Introduction

The majority of fungi have a filamentous lifestyle. The evolution of the hypha has been pivotal to the success of filamentous fungi and in determining the uniqueness of their lifestyle. It has also had important consequences in determining the modes of morphogenesis of filamentous fungi, and how they operate as non-motile, heterotrophic organisms (Read, 1994). This review focuses on hyphal and colony morphogenesis and how it is influenced by environmental signals in the context of the filamentous fungal lifestyle.

The supracellular, cellular and multicellular nature of filamentous fungi

The defining cellular element of the filamentous fungi is the hypha (Figs. 3.1–3.6). Hyphae possess a unique combination of structural, behavioural and functional attributes that clearly distinguish them from uninucleate animal and plant cells. The vegetative hypha is a tip-growing cellular element (Harris et al., 2005) (Figs. 3.1, 3.2) that undergoes regular branching (Trinci, 1983; Turner & Harris, 1997) (Figs. 3.3, 3.4), is typically multinucleate (Fig. 3.3) (Freitag et al., 2004), and possesses incomplete cross-walls (septa) which, when open, allow movement of cytoplasm and organelles between hyphal compartments (Harris, 2001) (Fig. 3.2). In sub-peripheral regions of the colony, hyphae frequently fuse with one another (Read & Roca, 2006) (Fig. 3.3) and septal pores often become blocked (Gull, 1978) (Fig. 3.2). Vegetative hyphae thus have a supracellular nature because they are part of a network of interconnected hyphal compartments and hyphae within the colony (Fig. 3.1).

Introduction

The mycorrhizal symbiosis is characterized by a reciprocal exchange of photosynthetically-fixed plant carbon in return for the main plant-growth-limiting nutrients, nitrogen or phosphorus. Studies of mycorrhizal functioning have focused on their roles in providing nutrients to plants, but their importance as a significant component of the terrestrial carbon (C) cycle has generally been overlooked. However, over 80% of plant species invest substantial amounts of their below-ground C flow into these fungal symbionts (Smith & Read, 1997; Leake et al., 2004). At the global scale, the annual C flux through soil respiration is ten times greater than fossil fuel combustion and recycles c. 10% of atmospheric CO2 (Raich et al., 2002). Roots and associated mycorrhizas are the single most important component of this flux. Knowledge of the mycorrhizal contribution to the C cycle is of increasingly paramount importance, as this component is likely to be among the most sensitive to ongoing anthropogenic disturbance of both C (Staddon et al., 2002) and nitrogen (N) biogeochemical cycles (Nilsson & Wallander, 2003).

The major biomes are dominated by plants with one of three kinds of mycorrhiza (Fig. 8.1), each of which is adapted to the particular vegetation and soil characteristics of the bioclimatic regions in which it is most important (Read et al., 2004). Central to understanding the contributions of mycorrhizas to the plant–soil–atmosphere continuum of the C cycle is appreciation of the properties and functions of these three major types of mycorrhiza and the ecosystems in which they are of greatest importance.

Fungi are ubiquitous in the aquatic and terrestrial environments, occurring as unicellular yeasts, polymorphic and filamentous fungi, and as both free-living and symbiotic forms. In the terrestrial environment, that part of the biosphere most closely associated with fungal activities, fungi are of fundamental importance as decomposer organisms, plant pathogens and mutualistic symbionts (mycorrhizas and lichens), playing important roles in carbon, nitrogen and other biogeochemical cycles. In soil they can comprise the largest pool of biomass (even exceeding that of other microorganisms and invertebrates) and also play a role in maintenance of soil structure owing to their filamentous branching growth habit and exopolymer production. Despite their important roles in the biosphere, fungi are frequently neglected within broader environmental and microbiological spheres, in contrast to bacteria. For example, symbiotic mycorrhizal fungi can be associated with the majority of plant species and are responsible for major transformations and re-distribution of inorganic nutrients as well as carbon flow, while free-living fungi have major roles in decomposition and solubilization of plant and other organic materials, including xenobiotics, and low-solubility phosphate compounds. As well as this general neglect, mycological interests can be somewhat fragmented between traditional microbiological and botanical activities and the fields of cell biology, plant symbiosis, and pathogenesis and genetics. This symposium volume provides a unique account of modern environmental mycology and includes accounts of major recent advances in molecular, imaging and modelling methodologies, which have the potential to draw together these disparate areas of mycology.

