Despite the fungal mode of nutrition figuring prominently in originally defining kingdom Fungi (Chapter 1), the fundamental aspect of cell biology which sets the fungi off from other major kingdoms is the apical growth of hyphae. Extension growth of the hypha is limited to the apex. Growth at the tip is what makes new fungal hypha, but there is more to development than growth at hyphal tips can achieve alone. The vegetative fungal mycelium is an exploratory, invasive organism. Its component hyphae are regulated to grow outwards into new territory and consequently possess controls which ensure that hyphae normally grow away from one another to form the typical ‘colony’ with an outwardly-migrating growing front (see Carlile, 1995). Tissue development requires that different hyphae cooperate in an organised way. For tissue to be formed the invasive outward growth pattern of the vegetative mycelium must be modified so that independent hyphal apices grow towards each other, allowing their hyphae to branch and differentiate in a cooperative fashion.

Since the developing structures (spore-forming fruiting bodies, for instance) are actually produced by the vegetative mycelium, these changes in growth pattern must be localised, and must be a response to regulatory processes which are imposed upon the vegetative mycelium. Another aspect of localisation is that tissue formation demands that the continuous tube of hypha produced by the growing apex is divided up into cells or compartments by the formation of cross-walls (usually called septa).

The biochemical capabilities summarised in Chapter 3 are used in a variety of ways during morphogenetic processes in fungi. In this chapter I will describe and discuss some of these. Throughout this account from now on my emphasis will be on finding general principles to weave into an overall model of fungal morphogenesis. Experimental observations, of course, deal with specific cases under particular conditions. I will describe some of these specific cases but, as I cannot describe them all, I have selected examples which seem to me to illustrate particular points which need to be included in any overall picture of morphogenesis. Other examples can be found in the literature and I will make reference to some of them. Furthermore, by attempting to generalise from the few cases I can illustrate, I will be relying on making inductive inferences, some of which will, inevitably, be more reliable than others. It is necessary to take the risk of being wrong in order to get some view of the overall picture.

The variety of data in the literature indicates that the major events in the growth and differentiation of a mycelium are essentially as follows. During growth of the vegetative hyphae a large proportion of the nutrients adsorbed from the substratum is stored. Different organisms use the different storage compounds (polysaccharide, protein, oils and fats and polyphosphates) to different extents.

I will now attempt to summarise the discussion and present an interpretation of plausible mechanisms for control of fungal morphogenesis. Because the data are so fragmentary, this will involve extensive generalisations and potentially outrageous extrapolations. I am aware of the dangers of over-interpretation. Generalisations from a few specific cases which combine incomplete information from organisms of arguable comparability does not make the best science. At the moment there is not much choice. My motive is to produce a developmental model which can be tested by further research. So this chapter comes with the challenge: if you don't like the ideas presented here, then fill the gaps in the knowledge. Do the research to prove me wrong.

The nature of morphogenetic control

The first lesson to learn from other organisms bears on the question of the ultimate level of morphogenetic control. It is clear that in animals and plants morphogenesis is not simply a matter of playing out a predefined genetic program and it is likely that this will be true for fungi also. Goodwin (1984) states that the “developmental process involves principles of organisation which are not caused by genes in the way that computer output is caused by a program.” Instead, he argued that macro-molecular and cellular structures, such as the cytoskeleton and endomembrane system, provide a more promising foundation for describing the forces which define morphogenetic fields during animal embryogenesis.

In this chapter I present an account of the ways in which fungal hyphal systems obtain, absorb, metabolise, reprocess and redistribute nutrients. The description is relatively brief and more details can be found in texts on fungal physiology, such as Jennings (1995).

This material is relevant here for a number of reasons. First, these metabolic and biochemical activities of fungi provide the background and context within which their differentiation and morphogenesis occur. In discussing differentiation and morphogenesis there will be frequent need to refer to biochemical processes and it is useful to have those details readily to hand for reference. Second, fungi adapt the metabolism which normally serves their vegetative hyphal growth phases in specific ways to provide for and support their morphogenesis. Consequently, description of the basic metabolism is a valuable preparation for understanding the ways in which it is adapted. Third, description of basic metabolism provides another opportunity to make comparisons with the other eukaryotic kingdoms and to show, again, how kingdom Fungi make use of advanced and sophisticated mechanisms in the management of their cell biology.

Almost all of the processes described in this chapter will appear in some guise again in discussions of fungal morphogenesis in later chapters.

Nutrients in nature

Texts on fungal physiology usually present lists of chemicals that fungi can utilise when added to culture media.

