Early fossil land plants of simple construction

Although trilete spores are known from the mid-Ordovician and early Silurian, undisputed vascular plants are not found until halfway through the Silurian. A number of these lack true tracheids (“protracheophytes”) or are insufficiently well preserved to allow us to be sure of the presence of tracheids (“rhyniophytoids”).

The earliest accepted tracheophyte-like plant is Cooksonia. Several species are now known ranging from the upper Silurian to the Lower Devonian. Cooksonia was evidently widespread, occurring in a number of localities in North and South America and Europe. The plants were dichotomously branched (Fig. 6.1a) and probably formed swards, perhaps in swampy areas, a few centimetres in height. The axes, which were bare of any appendages, terminated in reniform (Fig. 6.1b and c) or globose sporangia with little evidence of predetermined sites of dehiscence. So far as known, Cooksonia was homosporous. Vegetative axes of some species have been found with a simple strand of tracheids (true tracheophytes), but others appear to lack them (“rhyniophytoids”). The presence of stomata-like pores has been confirmed only in forms from the earliest Devonian. There is as yet no evidence of extensive aerating systems in Cooksonia which might support the suggestion that carbon dioxide was taken up through the underground organs (as in Isoetes and a few other living plants).

New techniques, such as nucleic acid sequencing and refined methods of spectrographic analysis of plant products, have contributed to the continuing vitality of botanical science, and correspondingly the need for a second edition of Green Plants. Sequence analyses have indicated, for example, the evolutionary distance between the mosses and liverworts, the latter appearing closer to the green algae, and presumably to the early colonists of the land. Chemical analyses have revealed surprisingly that the material thought to be sporopollenin coating the membranes of certain green algae, unlike sporopollenin, is largely aliphatic in nature. The evolutionary significance of this discovery is not yet clear, but it is noteworthy that a chemically similar, acetolysis-resistant, material has been found coating the female gamete in archegoniate plants.

Advances in comparative morphology and paleobotany have also been notable. Penetrating studies of sexual reproduction in the Gnetales have thrown fresh light on the origin of double fertilization as it is seen in flowering plants, and has strengthened the view that the endosperm, unique to the angiosperms, is in origin a second embryo, but remains a tissue in which embryogenesis is normally permanently suppressed. The firm evidence, now available, for certain lowly plants from the Rhynie Chert (Lower Devonian) being gametophytes of the rhyniophytes has confirmed the existence of an archegoniate life cycle in these early colonists of the land.

Green Plants is a thoroughly revised edition of the earlier Diversity of Green Plants by P. R. Bell and C. L. F. Woodcock (3rd edition, London, 1983). The continuing demand for a concise account of the algae and land plants from the point of view of their natural relationships and biology reflects the buoyant state of botanical science. Exciting advances remain a feature of all its aspects. The biophysically minded are revealing in impressive detail the electron pathways in the thylakoid membrane while paleobotanists expand significantly our knowledge of the earliest angiosperms of the Cretaceous and geneticists explore the molecular aspects of plant development. The theme of Green Plants is the astonishing diversity of forms which evolution has provided from the atmospheric carbon fixed by photosynthesis, the remarkable phenomenon which is basic to plant life. The treatment of the Plant Kingdom correspondingly extends from the simplest cellular organisms capable of phototrophy, the prokaryotic algae, to the complexities of the flowering plants, not omitting (so far as they are known) the essential features of the plants represented only by fossils.

The record of plant life provides a striking instance of both genetic conservation and variation. The photochemistry of the thylakoid membrane is presumably basically the same today as it was at the dawn of plant life in pre-Cambrian times, and the genetical system controlling its development likewise essentially unchanged.

SPERMATOPHYTINA (cont.): ANGIOSPERMS (flowering plants)

The angiosperms are the most abundant and widely distributed of the seed-bearing tracheophytes. They are of outstanding economic importance, being the source of many durable hardwoods, most of our vegetable foodstuffs, and about one-quarter (in monetary value) of commercially marketed drugs. They number some 250000 species and show remarkable diversity in growth form, morphology and physiology.

The general features of the angiosperms can be summarized as follows:

Magnoliopsida and Liliopsida

The angiosperms fall into two major classes, the Magnoliopsida (dicotyledons) and the Liliopsida (monocotyledons), in which the embryos are commonly furnished with two or only one cotyledon respectively. These groups also differ in many other features, with distinct trends in leaf venation and form, and flower symmetry.

