Sporophyte rootless, with dichotomous rhizomes and aerial branches. Lateral appendages spirally arranged, scale-like or leaf-like. Protostelic (either solid or medullated). Sporangia thick walled, homosporous, terminating very short lateral branches. Antherozoids flagellate.

List 3

This small group of plants is one of great interest to morphologists because its representatives are at a stage of organization scarcely higher than that of some of the earliest land plants, despite the fact that they are living today. Their great simplicity has been the subject of controversy for many years, some morphologists interpreting it as the result of extensive reduction from more complex ancestors. Others accept it as a sign of great primitiveness.

Two species of Psilotum are known, P. nudum (=P. triquetrum) and P.flaccidum (=P. complanatum), of which the first is widespread throughout the tropics and subtropics extending as far north as Florida and Hawaii and as far south as New Zealand. Most commonly, it is to be found growing erect on the ground or in crevices among rocks, but it may also grow as an epiphyte on tree-ferns or among other epiphytes on the branches of trees. P. flaccidum is a much rarer plant, occurring in Jamaica, Mexico and a few Pacific Islands, and is epiphytic with pendulous branches.

The organs of attachment in both species are colourless rhizomes which bear numerous rhizoidal hairs and which, in the absence of true roots, function in their place as organs of absorption. In this, they are probably aided by a mycorrhizal association with fungal hyphae, that gain access to the cortex through the rhizoids. Apical growth takes place by divisions of a single tetrahedral cell which is prominent throughout the life of the rhizome, except when dichotomy is occurring. It is said that this follows upon injury to the apical cell as the rhizome pushes its way through the soil and that two new apical cells become organized in the adjacent regions. In any case, there is no evidence of a median division of the original apical cell into two equal halves; to this extent, therefore, the rhizome cannot be said to show true dichotomy.

In Psilotum nudum, some branches of the rhizome turn upwards and develop into aerial shoots, commonly about 20 cm high, but as much as 1 m high in favourable habitats. Except right at the base, these aerial axes are green and bear minute appendages, usually described as ‘leaves’, despite the fact that they are without a vascular bundle (cf. Psilophyton). The axes branch in a regular dichotomous manner and the distal regions are triangular in cross-section (Fig. 6A). In the upper regions of the more vigorous shoots, the leaves are replaced by fertile appendages (Fig. 6B) whose morphological nature has been the subject of much controversy. Some have regarded them as bifid sporophylls, each bearing a trilocular sporangium, but the interpretation favoured here is that they are very short lateral branches, each bearing two leaves and terminating in three fused sporangia.

Psilotum flaccidum differs from P. nudum in two important respects: its aerial branches are flattened and there are minute leaf-traces which, however, die out in the cortex without entering the leaves (cf. Asteroxylon).

The internal anatomy of the rhizomes varies considerably, according to their size, for those with a diameter of less than 1 mm are composed of almost pure parenchyma, while large ones possess a well-developed stele. Fig. 6C is a diagrammatic representation of a large rhizome, as seen in transverse section. In the centre is a solid rod of tracheids with scalariform thickenings. As there is no clear distinction between metaxylem and protoxylem, it is impossible to decide whether the stele is exarch, mesarch or endarch. Around this is a region which is usually designated as phloem, although it is decidedly unlike the phloem of more advanced plants, for its elongated angular cells are often lignified in the corners. Surrounding this is a region of ‘pericycle’, composed of elongated parenchymatous cells, and then comes an endodermis with conspicuous Casparian strips in the radial walls. Three zones may often be distinguished in the cortex, the innermost of which is frequently dark brown in colour because of abundant deposits of phlobaphene (a substance formed from tannins by oxidation and condensation). The middle cortex consists of parenchymatous cells with abundant starch grains, while the outer cortex contains, in addition, the hyphae of the mycorrhizal fungus. In some cells the mycelium is actively growing while in others it forms amorphous partially digested masses.

