimic the vascular plant location of UV-B screening compounds in epidermal cells. Examples include the ventilated thalli of marchantiaceous liverworts, which have an epidermis with pores above the main assimilatory cells surrounded by gas spaces, and the nonphotosynthetic cells capping the photosynthetic laminae on the leaves of polytrichaceous mosses.
The three bryophyte papers here show, in a variety of ways, how the structure and physiology of bryophytes is not just a list of liabilities as far as life on land is concerned. Rather, many of the vegetative characteristics of bryophytes should be seen as permitting alternative strategies of existence on land to those of the ‘typical’ vascular plant. Indeed, extinct polysporangiophytes (the larger group, contrasting with the monosporangiophyte bryophytes, to which the tracheophytes belong) show substantial diversity in their structures related to homoiohydry relative to coexisting and extant tracheophytes (Raven & Edwards, 2001). Bryophytes frequently grow abundantly in environments not accessible to homoiohydric plants (Proctor & Tuba, 2002). In some habitats (field layer of certain Australian temperate closed forests) bryophyte gametophytes (Dawsonia), which have some homoiohydric characteristics, can be seen towering (by tens of centimeters) over creeping, putatively homoiohydric, dicotyledons. Given appropriate habitats there is a lot of evolutionary fight in the bryophytes!