This book is aimed at all biologists. Certainly, I started out with the intention to write a biological text rather than a mycological one because I believe the fungi are too important to remain in an intellectual ghetto in some faintly plant-like place which most people visit rarely, and then with unease.

Throughout, I have attempted to blend together physiological, biochemical, structural and molecular descriptions within an evolutionary framework, combining the older literature with the most recent. Without attempting a comprehensive description of fungi, I hope that I have provided sufficient information about fungal biology to give the general reader a rounded view of the mycological context within which fungal morphogenesis is played out without obscuring the broader biological significance. If I have got the balance right, the reader with knowledge of basic biology should not need to bring any other knowledge with him or her, nor need to refer elsewhere, in order to appreciate fungal morphogenesis.

The first chapter aims to give an overview of the evolutionary origins of fungi and the central role they played (and still play) in the evolution of life on Earth. The second chapter introduces hyphal growth, the essence of the fungal lifestyle, and identifies features which are crucial aspects of morphogenesis. Chapter 3 summarises fungal primary and secondary metabolism, necessary here because adaptation of primary metabolism and exploitation of secondary metabolism are both critical to fungal morphogenesis.

Since Lewontin & Hubby (1966) and Harris (1966) independently discovered allozyme polymorphisms within populations of Drosophila and humans, allozymes have provided the most widely used descriptors of genetic diversity in natural plant and animal populations. Their usefulness can be ascribed to several features, including codominant expression, apparent neutrality, and ease and cost of detection. Today allozymes are utilized in studies of plant populations to determine breeding systems, describe mating systems, determine paternity, estimate gene flow via seed and pollen, examine clonal structure, and determine systematic relationships (Soltis & Soltis, 1989). In conservation biology and crop science, the description of genetic structure provides sampling guidelines for the ex situ and in situ preservation of genetic diversity (e.g. Marshall & Brown, 1975; Brown & Briggs, 1991; Godt, Hamrick & Bratton, 1995; Swenson et al., 1995; Godt & Hamrick, 1996). Furthermore, allozymes have been utilized to study the evolution of crop species and to identify cultivars (Doebley, 1989; Torres, 1989).

Although allozyme diversity does not necessarily reflect variation in quantitative traits, it provides a handy yardstick for comparisons of diversity within populations and across species. Over 1000 published studies report allozyme variation in seed plants. These represent a wide crosssection of the plant world, although commercially valuable species (i.e. trees and crops) and temperate species have received the most attention. As the number of allozyme studies has grown, several reviewers have described patterns in allozyme diversity and its distribution (Gottlieb, 1977; Brown, 1979; Hamrick, Linhart & Mitton, 1979; Crawford, 1983; Hamrick & Godt, 1989).

Introduction

The majority of herbaceous plant roots growing in natural ecosystems are colonized by the arbuscular mycorrhizal (AM) fungi, otherwise known as the vesicular-arbuscular mycorrhizal (VAM) fungi (Trappe, 1987). These are relatively primitive fungi belonging to six genera (Acaulospora, Entrophospora, Gigaspora, Glomus, Sclerocystis and Scutellospora) in the order Glomales and class Zygomycetes (Morton & Benny, 1990). Despite their simplicity, these fungi have become the main mutualistic organisms associated with grasses, with the possible exception of clavicipitaceous leaf endophytic fungi (see Clay, this volume). AM fungi typically enter plant roots via root hairs from either chlamydospores in the root zone or more commonly from other colonized roots (Read, Koucheki & Hodgson, 1976) and form comparatively broad and typically non-septate hyphae within roots. These give rise to finely branched haustoria, termed arbuscules, which have a high surface area in contact with the plant plasmalemma and which are usually considered to be the point of nutrient exchange between the fungus and its host (Smith & Gianinazzi-Pearson, 1988). Large terminal or intercalary structures termed vesicles develop at later stages in the colonization of roots (Vietti & van Staden, 1990). These contain fatty acids, lipids and sterols (Jabaji-Hare, Deschene & Kendrick, 1984) and are usually thought to be storage organs.

Since AM fungi are heterotrophic, they rely upon their plant host for up to 20% of carbon fixed in leaves (Wang et al., 1989) in what Harley (1975) referred to as ‘a direct short-circuiting of photosynthesis’. In return, the fungus generally confers benefits on its plant host, most notably in the acquisition of phosphorus (P), a highly immobile element in soil which is therefore frequently limiting to plant growth.