Lichen symbiosis

Lichen-forming fungi are a polyphyletic group of nutritional specialists, which derive fixed carbon from a population of living cyanobacteria and/or green algal cells. Every fifth fungus (approximately 14,000 species), or every second ascomycete, respectively, is a lichen. Species names of lichens refer to the fungal partner, the photoautotrophic symbionts having their own names and phylogenies. Most lichen-forming fungi are physiologically facultatively biotrophic, but occur in nature almost exclusively in the symbiotic state.

The majority of lichen-forming fungi form crustose, often quite inconspicuous thalli on or within the substratum where they meet their photoautotrophic partners, but about 25% of lichen mycobionts differentiate morphologically and anatomically complex 3-D thalli, either shrubby, leaf- or band-shaped, erect or pendulous, which are the result of an amazing hyphal polymorphism. Morphologically and anatomically complex lichen thalli are sophisticated culturing chambers, built up by the fungal partner, for a population of minute photobiont cells. Most lichen-forming fungi grow at or even above the surface of the substratum in order to keep their photoautotrophic partner adequately illuminated. Thus they are exposed to solar radiation, drought and temperature extremes. Lichen-forming ascomycetes produce a wide range of poly-phenolic secondary metabolites, which crystallize at hyphal surfaces in the medullary layer and/or within the peripheral cortex, giving the thalli a characteristic coloration (Huneck & Yoshimura, 1996). Most of the cortical secondary compounds absorb ultraviolet (UV) light and transmit longer wavelengths, thus protecting fungal and photobiont cells from radiation damage.

Introduction

Fungal evolution and cell biology

Fungi are one of three major clades of eukaryotic life that independently evolved multicellular organization. They have radiated into a large variety of terrestrial and aquatic niches, employing strategies ranging from symbiotic to saprobic to pathogenic, and are remarkable for their developmental diversity and ecological ubiquity, with the number of species estimated to exceed one million (Hawksworth et al., 1995).

The fungi are highly varied in their mode of growth, ranging from unicellular yeasts to multicellular hyphal forms that produce complex fruiting bodies (Hawksworth et al., 1995). Hyphae grow through polarized tip-extension of a tubular cell (hypha), which can be partitioned by the formation of cross-walls called septa. Phylogenetic analysis reveals four major groups of fungi: the early-diverging Chytridiomycota and Zygomycota, and the Ascomycota and Basidiomycota (Fig. 2.1) (Berbee & Taylor, 2001; Lutzoni et al., 2004), which are sister clades that evolved more recently and contain the majority of fungal species (Bruns et al., 1992; Hawksworth et al., 1995). Hyphae are the predominant mode of vegetative cellular organization in the fungi and groups of fungi can be defined based on consistent differences in hyphal structure. The Zygomycota and Chytridiomycota can produce septa but these are infrequent in vegetative hyphae. In contrast, vegetative hyphae in the Ascomycota produce perforate septa at regular intervals and this is also found in the Basidiomycota, suggesting that this trait was present in their common ancestor (Fig. 2.1) (Berbee & Taylor, 2001).

Introduction

The fungal cell wall has been considered for a long time as an inert organelle but recent studies, mainly based on the analysis of the yeast cell wall, suggest that it is indeed a dynamic structure where constitutive polymers are continuously chemically modified and rearranged during morphogenesis. The cell wall plays an essential role in sensing adverse or favourable environments. In particular, it provides the fungus with adaptative responses to variable osmotic pressures and other stress factors including host defence reactions. The cell wall is continuously in contact with the host and acts also as a sieve and a reservoir for molecules such as enzymes, antigens, and elicitors or toxins that play an active role during infection (Mouyna & Latgé, 2001).

The major component of the cell wall is polysaccharide. It accounts for over 90% of the cell wall mass and and consists of three basic components: glucans, mannan and chitin (Fig. 13.1). The fibrillar skeleton of the cell wall is considered to be the alkali-insoluble fraction, whereas the material in which the fibrils are embedded is alkali-soluble (Fontaine et al., 2000). The central core of the cell wall is branched β1,3, β1,6 glucans that are linked to chitin via a β(1–4) linkage (Fontaine et al., 2000). This core is present in most fungi, and at least in all ascomycetes and basidiomycetes. The alkali-soluble amorphous cement varies with the fungal species; its composition has been analysed in few fungal species.

