Sporophyte

The fundamental architecture of the moss sporophyte is simple, similar to that of liverworts: an unbranched seta anchored into the maternal gameto-phyte by the foot and carrying a single terminal sporangium. Although an apical cell is differentiated early during embryogenesis, its activity is ephemeral. Soon, a new meristem, unique among bryophytes, is initiated below the apex. The segments above it will develop into the capsule and those below into the seta and the foot. Apical growth is thus confined to the earliest ontogenetic stages and much of the growth of the sporophyte results from the activity of the intercalary meristem. The foot is either tapered or bulbous and the placental region lining gametophytic tissues is typically composed of transfer cells. Whether the haustorium-like tissue is essential for the efficient uptake of water and nutrients, or merely for tightening the attachment of the sporophyte, is not clear.

The seta serves to raise the capsule above the perichaetial leaves protecting the developing sporophyte. The embryo is enclosed completely at first in

comitrium pyriforme. (c) Immersed capsule (here the casule is already dehisced and remains as small cupules among the perichaetial leaves) in Aphanorrhegma serratum.

an epigonium that is derived from the archegonium. Occasionally, growth is halted prematurely and the capsule is retained within the perichaetium (e.g. Aphanorrhegma, Fig. 4.14). An intercalary meristem and thus an actual seta is lacking in only two genera, Sphagnum and Andreaea. In these lineages, elevation of the capsule is accomplished by growth of gametophytic tissue into a stalk called a pseudopodium. Lateral meristems and thus appendages are always absent from the seta and the epidermis that is composed of smooth or more rarely papillose cells universally lacks stomata. The stalk is solid and composed of parenchyma cells (Fig. 4.4b). Long, thin-walled water-conducting

Fig. 4.15. Modification of the seta. In Rhachitheciopsis, the seta is twisted when dry (a) but erect when moist. The movement of the seta is accounted for by uneven wall thickenings of the cortical cells of the seta (b). In Microbryum curvicolle, an ephemeral ground-dwelling moss, the seta is curved downward (c), favouring dispersal of spores within the vicinity of the parental sporo-phyte (photo C. Rieser).

Fig. 4.15. Modification of the seta. In Rhachitheciopsis, the seta is twisted when dry (a) but erect when moist. The movement of the seta is accounted for by uneven wall thickenings of the cortical cells of the seta (b). In Microbryum curvicolle, an ephemeral ground-dwelling moss, the seta is curved downward (c), favouring dispersal of spores within the vicinity of the parental sporo-phyte (photo C. Rieser).

cells form an axial strand in some taxa, even those lacking conducting cells in the gametophyte. The walls of the cortical cells may be unevenly thickened, which leads to the twisting of the seta, even conspicuous bending in some taxa, upon drying, facilitating spore dispersal (Fig. 4.15a, b). In many, primarily ground-dwelling species, the seta is curved at the apex and the capsule hangs downward (Fig. 4.15c).

Early in the ontogeny of the sporangium, two tissues are differentiated. The four inner central cells form the endothecium. Its development lags behind that of the amphithecium, which develops from the outer rings and undergoes repeated divisions yielding new layers of multiple cells. The amphithecium forms the capsule wall and the underlying parenchyma as well as, in the region above the annulus, the teeth around the capsule mouth (i.e. the peristome). The endothecium forms the columella and the spore sac, although in Sphagnum this role is taken by the amphithecium. The columella is a sterile axis that extends through the sporogenous region and connects to the operculum except in basal taxa such as Sphagnum and Andreaea, in which it is dome-shaped, or in Archidium, which lacks a columella altogether.

The capsule typically bears stomata, dehisces subapically through the loss of a lid and bears one or two rings of teeth lining the mouth. Stomatal guard cells are rather elongate and kidney-shaped. They define a pore that is either round or slightly elliptical, resulting in a stoma that resembles that of other

(b)

Fig. 4.16. Stomata. (a) Phaneroporous: the guard cells are fully exposed on the surface of the capsule. (b) Cryptoporous: the guard cells are overarched by subsidiary cells. (c) Incomplete division of the guard cells results in the pore being defined by a single ring-shaped guard cell in the Funariaceae.