Introduction

Perennial grasses are a predominant component of the savanna and grassland biomes of sub-Saharan Africa. Savannas constitute more than half of the land surface area of this region. True grasslands are less widespread, occurring mainly in mid-latitude or high-altitude regions or as smaller fragments depending on local edaphic or climatic conditions (O'Connor & Bredenkamp, 1997). The terms grassland and savanna disguise the variation in climate and environmental conditions associated with each. Perennial grassland (true or savanna) can be encountered in regions receiving rainfall of as little as 150 mm yr−1 or as much as 1200 mm yr−1; they may occur in areas which experience snowfall in winter or areas of tropical climate; they may be found on leached, dystrophic, sandy soils or on extremely fertile volcanic, clay soils; they may be burned on an annual basis or have 20 or more years pass without experiencing a fire; most are associated with the remarkable adaptive radiation of African ungulates whilst others are barely subject to herbivory by large mammals; they are at the heart of a pastoral enterprise which directly supports a greater human population than any other pastoral enterprise in the world.

The variation in climate and environment is matched by a diversity of species and growth forms. In southern Africa alone there are 723 species of perennial grass (Gibbs Russell et al., 1990). A community may contain caespitose, stoloniferous or rhizomatous growth forms; swards may be a 5– cm-high grazing lawn or 3 m tall when flowering; swards may consist of scattered individuals or have a closed canopy.

Introduction

The caryopsis (hereafter called seed) germination stage of the life cycle of grasses is of much interest to (1) agriculturalists establishing fields of cereals to be harvested for grain, (2) range and grassland managers revegetating overgrazed or otherwise disturbed lands, (3) weed specialists attempting to control weeds in crops, pastures, lawns, and even in natural plant communities and (4) ecologists investigating plant life histories and the dynamics of plant populations, communities and ecosystems. Through experience, agriculturalists, land managers, weed biologists and ecologists have come to realize that the seeds of many grasses are difficult to germinate; consequently, much research has been done on their dormancy and germination. In fact, Simpson (1990) published a book entitled Seed Dormancy in Grasses. However, this wonderful compendium of information was written from a physiological point of view and, therefore, does not devote much attention to the ecological perspective of seed germination.

The importance of knowing about the germination ecology of grasses is illustrated by the fact that in moist temperate regions, where precipitation is not a limiting factor per se, seeds of grasses germinate in (1) autumn, (2) spring, (3) autumn and spring, (4) summer, (5) spring, summer and autumn or (6) spring and summer, depending on the species (Brenchley & Warington, 1930; Roberts & Ricketts, 1979; Roberts & Potter, 1980). Further, in seasonally wet regions grasses have distinct germination phenology patterns (Mott, 1972, 1978; Silva & Ataroff, 1985; Evans, Kay & Young, 1975).

Introduction

Over the last three decades, evidence has accumulated showing that plant species originating from nutrient-poor habitats tend to have a lower growth potential – i.e. when measured under optimal environmental conditions in the laboratory – than species from nutrient-rich habitats (e.g. Bradshaw et al., 1964; Grime & Hunt, 1975; reviews in Chapin, 1980,1988 and Lambers & Poorter, 1992). Whereas the adaptive value of a high growth potential is relatively clear, that of a low one has been the subject of much debate (Chapin, 1980,1988; Lambers & Dijkstra, 1987; Berendse & Elberse, 1990; Aerts & van der Peijl, 1993). One of the most convincing hypotheses currently put forward is that rather than the growth rate itself, it is one of its underlying components (namely the specific leaf area, the ratio of leaf area to leaf dry mass) which is the target of selection (Lambers & Dijkstra, 1987; Lambers & Poorter, 1992).

Species from habitats differing in fertility (or differing in growth potential) also exhibit differences in plasticity, defined as a variation in morphology and/or physiology in response to changes in environmental conditions (Schlichting, 1986). It has commonly been observed that the growth rate of species from nutrient-poor habitats (and slow-growing species) is less sensitive to a variation in external nutrient supply than that of species from nutrient-rich habitats (and fast-growing species: reviews in Chapin, 1980, 1988 and Lambers & Poorter, 1992). Furthermore, plants respond to nutrient stress by altering simultaneously a number of other traits: for example, when nitrogen availability decreases, internal plant nitrogen concentration decreases and biomass allocation to roots increases (both reviewed in Larsson, 1994).

Introduction

Grasses have many interesting features of their population biology that are explored in detail in this volume. One of the most unique features of grasses is their symbiotic association with systemic fungal endophytes (Clavicipitaceae, Ascomycota) that grow within or on aboveground plant parts. These fungi can have significant effects on all aspects of the grass life cycle from germination and establishment to growth and reproduction. The population biology of grasses therefore varies with their endophyte infection status.