Leaf Morphology and Anatomy

Angiosperm leaves display much morphological and anatomical diversity. Mature leaves of monocots are typically narrow and consist of a linear lamina with parallel venation and a leaf base that ensheathes the stem. This contrasts with the typical leaf of eudicots and magnoliids, which has a well-defined petiole and elliptical blade (lamina) with reticulate venation. However, exceptions and transitional forms are common; for example, leaves of some monocots (e.g. Dioscorea and Smilax) are petiolate and net-veined, and leaves of some eudicots (e.g. some Apiaceae) are linear. Some species possess compound leaves in which individual leaflets are borne either on a central stem-like axis (pinnate leaves; e.g. tomato, Solanum lycopersicum) or radiate from a single point at the distal end of the petiole (palmate leaves; e.g. Arisaema).

Some species that grow in dry (xeric) or seasonally dry habitats, or otherwise nutrient-deficient habitats, possess specialized xeromorphic features, including sunken stomata to minimize water loss and well-developed sclerenchyma to provide mechanical support and minimize tissue collapse. Other xeromorphic features include the presence of a hypodermis or thick epidermis and thick cuticle which diminish the intensity of light that reaches photosynthetic tissue. Well-developed palisade tissue is also sometimes correlated with high light intensity. Some xeromorphic species possess thick, sometimes even succulent, leaves; others have terete (centric or cylindrical) leaves, or hairy leaves, or even folded (plicate) or rolled leaves (Fig. 4.1).

In the twenty-first century, plant anatomy remains highly relevant to systematics, paleobotany, and the relatively new science of developmental genetics, which interfaces disciplines and utilizes a combination of techniques to examine gene expression in growing tissues. Modern students need to consider information from an increasingly wide range of sources, most notably integrating morphological and molecular data. The third, thoroughly revised, edition of this book presents an introduction to plant anatomy for students of botany and related disciplines.

Although the simple optical lens has been used for centuries to examine plant structure, detailed studies of plant anatomy originated with the invention of the compound microscope in the seventeenth century. Nehemiah Grew (1641−1712) and Marcello Malpighi (1628−1694), physicians working independently in England and Italy respectively, were early pioneers of the microscopical examination of plant cells and tissues. Their prescient work formed the foundation that eventually led to the development of our understanding of cell structure and cell division. Other early outstanding figures included Robert Brown (1773−1858), who discovered the nucleus, and the plant embryologist Wilhelm Hofmeister (1824–1877), who first described the alternation of generations in the life cycle of land plants. In the nineteenth and twentieth centuries plant anatomy became an important element of studies of both physiology and systematic biology, and an integral aspect of research in the developing field of anatomical paleobotany, led by such luminaries as Dukinfield Henry Scott (1854−1934). The physiologist Gottlieb Haberlandt (1854–1945) utilized anatomical observations in his ground-breaking work on photosynthetic carbon metabolism.

Organs

Plants consist of several organs, which in their turn are composed of tissues. Broadly, vegetative organs support plant growth, and reproductive organs enable sexual reproduction. The three main types of vegetative organ are the root, stem and leaf. Roots typically occur underground, and extract moisture and nutrients from the soil, though there are many examples of plants with aerial roots. The stem and leaves together comprise the shoot (Fig. 1.1). Stems occur both above and below ground. Some stems are modified into underground perennating or storage organs such as corms or rhizomes. Leaves typically occur above ground level, though some underground stems possess reduced scale leaves, and underground bulbs possess swollen leaves or leaf bases.

Primary organs and tissues develop initially from the shoot and root apical meristems and from cell divisions in meristems closely adjacent to them, such as the primary thickening meristem. Secondary tissues such as secondary xylem (wood) develop from lateral meristems such as the vascular cambium. Organs such as adventitious roots develop from differentiated cells that have retained meristematic capacity. At the onset of flowering, the shoot apical meristem undergoes structural modification from a vegetative to a reproductive apex and subsequently produces flowers (chapter 5). Flowers are borne on an inflorescence, either in groups or as solitary structures. A group of inflorescences borne on a single plant is termed a synflorescence (Fig. 1.2).