Fig. 4.16. Stomata. (a) Phaneroporous: the guard cells are fully exposed on the surface of the capsule. (b) Cryptoporous: the guard cells are overarched by subsidiary cells. (c) Incomplete division of the guard cells results in the pore being defined by a single ring-shaped guard cell in the Funariaceae.

embryophytes (Fig. 4.16a). Occasionally, the mother guard cell fails to complete its division and the stoma is then defined by a single ring-like cell. Single guard cells are found in all members of the Funariaceae (Fig. 4.16c). Stomata are often restricted to the neck of the capsule. In some taxa, the guard cells are overarched by adjacent or subsidiary cells (Fig. 4.16b), which probably reduce airflow and thus evapotranspiration. Like stomatal crypts in vascular plants, such cryptoporous stomata are homoplasious and are found primarily in taxa growing in xeric conditions, such as many epiphytic or saxicolous members of Orthotrichum. Superficial or phaneroporous stomata are the general condition in mosses. Shortly after their differentiation, the stomata regulate gas exchange (Garner & Paollilo 1973). They remain open thereafter and their function remains ambiguous. In Sphagnum, structures that are considered analogous to stomata (i.e. pseudostomata) line the equatorial region of the capsule (Boudier 1988). Their function is thought to be purely mechanical, rather than physiological, collapsing upon dehydration to force the release of the operculum. Stomata have been lost repeatedly during the diversification of mosses. In lineages derived from the earliest cladogenic events (e.g. Takakia and Andreaea), stomata are consistently lacking, suggesting that they originated after the divergence of mosses. Hence, stomata are

Fig. 4.17. Two fundamental architectures of the peristome. (a) In nemato-dontous peristomes (e.g. Atrichum undulatum, courtesy of Neil Bell), the teeth are composed of whole cells. In the Polytrichaceae, the teeth are connected to a thin membrane, the epiphragm (arrow). (b) In arthrodontous peri-stomes, the teeth are composed of remnants of cell walls. The peristome may be composed of two or one ring of teeth. The outer ring is called the exostome (black arrow), the inner one, the endostome (white arrow). Typically, only one wall per cell remains and is attached to the sole remaining wall of the cells facing it (c).

Fig. 4.17. Two fundamental architectures of the peristome. (a) In nemato-dontous peristomes (e.g. Atrichum undulatum, courtesy of Neil Bell), the teeth are composed of whole cells. In the Polytrichaceae, the teeth are connected to a thin membrane, the epiphragm (arrow). (b) In arthrodontous peri-stomes, the teeth are composed of remnants of cell walls. The peristome may be composed of two or one ring of teeth. The outer ring is called the exostome (black arrow), the inner one, the endostome (white arrow). Typically, only one wall per cell remains and is attached to the sole remaining wall of the cells facing it (c).

probably not homologous among mosses, hornworts and vascular plants (see Section 1.4.2).

The peristome is a unique attribute of mosses but is not present in all species: this innovation was acquired after the divergence of the Andreaeo-bryopsida (Fig. 4.22) and subsequently lost in many taxa. The peristome consists of one or two concentric rings of teeth exposed following the loss of the operculum (Fig. 4.17). In Polytrichum and allied taxa, the teeth are composed of entire elongated cells (Fig. 4.17a) and the peristome is said to be nematodontous. In all other peristomate mosses, the cells contributing to the peristome are partially degraded and the teeth are built almost exclusively from vertical cell walls (Fig. 4.17b, c). The teeth are articulate. They can bend inward or outward, hence the name arthrodontous for this peristomial architecture. As is always the case in bryophytes, movement is accounted for by differential forces acting upon hydration (or dehydration) of cell walls of different thicknesses. Each tooth is composed of two radial columns of plates, an inner and an outer set. As water evaporates, the thicker walls shrink and the collective movement along the columns results in the tooth bending towards that side.

The architecture of the peristome varies and is fundamental to the diagnosis of major lineages (Fig. 4.18). With the exception of Mittenia, cells from three amphithecial layers may contribute to peristome formation: the inner, primary and outer peristomial layer, referred to as the IPL, PPL and OPL, respectively (Fig. 4.18b). Only the outer vertical wall of each IPL remains at

1/8th

1/8th

(c)

Fig. 4.18. Peristome architecture in mosses. (a) Diagram of a transverse section through the putative peristome-forming region at the apex of an immature moss sporophyte. (b) Detail of an eighth of the section in (a), showing the endothecium, e, and the three innermost amphithecial layers that contribute to peristome formation: outer (OPL), primary (PPL) and inner (IPL) peristomial layer. (c-f) Diagram of an eighth of a Timmia-, Funaria-,

