16–1 A dry-land moss Tortula obtusissima lives on and around limestone in the central plateau of Mexico. Having no roots, the plants obtain their moisture directly from the external environment in the form of dew or rain. They can recover physiologically from complete dryness in less than five minutes.
The Relationships of Bryophytes to Other Groups
In many respects, bryophytes are transitional between the charophycean green algae (page 353) and the vascular plants (discussed in Chapters 17 through 20). Both “bryophytes” and “charophycean green algae” are paraphyletic groups (groups that do not include all the descendants of a single common ancestor)—hence the use of informal names for these groups. Informal names are useful for discussing organisms having similar habitats or adaptations. In the last chapter, we considered some of the features shared by charophytes and plants (bryophytes and vascular plants, which are adapted for life on the land). Both contain chloroplasts with well-developed grana, and both have motile cells that are asymmetrical, with flagella that extend from the side rather than the end of the cell. During the cell cycle, both charophycean green algae and plants exhibit breakdown of the nuclear envelope at mitosis and persistent spindles or phragmoplasts during division of the cytoplasm (cytokinesis). In addition, you may recall that, among the charophycean green algae, the Coleochaetales and Charales appear to be more closely related to the plants than are any others. For example, members of these groups, such as Coleochaete and Chara, are like plants in having oogamous sexual reproduction, that is, a non-flagellated egg cell that is fertilized by a flagellated sperm. In Coleochaete, the zygotes are retained within the parental thallus and, in at least one species of Coleochaete, the cells covering the zygotes develop wall ingrowths. These covering cells apparently function as transfer cells involved with the transport of sugars to the zygotes.
Bryophytes and vascular plants share a number of characters that distinguish them from the charophytes. These shared
16–2 Moss in Antarctica (a) At about 3000 meters elevation on Mount Melbourne, Antarctica, the daily temperatures in summer mainly range from –10° to –30°C. In this incredibly harsh environment, botanists from New Zealand discovered patches of a moss of the genus Campylopus (b), growing in the bare areas visible in the photograph, where volcanic activity produces temperatures that may reach 30°C. The growth of Campylopus in this locality demonstrates the remarkable dispersal powers of mosses, as well as their ability to survive in harsh habitats.
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16–3 Cladogram of embryophytes This cladogram reflects one point of view of the phylogenetic relationships among the bryophyte lineages and between the bryophytes and the polysporangiophytes (plants with branching sporophytes and multiple sporangia). The term “embryophytes,” a synonym for plants, refers to the fact that a multicellular embryo is retained within the female gametophyte (see page 372). This cladogram indicates that the hornworts share a more recent common ancestor with the polysporangiophytes than do the liverworts or mosses and that the liverworts are a sister group to all other embryophytes.
characteristics include: (1) the presence of male and female gametangia, called antheridia and archegonia, respectively, with a protective layer called a sterile jacket layer; (2) retention of both the zygote and the developing multicellular embryo, or young sporophyte, within the archegonium or the female gametophyte; (3) the presence of a multicellular diploid sporophyte, which results in an increased number of meioses and an amplification of the number of spores that can be produced following each fertilization event; (4) multicellular sporangia consisting of a sterile jacket layer and internal spore-producing (sporogenous) tissue; (5) meiospores with walls containing sporopollenin, which resists decay and drying; and (6) tissues produced by an apical meristem. Charophytes lack all of these shared bryophyte and vascular plant characters, which are correlated with the existence of plants on land. Therefore, only the bryophytes and vascular plants are placed in the kingdom Plantae in this book.
Living bryophytes lack the waterand food-conducting (vascular) tissues called xylem and phloem, respectively, that are present in vascular plants. Although some bryophytes have specialized conducting tissues, the cell walls of the bryophyte water-conducting cells are not lignified, as are those of the vascular plants. Also, there are differences in the life cycles of bryophytes and vascular plants, both of which exhibit alternating heteromorphic gametophytic and sporophytic generations. In the bryophytes, the gametophyte usually is larger as well as free-living, and the sporophyte is smaller and permanently attached to, and nutritionally dependent on, its parental gametophyte. By contrast, the sporophyte of vascular plants is larger than the gametophyte and ultimately free-living. In addition,
the bryophyte sporophyte is unbranched and bears only a single sporangium, whereas the sporophytes of extant vascular plants are branched and bear many more sporangia (polysporangiophytes). Vascular plant sporophytes therefore produce a great many more spores than do the sporophytes of bryophytes.