Polypodiopsida (ferns)

The class Polypodiopsida encompasses both wholly fossil and also living representatives, many of which have a long fossil history. The general features of the class can be summarized as follows:

The living Polypodiopsida fall into six orders, namely the Marattiales, Ophioglossales, Psilotales, Osmundales, Polypodiales and Hydropteridales, referred to collectively as ferns. Of these, the first three orders are eusporangiate (p. 151), while the Polypodiales, and the Salviniales and Marsileales (p. 212) of the now validated Hydropteridales (p. 216), are leptosporangiate (p. 190). The Osmundales have in general leptosporangiate characteristics, but the sporangia develop in a manner recalling that of eusporangiate sporangia. The ferns are an important element of the world's flora, numbering about 10000 species and being particularly conspicuous in warm humid regions. They show the greatest range of growth forms amongst the vascular archegoniates. Although largely herbaceous, a number of ferns of the tropics and subtropics (mostly belonging to the family Cyatheaceae) achieve the form and stature of simple trees.

Biological features of algae

The simplest phototroph imaginable is a single cell floating in a liquid medium, synthesizing its own sugar, and reproducing at intervals by binary fission. Such organisms do in fact exist in both fresh and salt waters. Examples are provided by the cyanophyte Synechococcus (p. 28) and the minute marine Micromonas (Fig. 1.6).

These organisms are examples of algae, the group of plants showing the greatest diversity of any major division of the plant kingdom. They range from minute, free-floating, unicellular forms (represented by both prokaryotes and eukaryotes) to large plants, exclusively marine, several meters in length. Many of the smaller algae form a component of plankton, the communities of minute plants and animals which float at or near the surface of fresh waters and oceans. Algae are responsible for a large part of the photosynthesis in the biosphere, the productivity of some coastal communities in the surf of warm seas exceeding that of the tropical rain forest. Much of the carbon so fixed enters the food chain of the aquatic heterotrophs.

Despite the enormous range in size, the algae remain comparatively simple in organization. In the smaller multicellular species (e.g., Merismopedia, Fig. 2.6; Pediastrum, Fig. 3.8) the cells resemble each other in appearance and function, and they can be regarded as forming little more than an aggregate of independent units.

Algae containing chlorophylls a and b

In proceeding from the “chlorophyll a” to the “a + b” algae a striking difference is seen in the arrangement of the photosynthetic thylakoids. Thylakoids whose membranes contain only chlorophyll a tend to be clearly separate from each other. In the presence of chlorophyll b the apposed faces of the thylakoids are closely appressed, either generally or regionally. The stacking of the thylakoids may be in pairs or in greater numbers. This stacking of the thylakoids remains a feature of the land flora, all of which are “a+b” plants.

Prokaryotic forms

The prokaryotic algae containing chlorophylls a and b are placed in the Prochlorophyta. So far only a few examples are known and the classification is clearly tentative.

PROCHLOROPHYTA

Habitat Symbiotic, freshwater, marine.

Pigments Chlorophylls a, b; β-carotene (α- carotene in one form); zeaxanthin. Biliproteins absent.

Food reserves Starch (where known).

Cell wall components Probably cyanophyte-like.

Reproduction Presumably asexual.

Growth forms Unicellular, filamentous.

Flagella None.

Of the three prochlorophytes discovered Prochloron is the most studied. It is a unicellular extracellular symbiont of colonial ascidians of tropical and subtropical waters. The cells are 10−20μm in diameter, and divide by binary fission. The thylakoids are more or less concentric and closely stacked. A vacuole may be present, but this seems to be more in the nature of an inflated thylakoid than a discrete sac, as in eukaryotic cells.

Characteristics of the living state

The living state is characterized by instability and change. The numerous chemical reactions, called collectively metabolism, within a living cell both consume (in the form of foodstuffs) and release energy. Metabolism is indicative of life. Even the apparently inert cells of seeds show some metabolism, but a mere fraction of that which occurs during germination and subsequent growth. Metabolism depends upon the interaction of molecules in an ordered sequence. If this order is destroyed (for example by poisons or heat) metabolism ceases and the cell dies. In some instances it is possible to arrest metabolism without death. With yeast and some tissue cultures, for example, this can be achieved by very rapid freezing at temperatures of −160°C (−265°F) or lower. The cells can then be preserved in liquid nitrogen (−195°C; −319°F), in an apparently genuine state of “suspended animation”, indefinitely. With yeast up to 95 percent of cells of rapidly frozen cultures resume metabolism and growth following careful thawing.