Fig. 4.18. Peristome architecture in mosses. (a) Diagram of a transverse section through the putative peristome-forming region at the apex of an immature moss sporophyte. (b) Detail of an eighth of the section in (a), showing the endothecium, e, and the three innermost amphithecial layers that contribute to peristome formation: outer (OPL), primary (PPL) and inner (IPL) peristomial layer. (c-f) Diagram of an eighth of a Timmia-, Funaria-, maturity and only the inner wall of the OPL. In some taxa, one of these layers may be completely disintegrated at maturity. The PPL contributes two walls: the inner one, lying against the IPL wall; and the outer one, attached to the OPL wall. All other walls are degraded (Fig. 4.18c-f). Thus, two concentric rings of teeth may be formed, one composed of the OPL + PPL (the exo-stome) and the other composed of the PPL + IPL (the endostome; Fig. 4.18c, d, f). Some mosses develop a double peristome, others a simple one, consisting only of either the outer or inner ring and others have lost the peristome completely. The number of cell divisions within the three peristomial layers varies. The PPL is typically composed of 16 cells and the OPL of 32, whereas the IPL has between 16 and 64 cells. Consequently, each PPL cell faces 2 outer cells and 1 to 4 inner cells. The exostome and endostome typically comprise 16 teeth each. The outer teeth are often fused into 8 pairs and more rarely divided into 32 teeth. The complexity of the endostome varies along with the architecture of the IPL (Fig. 4.18c, d, f). The teeth, here called segments to distinguish them from the outer teeth, number 16. Divisions within the IPL resulting in more than 32 cells lead to the formation of additional appendages, which, except in Timmia (Fig. 4.18g), are much narrower and smaller than the segments (Fig. 4.18j, k). Endostomial segments and cilia are also often mounted on a basal membrane (Fig. 4.18k). Whereas the divisions within the OPL and PPL are always symmetric, those in the IPL may be conspicuously displaced from the median, resulting in two daughter cells of unequal size (Fig. 4.18e, f). The pattern in number and plane of cell divisions and in the resorption of cell walls defines major peristome types: the diplolepideous opposite (Fig. 4.18d, i) and alternate types (Fig. 4.18f, j), and

Dicranum- and Bryum-type peristome. Black areas identify thickened cell walls composing the peristomes. Dotted lines mark the walls of the IPL, PPL and OPL cells that are resorbed and hence that are not contributing to the peristome. (g) Diplolepideous peristome of Timmia megapolitana, showing the 64 filamentous appendages of the endostome. (h) Outer view of the haplolepideous peristome of Tortula plinthobia. Each tooth is fenestrate along the vertical walls of the IPL and hence one and a half cells of the IPL face each PPL cell (outer cells in view here). (i) Inner view of the peristome of Funaria hygrometrica, showing the four IPL cells composing the two segments, which lie opposite the two exostome teeth. (j) Diplolepideous peristome of Pseudoscleropodium purum, showing the keeled endostome segments alternating with the exostome teeth and the cilia between two consecutive segments. (k) Inner view of the diplolepideous peristome of Mnium thomsonii, showing the numerous cells composing the IPL. Reproduced from Budke et al. (2007) (a-f) and Goffinet et al. 2009 (g-k).

the haplolepideous type (Fig. 4.18e, h). In the diplolepideous peristome, the outer tooth is derived from two columns of cells facing each column of PPL cells (Fig. 4.18c, d, f). In the haplolepideous peristome, each tooth bears the remnants of a single column (Fig. 4.18e). Two rings of teeth occur in most diplolepideous peristomes, whereas haplolepideous peristomes consist of only the endostome. The haplolepideous peristome characterizes the Dicranideae (therefore also referred to as haplolepideous mosses), whereas all other arthrodontous peristomes are of the diplolepideous type. Reduction through the loss of one or both rings, of endostomial cilia, or the truncation of the teeth, has occurred many times independently among mosses (Vitt 1981) and in these cases the architecture at maturity can be phylogenetically misleading.