It is quite clear that the bryophytes include the earliest of the extant plant groups. Modern bryophytes can therefore provide important insights into the nature of the earliest landadapted plants and the process by which plants evolved. A comparison of the structure and reproduction of extant bryophytes with those of ancient fossils and living vascular plants can show how various features of vascular plants may have evolved. Research on the moss Physcomitrella patens, whose genome has been sequenced, promises to add substantially to our understanding of plant evolution and diversity (see Figure 16–20). Its role as a model plant system that allows targeting of specific genes is proving to be valuable.
The bryophytes are grouped into three phyla: Marchantiophyta (the liverworts), Bryophyta (the mosses), and Anthocerotophyta (the hornworts). A recent study, involving analyses of three datasets (chloroplast, mitochondrial, and nuclear genes), strongly supports liverworts as sister to all other land plants and also that the hornworts share a more recent ancestor with the vascular plants (Figure 16–3).
Comparative Structure and
Reproduction of Bryophytes
Some bryophytes, namely the hornworts and certain liverworts, are described as “thalloid,” because their gametophytes, which
Comparative Structure and Reproduction of Bryophytes
are generally flat and dichotomously branched (forking repeatedly into two equal branches), are thalli (singular: thallus). Thalli are undifferentiated bodies, or bodies not differentiated into roots, leaves, and stems. Such thalli are often relatively thin, which may facilitate the uptake of both water and CO2. Some bryophyte gametophytes have specialized adaptations on their upper surface for increasing CO2 permeability while at the same time reducing water loss. The surface pores of the thalloid liverwort Marchantia are one such example (Figure 16–4). On the other hand, the gametophytes of some liverworts (the leafy liverworts) and the mosses are said to be differentiated into “leaves” and “stems,” but it could be argued that these are not true leaves and stems because they occur in the gametophytic generation and do not contain xylem and phloem. However, the thalli of certain liverworts and mosses do contain centrally located strands of cells that appear to have conducting functions. Such cells may be similar to ancient evolutionary precursors of phloem and lignified vascular tissues. Inasmuch as the terms “leaf” and “stem” are commonly used when referring to the leaflike and stemlike structures of the gametophytes of leafy liverworts and mosses, this practice will be followed in this book. The true leaves and stems of vascular plants are produced by the sporophytes.
Surface layers reminiscent of the waxy cuticles commonly found on surfaces of the true leaves and stems of vascular plants also occur on the surfaces of some bryophytes. The cuticle of sporophytes is closely correlated with the presence of stomata, which function primarily in the regulation of gas exchange. The pores seen in some bryophyte gametophytes,
such as those of Marchantia, are considered to be analogous to stomata (Figure 16–4). The biochemistry and evolution of the bryophyte cuticle are poorly understood, however, primarily because bryophyte cuticles are more difficult to remove for chemical analysis than are cuticles of vascular plants.
The gametophytes of both thalloid and leafy bryophytes are generally attached to the substrate, such as soil, by rhizoids (Figure 16–4). The rhizoids of mosses are multicellular, each consisting of a linear row of cells, whereas those of liverworts and hornworts are unicellular. The rhizoids of bryophytes generally serve only to anchor the plants, because absorption of water and inorganic ions commonly occurs directly and rapidly throughout the gametophyte. Mosses, in particular, often have special hairs and other structural adaptations that aid in external water transport and absorption by leaves and stems. In addition, bryophytes often harbor fungal or cyanobacterial symbionts that may aid in acquisition of mineral nutrients. Rootlike organs are lacking in the bryophytes.
The cells of bryophyte tissues are interconnected by plasmodesmata. Bryophyte plasmodesmata are similar to those of vascular plants in possessing an internal component known as the desmotubule (Figure 16–5). The desmotubule is derived from a segment of tubular endoplasmic reticulum that becomes entrapped in developing cell plates during cytokinesis (see Figure 3–46). Certain charophycean green algae also possess plasmodesmata.
of most bryophytes resemble those of vascu-
having many small, disk-shaped plastids. All
the cells of
some hornwort species, and the apical and/or
16–4 Surface pores of Marchantia (a) Transverse section of the gametophyte of Marchantia, a thalloid liverwort. Numerous chloroplast-bearing cells are evident in the upper layers, and there are several layers of colorless cells below them, as well as rhizoids that anchor the plant body to the substrate. Pores permit the exchange of gases in the air-filled chambers that honeycomb the upper photosynthetic layer. The specialized cells that surround each pore are usually arranged in four or five superimposed circular tiers of four cells each, and the whole structure is barrel-shaped. Under dry conditions, the cells of the bottommost tier, which usually protrude into the chamber, become juxtaposed and retard water loss, whereas under moist conditions they separate. Thus the pores serve a function similar to that of the stomata of vascular plants. (b) A scanning electron micrograph of two pores on the dorsal surface of a gametophyte of Marchantia.