The sources of energy a cell requires to maintain its dynamic state are predominantly compounds of carbon. In addition a cell requires water, since much of the metabolism takes place in the aqueous phase in the cell. Also essential are those materials necessary for the maintenance of its structure which it is unable to make for itself.

Introduction

Research into the classical genetics of mosses is of long standing (see Cove 1983, Reski 1998) but molecular genetic studies of mosses have been slow to gather momentum and are much less extensive than such studies of flowering plants. Nevertheless, mosses present unique opportunities for the study of plant genetics and development, combining simplicity with technical convenience (see reviews by Cove et al. 1997, Reski 1998, Knight 2000). As a result, molecular genetic studies are gaining impetus. DNA, RNA, and proteins are easy to extract particularly from protonemal tissue and genetic transformation is routine for a number of species. The recent establishment that, in Physcomitrella patens, recombination occurs between a homologous sequence in transforming DNA and the corresponding sequence in the genome, allows not only gene knockout but also the prospect of more sophisticated gene manipulation. Furthermore, the characterization of the homologous recombination system has focused attention on mosses and has already resulted in a considerable increase in the numbers of researchers using moss species for molecular genetic studies.

The most extensively studied moss species at the molecular level is Physcomitrella patens. It was Harold Whitehouse, famous for his genetic research on fungi, but a lifelong bryologist, who suggested that P. patens would be suitable for modern genetic research, and the wild-type strain isolated by him from near Cambridge, UK, remains the stock wild type used in most studies of this species.

Introduction

There is growing consensus within the scientific community that increases in atmospheric methane (CH4) and carbon dioxide (CO2) are enhancing the earth's natural greenhouse effect. Because of the potential effects of these gases on the global energy budget and future climate, there is an urgent need to quantify terrestrial sources and sinks of carbon. Bryophytes are the primary form of carbon storage in many northern ecosystems. There is more carbon stored in Sphagnum and Sphagnum litter (150 × 1012 g) than in any other genus of plants, vascular or non-vascular (Clymo & Hayward 1982). Since the end of the last glacial period (∼ 18 000 y.b.p.), the soils of the northern latitudes have served as a reservoir for terrestrial carbon (Harden et al. 1992). Northern peatlands alone may contain two to three times the amount of carbon stored in tropical rainforests (Post et al. 1982, Gorham 1991). The majority of this carbon has been frozen in permafrost soils and sequestered from atmospheric circulation for thousands of years. On a warming planet, this carbon represents a “ticking time bomb” that could rapidly decompose and increase the amount of CO2 in the atmosphere by as much as 50% (Billings 1997, Goulden et al. 1998). Predicting how the vast stores of soil carbon in moss-dominated ecosystems will be affected by anthropogenic disturbance is critical for models of global climate change.

Experimental studies of morphogenesis in the bryophytes certainly date to the work of von Wettstein early in the 20th century and has its beginnings even earlier. In part because of this extensive history, in part because the mosses, liverworts, and hornworts represent a paraphyletic assemblage that includes three-fourths of the systematic range in land plant lineages, and in part because of the taxonomic diversity within any particular type of bryophyte, the literature in this area is particularly rich and voluminous (to adapt a phrase used by Katherine Esau [1965]). There are many still-excellent reviews in this area, in particular, reviews that concentrate on hormone physiology, as well as book-length treatments of bryophyte development and physiology, including the exhaustive treatments by Chopra and Kumar (1988) and Bhatla (1994).

This chapter will briefly sketch out what is known about hormonal and other external triggers to morphogenesis in the bryophytes, including factors described recently in higher plants but not yet examined in bryophytes. That overview will be followed by case studies, selected for their importance to our understanding of bryophyte biology, their potential for elucidating general features of plant biology, or for their use of novel and generally useful approaches.

Plant growth regulators and bryophyte development

The concept of a plant “hormone” has beguiled botanists for some period of time, and this concept is particularly problematic when botanists restrict their view of plants to just the angiosperms.