Psilotum nudum

In the colourless, or brown, transitional region at the base of the aerial axes, the xylem increases in amount, becomes medullated and splits up into a variable number of separate strands. This process of medullation continues higher up the stem, as shown in Fig. 6D, and the central pith region becomes replaced by thick-walled fibres. There is here a transition from the protoxylem, with its helical or annular helical thickenings, to scalariform metaxylem tracheids, the protoxylem being exarch. The xylem is surrounded by a region of thin-walled cells, not clearly separable as phloem and pericycle, and the whole stele is enclosed in a well marked endodermis. The cortex is again divisible into three regions, the innermost containing phlobaphene, the middle region being heavily lignified and the outermost being photosynthetic. The chlorophyllous cells in this outermost region are elongated and irregularly ‘sausage shaped’, with abundant air spaces between them, which connect with the stomata in the epidermis. The leaves are arranged in a roughly spiral manner in which the angle of divergence is represented by the fraction J, but although internally they are composed of chlorophyllous cells like those of the outer cortex of the stem, they can contribute little to the nutrition of the plant, for they are without stomata as well as having no vascular supply.

In this last respect, the leaves are in marked contrast to the fertile appendages, for these each receive a vascular bundle, which extends to the base of the fused sporangia, or even between them. In their ontogeny, too, they are markedly different from the leaves, for they grow by means of an apical cell, whereas the young leaf grows by means of meristematic activity at its base. Shortly after the two leaves have been produced on its abaxial side, the apex of the fertile appendage ceases to grow and three sporangial primordia appear. Each arises as a result of periclinal divisions in a group of superficial cells, the outermost daughter cells giving rise, by further divisions, to the wall of the sporangium, which may be as much as five cells thick at maturity. The inner daughter cells provide the primary archesporial areas, whose further divisions result in a mass of small cells with dense contents. Some of these disintegrate to form a semi-fluid tapetum, in which are scattered groups of spore-mother cells, whose further division by meiosis gives rise to tetrads of cutinized spores.

The genus Tmesipteris is much more restricted in its distribution than Psilotum, for T. tannensis is known only from New Zealand, Australia, Tasmania and the Polynesian Islands, while another species, T. Vieillardi, is probably confined to New Caledonia. (Some workers recognize a further four species, of restricted distribution, although it is possible that they warrant no more than subspecific status.) T. tannensis most commonly grows as an epiphyte on the trunks of tree-ferns or, along with other epiphytes, on the trunks and branches of forest trees, in which case its aerial axes are pendulous, but occasionally it grows erect on the ground. By contrast, T. Vieillardi is more often terrestrial than epiphytic. It may further be distinguished by its narrower leaves and by certain details of its stelar anatomy.

Like Psilotum, Tmesipteris is anchored by a dichotomous rhizome with rhizoidal hairs and mycorrhizal fungus hyphae. The aerial axes, however, seldom exceed a length of 25 cm and seldom branch or, if they do so, then there is but a single equal dichotomy. Near the base, the aerial axes bear minute scale-like leaves very similar to the leaves of Psilotum, but elsewhere the branches bear much larger leaves, up to 2 cm long, broadly lanceolate and with a prominent mucronate tip (Fig. 6E). Their plane of attachment is almost unique in the plant kingdom, for they are bilaterally symmetrical, instead of being dorsiventral. They are strongly decurrent, with the result that the stem is angular in transverse section and they each receive a single vascular bundle which extends unbranched to the base of the mucronate tip, but does not enter it. In the distal regions of some shoots, the leaves are replaced by fertile appendages which, like those of Psilotum, may be regarded as very short lateral branches, each bearing two leaves and terminating in fused sporangia (normally two) (Figs. 6F-6H).

The internal anatomy of the rhizome is so similar to that of Psilotum that the same diagram (Fig. 6C) will suffice to represent it. In the transition region of Tmesipteris tannensis (Fig. 61), the central rod of tracheids becomes medullated and splits up into a variable number of strands which are mesarch (in contrast to the exarch arrangement in Psilotum). (T. Vieillardi differs in having a strand of tracheids that continues up into the aerial axis in the centre of the pith region.) Whereas in the rhizome there is a well marked endodermis, in the aerial axes no such region can be discerned. Instead, between the pericycle and the lignified cortex, all that can be seen is a region of cells packed with brown phlobaphene. The outer cortex contains chloroplasts, but the epidermis is heavily cutinized and is without stomata. These are restricted to the leaves (and their decurrent bases) which, like the stem, are also covered with a very thick cuticle, but in which are abundant stomata. The leaf-trace has its origin as a branch from one of the xylem strands in the stem and consists of a slender strand of protoxylem and metaxylem tracheids surrounded by phloem. As the stem apex is approached, the number of groups of xylem tracheids is gradually reduced (Fig. 6J), all the tracheids being scalariform, even to the last single tracheid.