Plant population biology research has focused on describing patterns of recruitment, survival and reproduction, and on investigating how resource levels, density and genetic variability affect these processes. Increasing attention is being given to microbial symbioses in plant population dynamics (Burdon, 1987; Allen, 1991; Jarosz & Davelos, 1995). Mycorrhizal fungi infecting grasses enhance nutrient uptake and plant vigour, and alter interactions with pathogens and competitors (Hartnett et al., 1993; Stanley, Koide & Shumway, 1993; Newsham, Fitter & Watkinson, 1995; Newsham & Watkinson, this volume). Other mutualistic microbes in the rhizosphere and phyllosphere of grasses also occur (Turkington et al., 1988; Bever, 1994). For example, a nitrogen-fixing bacterial endophyte in the stems of sugar cane contributes most or all of the plant's nitrogen requirements (Dong et al., 1994). Fungal pathogens have been better studied compared with mutualists, especially in agricultural systems where grasses predominate (Burdon, 1987; Dinoor & Eshed, 1984; Clay, 1995). In contrast with mutualists, pathogens reduce the survival, growth and reproduction of host grasses (Mack & Pyke, 1984; Clay, Cheplick & Marks, 1989; Van der Putten, Van Dijk & Peters, 1993; Fowler & Clay, 1995; Govinthasamy & Cavers, 1995).

Plants do not experience average population densities or overall levels of resource supply. Spatial structure of plant populations and communities is an important consequence of the sessile nature of plants and of the discrete quality of individual organisms (Silvertown & Lovett Doust, 1993; Tilman, 1994). Close neighbours exploit the same resources, endure the same macro- and microenvironmental controls, and interact more or less independently with herbivores, pathogens and mutualistic organisms. Although plant–plant interactions are affected by all these factors, in this chapter we will focus on direct effects between neighbours and individual interactions mediated by resource exploitation. The remaining influences are covered elsewhere in this volume (see Chapters 9, 10 and 11).

The reciprocal effects between plants and their local environment are modulated by their life cycle. Establishment, resource acquisition, growth, recruitment, and death all affect and are affected by attributes of the local environment or neighbourhood. These continuous interactions among plants and their local environment are experienced by close neighbours over a range of temporal scales. The results of these interactions ramify upwards through the system to affect population, community, and ecosystem level properties.

In our analysis of plant–plant interactions, we will first deal with the spatial pattern of individuals, focusing on neighbourhood characteristics and their significance for individual performance and the recruitment of new individuals. We will then turn our attention to competitive ability. Here we will discuss both the effects of grasses on resource availability as well as the response of grasses to resource availability. We will end with an evaluation of the significance of plant-plant interactions for community and ecosystem processes.

Introduction

The life history characteristics of bamboos differ conspicuously from other grasses in their peculiar flowering habits. Many bamboo species are long-lived monocarpic plants (McClure, 1966; Janzen, 1976; Soderstrom & Calderon, 1979; Simmonds, 1980; Veblen, 1982; Dransfield & Widjaja, 1995). In temperate regions in particular, the bamboos have long flowering intervals, estimated at 100 years or more (Janzen, 1976; Campbell, 1985). They often flower simultaneously over an extensive area and then die (Taylor & Qin 1988; Makita, 1992, Makita et al., 1993).

Bamboos often form exclusive dense populations with vigorous rhizomatous vegetative reproduction. After mass flowering and death, their populations recover mainly by the development of seedling cohorts (Veblen, 1982; Taylor & Qin, 1988; Makita, 1992; Makita et al., 1993). In clonal plants, the phase just after germination seems to be the most vulnerable period in their life history (Langer, Ryle & Jewiss, 1964; Kays & Harper, 1974; Cook, 1979; Solbrig, 1980; Bierzychudek, 1982; Liddle, Budd & Hutchings, 1982). Bamboos similarly suffer high mortality during seedling growth (Taylor & Qin, 1988; Makita, 1992, Makita et al., 1993). After die-off of bamboos, many other species may be able to invade the bamboo stands because light conditions at ground surface are improved considerably (Nakashizuka, 1988; Taylor & Qin, 1988; Makita, 1992). Especially in forests with an undergrowth of bamboos, the mass death of bamboos provides opportunities for tree regeneration (Veblen, 1982; Nakashizuka, 1987, 1988; Taylor & Qin, 1988, 1992, 1997; Taylor, Qin & Liu, 1995; Makita, 1997; Widmer, 1997). Thus the simultaneous flowering and death of bamboos is an important episodic event in the local vegetation dynamics.