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16–5 Bryophyte plasmodesmata Longitudinal view of plasmodesmata in the liverwort Monoclea gottschei. Note that the desmotubule in the plasmodesma on the right (arrows) is continuous with the endoplasmic reticulum in the cytosol.
reproductive cells of many bryophytes, by contrast, have only a single large plastid per cell. This characteristic is believed to be an evolutionary holdover from ancestral green algae, which, like modern Coleochaete, probably contained only a single large
Sterile jacket layer
plastid per cell. During cell division, the cells of bryophytes and vascular plants produce preprophase bands consisting of microtubules that specify the position of the future cell wall. Such bands are lacking in the charophycean green algae.
Neck canal cells
16–6 Gametangia of Marchantia, a liverwort (a) A developing antheridium, consisting of a stalk and a sterile—that is, non-sperm-forming—jacket layer enclosing spermatogenous tissue. The spermatogenous tissue develops into spermatogenous cells, each of which forms a single sperm propelled by two flagella.
(b) Several archegonia at different stages of development. An egg is contained in the venter, a swollen portion at the base of each flask-shaped archegonium. When the egg is mature, the neck canal cells disintegrate, creating a fluid-filled tube through which the biflagellated sperm swim to the egg in response to chemical attractants. In Marchantia, the archegonia and antheridia are borne on different gametophytes.
Sperm Are the Only Flagellated Cells Produced by Bryophytes, and They Require Water to Swim to the Egg
Many bryophytes can reproduce asexually by fragmentation (vegetative propagation), whereby small pieces of tissue produce an entire gametophyte. Another widespread means of asexual reproduction in both liverworts and mosses is the production of gemmae (singular: gemma)—multicellular bodies that give rise to new gametophytes (see Figure 16–13). Unlike some charophycean green algae, which can generate flagellated zoospores for asexual reproduction, sperm are the only flagellated cells produced by bryophytes. Loss of the ability to produce zoospores, which are likely to be less useful on land than in the water, is probably correlated with the absence of centrioles from the spindles of bryophytes and other plants (page 64). Mitosis in certain liverworts and hornworts shows features that are intermediate between those of charophycean green algae and vascular plants, suggesting evolutionary stages leading to the absence of centrioles in plant mitosis.
Sexual reproduction in bryophytes involves production of antheridia and archegonia, often on separate male and female gametophytes. In some species, sex is known to be controlled by the distribution at meiosis of distinctive sex chromosomes. In fact, sex chromosomes in plants were first discovered in bryophytes. The spherical or elongated antheridium is commonly stalked and consists of a sterile jacket layer, one cell thick, that surrounds numerous spermatogenous cells, cells
Comparative Structure and Reproduction of Bryophytes
that develop into sperm cells (Figure 16–6a). The “jacket” layer of cells is said to be “sterile” because it cannot produce sperm. Each spermatogenous cell forms a single biflagellated sperm that must swim through water to reach the egg, located inside an archegonium. Liquid water is therefore required for fertilization in bryophytes.
The archegonia of bryophytes are flask-shaped, with a long neck and a swollen basal portion, the venter, which encloses a single egg (Figure 16–6b). The outer layer of cells of the neck and venter forms the sterile protective layer of the archegonium. The central cells of the neck, the neck canal cells, disintegrate when the egg is mature, resulting in a fluidfilled tube through which the sperm swim to the egg. During this period, chemicals are released that attract sperm. After fertilization, the zygote remains within the archegonium, where it is nourished by sugars, amino acids, and probably other substances provided by the maternal gametophyte. This form of nutrition is known as matrotrophy (“food derived from the mother”). Thus supplied, the zygote undergoes repeated mitotic divisions, generating the multicellular embryo (Figure 16–7), which eventually develops into the mature sporophyte (Figure 16–8).