To release the spores from the capsule, mosses either shed an operculum, have sporangia that dehisce along longitudinal lines or irregularly through the breakdown of the capsule wall. Sphagnum and most other mosses see their spore mass exposed after the capsule looses an apical lid. The loosening and shedding of the operculum is often triggered by the tensions in the annulus, composed of one or more rings of cells with uneven wall thickenings. In Takakia, the capsule dehisces along a spiral line extending nearly to the poles (Fig. 4.2a). In Andreaea and Andreaeobryum, the lines are vertical converging towards, but ending below, the apex, respectively (Fig. 4.2e, f). Mosses occurring in highly seasonal habitats tend to dehisce along an irregular line or randomly as the capsule wall breaks down or is physically damaged. Peristomes occur only in operculate taxa, a pattern consistent with the function of peristomes in controlling spore release. Only Tetraplodon paradoxus bears a peristome, despite the capsule remaining closed at maturity.

Spore dispersal is passive, except in entomophilous Splachnaceae (Box 4.2), and gradual. In Sphagnum, spores become airborne following the implosion of the capsule and the ejection of the operculum. During the final stages of sporangium maturation, gases accumulate inside the capsule. Upon dehydration, the capsule wall collapses inward along the equatorial region bearing the pseudostomata. The compression of the gases results in an increase in pressure, forcing the rapid tearing of the capsule along its line of dehiscence and the explosive release of the operculum. In some nematodontous mosses, the capsule mouth is closed by an epiphragm, a thin membrane spanning the mouth (Fig. 4.17a). It bears minute perforations along its circumference, which prevent spores from being released all at once. Similarly, in arthrodon-tous mosses, the peristome ensures the gradual release of spores. Spreading the dispersal of spores over several days or weeks may increase the likelihood of spores being more widely distributed under different climatic conditions. In some taxa, the peristome overarches the mouth when moist to prevent water

Box 4.2

Fly-mediated spore dispersal in dung mosses

Bryophyte spores are typically dispersed by wind and few may find optimal conditions for their germination and subsequent survival. Targeted dispersal to specific microhabitats would enhance germination rates but requires a vector. Flowering plants often recruit either insects, birds or bats to pick up and deliver pollen grains. Elaborate displays and rewards increase visitations, specificity and effectiveness of delivery. The costs are high, but so are the dividends: fewer pollen grains need to be produced to achieve a given rate of sexual reproduction.

Among seedless embryophytes, only members of the moss family Splachnaceae rely on insects to disperse their spores. Approximately half of the species are coprophilous: they live exclusively on dung or animal remains, which gives the family the common name dung mosses. These substrata are not hostile to other mosses, but the Splachnaceae claim residency before their competitors have a chance to get established. They achieve this by recruiting flies that seek fresh dung and carrion to feed or lay their eggs. To attract the vector, Splachnaceae use deceptive visual and olfactory cues, displayed and emitted by the highly modified sporophyte. The capsules are white, bright yellow, red or deep purple in colour and are often inflated (Box 4.2 Fig. 1). Critical for attracting flies to the sporophyte are the odours mimicking the decaying animal substrata. These volatile compounds are produced by the seta and the apophysis. The chemistry differs between dung and carrion inhabiting species, and the diversity of compounds seems to be inversely correlated to the size of the sporophyte: large, showy sporophytes emit fewer compounds than small, inconspicuous capsules (Marino et al. 2009). Taxa with overlapping geographic ranges may partition the habitat or co-exist. In Patagonia, Tayloria mirabilis lives on cow dung, whereas T. dubyi occurs only on geese dung. Tetraplodon fuegienus is restricted to carnivore dung, like its close relatives from the Northern Hemisphere. In Alaska, Splachnum luteum, S. rubrum and S. sphaericum often coexist on the same patch. The three species produce strikingly different odours and their capsules are highly dissimilar in colour and shape. A diversity of dipterans lands on the sporophyte, which they quickly realize is not the substrate they seek. Visitation time is thus short, but long enough for the fly to come into contact with the protruding mass of sticky spores, which cling to its legs and body. When the fly reaches a patch of fresh dung, or carrion, the spores may fall off. Establishment is rapid and soon a dense population of Splachnaceae colonizes this microhabitat. Dispersal to a specific habitat is thus very effective and relies on highly modified sporophytes that function much like flowers. Unlike pollination, insect-mediated spore dispersal requires a single visitation to be successful. Recruiting insects to disperse spores has obvious advantages and may be critical for a species to occupy such patchily distributed substrate as

dung or carrion. However, the costs are high and the constraints severe: the moss must invest many resources into the synthesis of olfactory and visual cues, and success is guaranteed only if the vector is present. Not surprisingly, phylogenetic inferences suggest that reversion to wind dispersal might have occurred once or more during the evolutionary history of the Splachnaceae (Goffinet et al. 2004).