Interest in bryophytes has undergone a resurgence in the last decade. This renewed focus on the mosses, liverworts, and hornworts has converged from diverse quarters within the scientific community. With recent advances in DNA sequencing technology and analytical approaches to phylogeny reconstruction, systematists have made unprecedented progress toward reconstructing the “tree of life.” One of the truly monumental events in the history of life was the origin of land plants, or Embryophytes. The bryophytes have long been considered a pivotal group positioned at or near the base of the embryophytes and a great deal of molecular work has recently been aimed at resolving relationships among the disparate groups of bryophytes, and their relationships to the tracheophyte clade (see chapter 4). At the same time, the utility of bryophytes, especially mosses, for analyses of plant function and development has been increasingly appreciated and capitalized upon (see chapter 7). Haploidy and structural simplicity among land plants gives the mosses “added value” for research in functional genomics and several species are presently being utilized as model systems (see chapter 5). The ecological importance of bryophytes has long been appreciated, but recent concerns about the implications of global climate change has focussed renewed attention on some bryophyte-dominated ecosystems, especially boreal peatlands (see chapters 10 and 11).

The idea for this volume came about from two divergent directions. Schofield's recent textbook of bryology is no longer in print, and students in bryology classes have few other succinct options.

Introduction

Except for the marine environment, bryophytes, as a group, are nearly cosmopolitan in distribution. Because of the small size of spores and the frequent occurrence of vegetative propagules, bryophytes are easily dispersed across the landscape. Consequently, many show much wider distribution patterns than the seed plants (Watson 1974). This is especially true at the family and generic levels. The purported greater age of bryophytes may have contributed further to the wider range of bryophytes (Schofield 1992).

The ecological and biological factors shaping the distribution patterns of seed plants have also affected the bryophytes. Indeed, like the seed plants, many bryophyte species found in the arctic and boreal zones are the same in North America, Asia, and Europe. In the tropics, there is a significant number of moss taxa that are pantropical, but the number is far lower when compared to the circumboreal taxa.

Although a great number of bryophyte genera and species are cosmopolitan and distributed throughout different climatic regions, many do exhibit a disrupted or narrow range. The latter represent the uncommon, rare and endemic bryophytes. Their ultimate survival is critically dependent on the preservation of their natural habitats.

Factors affecting the dispersal of bryophyte diaspores

Diaspores are defined as any propagative parts of bryophytes, be they spores or gemmae, capable of giving rise to a new individual. Among the bryophytes, few members, like the moss family Splachnaceae, produce sticky spores that are dependent on flies for their dispersal.

Introduction

The origin of a land flora during the Upper Ordovician–Lower Silurian border (± 440 millions years ago) represents a significant evolutionary event in the history of life. The subsequent evolution of a diverse auto trophic land flora created the conditions necessary for the diversification of a terrestrial hetero trophic fauna (Behrensmeyer et al. 1992). Today the land flora comprises roughly 300000 species distributed among three major groups, the bryophytes, the pteridophytes, and the seed plants. Considering the evolutionary significance of land plants, as well as their dominance and thus their ecological importance in today's biosphere, it is not surprising that evolutionary biologists are investing much time and resources in understanding the transition to land, and the relationships between major lineages of terrestrial plants. Elucidating the evolution of early land plants may allow for a better understanding on how these plants overcame new obstacles encountered in a terrestrial habitat. Character innovations that coincide with exposure to new selective forces can then be examined in a phylogenetic context for their evolutionary significance or potential adaptive value (Knoll et al. 1984, Knoll & Niklas 1987).

Introduction

Recently implicated as the oldest extant lineage of land plants, the anthocerotes hold many clues to the early diversification of terrestrial organisms (Malek et al. 1996, Garbary & Renzaglia 1998, Hedderson et al. 1998, Vaughn & Renzaglia 1998, Beckert et al. 1999, Nishiyama & Kato 1999, Renzaglia et al. 2000). Insights into adaptive strategies that enabled plants to survive during early land radiation and to persist through the millennia are gained through exploration of the morphology and reproductive biology of this ancient plant lineage (Renzaglia et al. in press). Such information also provides an essential foundation for future comparative studies among bryophytes and with basal groups of tracheophytes. In this chapter, we overview the current state of our knowledge on the morphology, ultrastructure, and developmental diversity within the anthocerotes. This information is evaluated from a comparative point of view in a broader context of relationships among streptophyte lineages. Throughout our discussion, we identify future lines of investigation that will provide significant new phylogenetic information on hornworts. Finally, we briefly review the prevalent ideas on the classification of anthocerotes.