There are no plasmodesmatal connections between cells of the two adjacent generations. Nutrient transport is thus apoplastic—that is, nutrients move along the cell walls. This
transport is facilitated
by a placenta located at the inter-
face between the two
generations, sporophyte and parental
16–7 Marchantia embryo An early stage in development of the embryo, or young sporophyte, of Marchantia. Here the young sporophyte is nothing more than an undifferentiated spherical mass of cells within the enlarged venter, or calyptra.
16–8 Marchantia sporophyte A nearly mature sporophyte of Marchantia, with a distinct foot, seta, and capsule, or sporangium. The placenta is at the interface between the foot and gametophyte and consists of transfer cells of both sporophyte and gametophyte.
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16–9 Bryophyte placenta The gametophytesporophyte junction—the placenta—in the liverwort Carrpos monocarpos. Extensive wall ingrowths develop in the single cell layer of transfer cells
in the sporophyte (upper three cells). There are several layers of transfer cells in the gametophyte (lower left corner), but their wall ingrowths are not as highly branched as those of the sporophyte
layer. Numerous chloroplasts and mitochondria are present in the placental cells of both generations.
gametophyte (Figure 16–9), and therefore analogous to the placenta of mammals. The bryophyte placenta is composed of transfer cells with an extensive labyrinth of highly branched cell wall ingrowths that vastly increase the surface area of the plasma membrane across which active nutrient transport takes place. Similar transfer cells occur at the gametophytesporophyte interface of vascular plants (for example, Arabidopsis and soybean) and at the haploid-diploid junction of Coleochaete (page 357). The occurrence of placental cells in Coleochaete suggests that matrotrophy had already evolved in the charophyte ancestors of plants.
As the bryophyte embryo develops, the venter undergoes cell division, keeping pace with the growth of the young sporophyte. The enlarged venter of the archegonium is called a calyptra. At maturity, the sporophyte of most bryophytes consists of a foot, which remains embedded in the archegonium, a seta, or stalk, and a capsule, or sporangium (Figure 16–8). The transfer cells at the junction between the foot and archegonium constitute the placenta.
The Term “Embryophytes” Is an Appropriate Synonym for Plants
The occurrence of a multicellular, matrotrophic embryo in all groups of plants, from bryophytes through angiosperms, is the basis for the term embryophytes as a synonym for plants (Figure 16–3). The advantage of matrotrophy and the plant placenta is that they fuel the production of a many-celled diploid sporophyte, each cell of which is genetically equivalent to the fertilized egg. These cells can be used to produce many genetically diverse haploid spores upon meiosis in the sporangium. This condition may have provided a significant advantage to early plants as they began to occupy the land. Production of greater numbers of spores per fertilization event may also have helped compensate for low fertilization rates when water became
scarce. The sporophytic generation of plants is thought to have evolved from a zygote, such as those produced by charophytes, in which meiosis was delayed until after at least a few mitotic divisions had occurred. The more mitotic divisions that occur between fertilization and meiosis, the larger the sporophyte that can be formed and the greater the number of spores that can be produced. Throughout the evolutionary history of plants, there has been a tendency for sporophytes to become increasingly larger in relation to the gametophyte generation.
The sporophyte epidermis of mosses and many hornworts contains stomata—each bordered by two guard cells—that resemble the stomata of vascular plants. The moss stomata, however, are able to open and close and thus regulate gas exchange for only a short period after their development. Thereafter they remain open and their function is uncertain. Perhaps they then function to generate a flow of water and nutrients between the sporophyte and gametophyte, induced by the loss of water vapor through the stomata. The hornwort stomata apparently lack the ability to open and close. Once open they remain open. It has been suggested that these stomata are essential for the dehydration and dehiscence (splitting) of the sporangium. The presence of stomata on the sporophytes of mosses and hornworts is regarded as evidence of an important evolutionary link to the vascular plants. Liverwort sporophytes, which are typically smaller and more ephemeral than those of mosses and hornworts, lack stomata. The epidermal cell walls of the moss and liverwort sporophytes are impregnated with decay-resistant phenolic materials that may protect developing spores. Those of the hornwort sporophyte are covered with a protective cuticle.
The Sporopollenin Walls of Bryophyte Spores Have
Bryophyte spores, like those of all other plants,
in a substantial wall impregnated with the most