Box 4.2 Fig. 1. (a) Splachnum luteum: the sterile base of the capsule is expanded to a broad disc, likely designed to display the bright yellow colour and facilitate visitation. (b) Tayloria dubyi: a Patagonian endemic restricted to goose dung on Sphagnum hummocks in bogs. (c) Simple trapping experiments allow researchers to study the diversity of insects recruited by the mosses. See plate section for colour version.

from entering the capsule and triggering the premature germination of spores. The endostome often lacks conspicuous hygroscopic movement in double peristomate mosses. Such attributes may be critical for taxa with pendent capsules to avoid loosing the entire spore mass at once.

The peristome is not the sole structure designed to control spore dispersal. Modifications of the wall or the internal architecture of the capsule may also contribute to regulating the release of spores. Through contraction and expansion in response to changes in atmospheric moisture, the capsule may constrict at the mouth or, more commonly, in the region immediately below. Such changes are, as in other cases of movement, accounted for by uneven degrees of cell wall thickness. This is best seen in ribbed capsules, wherein the ribs are defined by vertical rows of thick-walled cells alternating with bands of thin-walled cells. In some cases, the shrinking is axial, due to thin longitudinal and thick horizontal walls. This movement may promote the exposure of the spore mass upon drying. In Scouleria aquatica, a semi-aquatic species, the operculum is retained on a persistent columella. Spores are dispersed following the vertical contraction of the capsule when exposed to dry air. When moist, the capsule expands and is closed by the lid.

Spores are unicellular. In rare cases the spore, undergoes divisions prior to dispersal. The wall of the spore is composed of sporopollenin, a compound that confers high resistance to mechanical and physiological stress. The outer layer is often patterned and the ornamentation may provide critical information for distinguishing species (Fig. 4.19).

For the completion of its development, the sporophyte depends exclusively on the maternal gametophyte to acquire nutrients and water. Throughout much of its growth, the presumptive sporangial region of the sporophyte is covered by a hood. Following fertilization, the archegonium acquires

Fig. 4.19. Diversity in spore ornamentation. (a) Papillose (Funaria hygro-metrica). (b) Lirellate (Rhachitheciopsis tisserantii). (c) Granulose (Schlothei-mia tecta). (d) Pitted (Rhachithecium papillosa).

a protective function for the developing embryo. The venter and the cauline tissue immediately below form an epigonium, or sac, enclosing the young sporophyte. The epigonium is of determinate size. The pressure resulting from the growth of the sporophyte causes the protective sac to tear. The basal section remains around the base of the seta and the remainder forms a hood, or calyptra, covering part or all of the sporangium. Removal of the calyptra prior to sporogenesis results in aberrations and sporophyte abortions, although it must eventually be shed to allow for capsule dehiscence and spore dispersal. The mechanisms by which the calyptra controls sporophyte development are not fully understood and may be physiological or solely physical. The calyptra offers critical taxonomic characters, diagnostic of species or lineages of higher rank. It varies in size (covering only the opercu-lum or enclosing the entire capsule), in outline (from conical to bell-shaped or long cylindrical), in basal lobing (from entire to broadly or finely incised), in ornamentation (from glabrous to pubescent), in surface relief (from smooth to ridged) and in surface roughness (from smooth to papillose; Fig. 4.20). The calyptra is rarely persistent. Typically, it is blown off by wind. This is facilitated by loosening the fit of the calyptra on the sporangium, either by elevating it via the growth of a long pointed rostrum on the operculum or via curving of the capsule. Cucullate calyptrae bear a longitudinal slit and are typically associated with asymmetric capsules or oblique rostra (Fig. 4.20). Mitrate calyptrae lack such tearing.

Fig. 4.20. Variation in calyptra shape. (a) Long mitrate (and pubescent or hairy) and lobed at base. (b) Short, entire and mitrate. (c) Short cucullate. (d) Long cucullate.

Fig. 4.20. Variation in calyptra shape. (a) Long mitrate (and pubescent or hairy) and lobed at base. (b) Short, entire and mitrate. (c) Short cucullate. (d) Long cucullate.

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