Anatomy and development

The description that follows is intended to provide 1) an overview of the unifying morphological features of anthocerotes, 2) a brief survey of diversity in structure among hornwort taxa, and 3) a synthesis of published and unpublished data derived from recent ultrastructural studies.

Only 30 years ago the chemistry of bryophytes was virtually unknown. Recent research on the biology of bryophytes and progress in analytical techniques has resulted in a deeper knowledge about the chemical constituents of bryophytes, although our understanding of their biochemical processes, especially biosynthetic pathways, compared to vascular plants, is still rather poor. In the first part of this chapter the present state of the art regarding the chemistry of bryophytes will be presented, the second part deals with some aspects of chemosystematics, and in the third part knowledge of the biochemistry of bryophytes is summarized. A recent thorough and comprehensive review on the topic has been published by Asakawa (1995). A further review, in 1997, on “heterocyclic compounds in bryophytes” was published by the same author. He deals mainly with secondary metabolites and does not mention inorganic compounds. Primary metabolites are partly discussed, e.g., lipids, carbohydrates, and phaeophytins. Biochemistry was not a topic of his review; this field of research was recently surveyed in Chopra and Bhatla (1990) and Rudolph (1990).

In the section ‘Chemistry of bryophytes’, present knowledge about inorganic compounds and primary metabolites, their structural analogues, and other ubiquitous compounds in bryophytes will be discussed, followed by the main classes of secondary products. The examples mentioned here are selected from recent original papers not cited in Asakawa (1995, 1997); they are more or less confined to those compounds typical of bryophytes in general.

Introduction

Like other bryophytes, liverworts are small, herbaceous plants of terrestrial ecosystems. They share, with the mosses and hornworts, a heteromorphic life cycle in which the sporophyte is comparatively shortlived and nutritionally dependent on the free-living gametophyte, but differ from both in numerous anatomical features as detailed by Crandall-Stotler (1984). Notable among these is that their sporophytes mature completely within the confines of gametophytic tissue, without differentiation of a meristematic zone, and always lack sto mates and a columella. Gametophytes usually grow prostrate on their substrates and are of three fundamental types, 1) a leafy shoot system, 2) a simple thallus, or 3) a complex thallus, with air chambers. Traditionally, liverworts are subdivided into two major groups, the marchantioids and the jungermannioids, based somewhat on these growth forms. For example, complex thalloid organization is restricted to genera of the marchantioid group, while leafy shoot systems are the most common growth form in the jungermannioid group. Only simple thalloid morphologies are expressed in both marchantioid and jungermannioid taxa.

There are an estimated 6000 to 8000 species of liverworts, of which at least 85% are leafy jungermannioids (Schuster 1984a). In general, leafy liverworts possess fairly simple stems and two or three rows of unistratose, frequently divided leaves (Fig. 2.1). Some taxa are isophyllous, with all three rows of leaves transversely inserted, but more commonly, they are anisophyllous with a small row of transversely inserted ventral leaves, or amphigastria, and two rows of larger, obliquely inserted lateral leaves.

Introduction

Peatlands are unbalanced ecosystems where plant production exceeds decomposition of organic material. As a result, organic material, or peat, accumulates. This organic material is composed primarily of plant fragments remaining after partial decomposition of the plants that at one time lived on the surface of the peatland. Decomposition occurs through the action of microorganisms that have the ability to utilize dead plant components as sources of carbon for respiration (Thormann & Bayley 1997) in both the aerobic acrotelm and the anaerobic catotelm (Clymo 1984, Wieder et al. 1990, Kuhry & Vitt 1996). Labile cell contents, cellulose, and hemicellulose are more readily available sources of carbon than recalcitrant fractions that contain lignin-like compounds, with these latter compounds being concentrated in peat by decomposition (Turetsky et al. 2000). Vascular-plant-dominated, tree, shrub, and herb layers produce less biomass (Campbell et al. 2000) and decompose more readily than the bryophyte-dominated ground layer (Moore 1989). Surfaces of northern peatlands are almost always completely covered by a continuous mat of moss (National Wetlands Working Group 1988, Vitt 1990), and the large amount of biomass contained in this layer is composed of cell-wall material that decomposes slowly. This slow decomposition coupled with saturated, anaerobic conditions, cool climate, and/or short growing season allows organic matter to accumulate over large areas. Thus, most peat from northern peatlands is largely composed of a high percentage of material derived from bryophytes.