The vascular strand supplying the fertile appendages branches into three, one to each of the abaxial leaves and one to the sporangial region. The latter branches into three again in the septum between the two sporangia. The early stages of development closely parallel those in Psilotum, giving rise to thick-walled sporangia containing large numbers of cutinized spores. Both sporangia dehisce simultaneously, by means of a longitudinal split along the top of each.

When discussing the morphological nature of the fertile appendages of the Psilotales, morphologists have made frequent reference to abnormalities (the study of which is referred to as ‘teratology’). In both genera, the same types of variation occur, some of which are represented diagrammatically in Figs. 6L and 6M. The normal arrangement is indicated in Fig. 6K — a lateral axis (shaded) terminating in a sporangial region (black) and bearing two leaves (unshaded). In Fig. 6L one of the leaves is replaced by a complete accessory fertile appendage, while in Fig. 6M both leaves are so replaced and instead of the sporangial region there is a single leaf. There has for a long time been a widely held belief that freaks are ‘atavistic’, i.e. they are a reversion to an ancestral condition. However, it must be stressed that this belief rests on very insecure foundations. As applied here, the conclusion has been that the reproductive organs of the Psilotales are reduced from something more complex, at one time assumed to have been a fertile frond. It may well be, however, that the only justifiable conclusion is that, at this level of evolution, leaf and stem are not clearly distinct as morphological categories, and that they are freely interchangeable — interchangeable on the fertile appendages of abnormal plants, just as, on any normal shoot, fertile appendages replace leaves in the phyllotaxy.

Psilotum nudum - development

Few botanists have had the good fortune to see living specimens of the gametophyte (prothallus) stage of either Psilotum or Tmesipteris, but all who have testify, not only to their similarity to each other, but also to their remarkable resemblance to portions of sporophytic rhizomes. So similar are the prothalli and sex organs of Psilotum to those of Tmesipteris that the same diagrams and descriptions will suffice for both. Like the rhizomes the prothalli are irregularly dichotomizing colourless cylindrical structures, covered with rhizoids (Fig. 7A), and the similarity is further enhanced by the fact that they are also packed with mycorrhizal fungus hyphae. Both archegonia and antheridia are borne together on the same prothallus (i.e. they are monoecious), but because of their small size they cannot be used in the field to distinguish prothalli from bits of rhizomes. Stages in their development are illustrated in Figs. 7B-H (archegonia) and 7I-M (antheridia).

The archegonium is initiated by a periclinal division in a superficial cell (Figs. 7B and 7C) which cuts off an outer ‘cover cell’ and an inner ‘central cell’. The cover cell then undergoes two anticlinal divisions, followed by a series of periclinal divisions to give a long protruding neck, composed of as many as six tiers of four cells. The central cell, meantime, divides to produce a ‘primary ventral cell’ and a ‘primary neck canal cell’ (Fig. 7F). Beyond this stage there are several possible variants, only one of which is illustrated in Fig. 7G, where the primary ventral cell has divided to give an egg cell and a ventral canal cell, while the nucleus of the primary neck canal cell has divided without any cross wall being laid down. In the mature archegonium, however, most of the cells break down so as to provide access to the egg cell from the exterior, through a narrow channel between the few remaining basal cells of the neck, whose walls, in the meantime, have become cutinized (Fig. 7H).

The antheridium, likewise, starts with a periclinal division in an epidermal cell (Fig. 7I). The outer cell is the ‘jacket initial’ whose further divisions in an anticlinal direction give rise to the single-layered antheridial wall, while the inner ‘primary spermatogenous cell’ gives rise to the spermatogenous tissue, by means of divisions in many planes (Fig. 7L). At maturity (Fig. 7M) the antheridium is spherical, projects from the surface of the prothallus and contains numerous spirally coiled multifiagellate antherozoids (Fig. 7S). These escape into the surrounding film of moisture and, attracted presumably by some chemical substance, find their way by swimming to the archegonia, where fertilization occurs.

Stages in the development of the young sporophyte from the fertilized egg are illustrated in Figs. 7N-R. The first division of the zygote is in a plane at right angles to the axis of the archegonium (Fig. 7O) giving rise to an outer ‘epibasal cell’ and an inner ‘hypobasal cell’. The latter divides repeatedly to give a lobed attachment organ called a ‘foot’ (Fig. 7Q), while the epibasal cell, by repeated divisions, gives rise to the first rhizome, from which other rhizomes and aerial shoots are produced. Fig. 7R shows a young sporophyte with three rhizomatous portions and a young aerial shoot, the whole plant being still attached to the gametophyte. This kind of embryology, where the shoot-forming apical cell is directed outwards through the neck of the archegonium, is described as ‘exoscopic’. While relatively unusual in pteridophytes, it is nevertheless universal in mosses and liverworts. Indeed, the young sporophyte of the liverwort Anthoceros is very similar indeed to that of Tmesipteris, at least up to the stage illustrated in Fig. 7Q even in such details as the lobed haustorial foot, and some morphologists have gone so far as to suggest some sort of phylogenetic relationship. However, until more is known of the factors which determine the polarity of developing embryos, such suggestions should be received with considerable caution.

For many years there has been speculation among botanists as to the kind of life-cycle that might have been exhibited by the earliest land plants. Some held the belief that there was a regular alternation of sporophytes and gametophytes that resembled each other in their vegetative structure and that even their reproductive organs (sporangia and gametangia, respectively) could be reconciled as having a similar basic organization: on this basis, the generations were regarded as ‘homologous’. Others believed that the sporophyte generation evolved after the colonization of the land by gametophytic plants. From being initially very simple, the sporophyte then evolved into something much more complex, by reason of its possessing far greater potentialities than the gametophyte. On this basis, the generations were regarded as ‘antithetic’. Until bona fide gametophytes are described from the Devonian, or earlier, rocks, there is little hope that this controversy will be resolved satisfactorily. All that can be done is to examine the most primitive living land plants and see whether, at this level of evolution, the sporophyte appears to have fundamentally different capabilities.

The extremely close similarity in external appearance between the gametophytes of the Psilotales and their rhizomes is, therefore, of more than passing interest. Until 1939, however, it was believed that there was one important anatomical distinction between them, in that gametophytes were without vascular tissue. In that year, Holloway described some abnormally large prothalli of Psilotum from the volcanic island of Rangitoto, in Auckland harbour, New Zealand. These were remarkable in having well-developed xylem strands, of annular and scalariform tracheids, surrounded by a region of phloem which, in turn, was enclosed by a clearly recognizable endodermis. There was, therefore, almost no morphological feature distinguishing them from the sporophytic rhizomes, except their archegonia and antheridia. It was subsequently found that the cells of these prothalli contained twice as many chromosomes as those from Ceylon (i.e. they were diploid), while the sporophytes from this locality were tetraploid. To some botanists, this appeared to be sufficient to explain the presence of vascular tissue, and tended to diminish the importance of the similarity of these gametophytes to the rhizomes. But it must be emphasized that diploid prothalli are known elsewhere among pteridophytes and that no morphological aberration need necessarily accompany a simple doubling of the chromosome number. This being so, then, whatever their chromosome content, these abnormal vascularized prothalli still provide strong support for the Homologous Theory of Alternation of Generations. This topic is discussed further in the final chapter.

Concerning chromosome numbers generally in the group, it now appears that all plants of Psilotum nudum from Australia and New Zealand have the same chromosome number n = 100 - 105, while plants from Ceylon are like Psilotum flaccidum in having about half this number (n = 52 - 54). Tmesipteris tannensis has a chromosome number n = 200+, while of the six new species (or subspecies) recognized by Barber five have n = 204 - 210 and one has n = 102 - 105. It is suggested that both Psilotum and Tmesipteris occur in polyploid series, but that both have the same basic number.