Primary Root Structure

The seedling radicle ultimately becomes the primary root (tap root), which frequently develops side branches (lateral roots). In monocots the seedling radicle commonly dies at an early stage; the stem-borne (adventitious) roots of the mature plant originate from differentiated cells (Fig. 3.4). Adventitious roots can be branched or unbranched. Although roots can originate from various organs, their basic primary structure retains a characteristic root groundplan that is different from that of the stem. Each root possesses clearly-defined concentric tissue regions: dermal tissue (epidermis), ground tissue (cortex, including the endodermis) and central vascular tissue surrounded by a pericycle (Fig. 3.3).

Root Apex

Root apices possess a terminal protective root cap and a proximal root apical meristem (Fig. 3.1). The quiescent centre is a group of relatively inactive cells at the very centre and tip of the root apical meristem. The cells of the quiescent centre divide infrequently; their role is obscure, but they maintain initial cells in an undifferentiated state. These cells, together with the root cap initials, are derived from the uppermost cell of the suspensor (hypophysis) in the embryo (Fig. 6.7). Cell division activity occurs in the cells surrounding the quiescent centre. In Arabidopsis thaliana the initial cells lie in clearly defined regions relative to the quiescent centre, the pericycle and vascular initials proximal to it (on the shoot side), the root cap and epidermis initials distal to it (on the root cap side) and the cortical and endodermal initials radial to it.

Seed Coat

The seed coat prevents destruction of the seed by dehydration or predation. In bitegmic seeds the testa is derived from the outer integument, and the inner integument forms the tegmen (Fig. 6.1). In unitegmic seeds the term “testa” applies to the entire seed coat. Seed coats are multilayered tissues; they generally include a hard, protective mechanical layer that is formed from all or part of the testa or tegmen. In exotestal seed coats the mechanical layer is derived from the outer epidermis of the outer integument, whereas in endotegmic seed coats it is derived from the inner epidermis of the inner integument. In some species the mechanical layer consists of one or more rows of elongated, palisade-like cells, such as the macrosclereids in the exotesta of many Fabaceae.

Seed coat surfaces exhibit a variety of cellular patterns, often with characteristic papillate or striate surface sculpturing (Fig. 6.2). Some seeds possess epidermal trichomes; for example, the seed coat hairs of Gossypium (cotton) are an important source of textile fibres.

Seed-coat vasculature usually consists of a single bundle passing from the raphe to the chalaza, but this can vary in extent and degree of branching. Many seed coats possess specialized structures that are related to dispersal. For example, some wind-dispersed seeds possess wings, and some animal-dispersed seeds are fleshy. The fleshy part of the seed coat, termed the sarcotesta, is most commonly formed from part of the outer integument. Arils are fleshy outgrowths of the funicle.

Shoot Apex

The vegetative shoot apex contributes to extension growth of the shoot and initiates leaf primordia. Most shoot apices are indeterminate, though some (e.g. shoot thorns) become determinate. The vegetative shoot apical meristem is typically dome-shaped and partitioned by distinct zones of activity (Fig. 2.1). In many species, the outermost two (sometimes more) cell layers (L1 and L2, collectively termed the tunica) are maintained predominantly by anticlinal cell divisions. The corpus (L3), in which cell divisions are randomly oriented, is the region proximal to the tunica. Thus, the outer layers contribute to surface growth and the inner layers to an increase in volume, though there is often slight intergradation between the two layers.

The central regions of both tunica and corpus are sometimes larger and more highly vacuolated than those on either side. The central region underlying the corpus layer is a rib meristem; this gives rise to files of cells that later become the pith. This central region is surrounded by a peripheral flank meristem that produces the procambium, cortical region and leaf primordia.

Reproductive shoot apices are complex examples of determinate growth. During the transition to the flowering phase (termed floral transition), the shoot apex commonly undergoes profound morphological change, though the tunica/corpus structure is maintained. In general, at floral transition there is an overall increase in mitotic activity at the shoot apex, but a proportionally greater increase among the axial apical cells than among the peripheral cells.

Floral Organs

Flowers are complex structures that consist of several organ types borne on a central axis (the receptacle). In many species each flower is subtended by a modified leaf-like structure termed a bract (Fig. 1.2), though bracts are absent from some other species. Within each flower, the organs are arranged in distinct bands (whorls) or in a spiral pattern (Figs 5.1, 5.2). The degree of fusion of individual floral organs within each flower is normally characteristic of a species (i.e. genetically determined). Fusion between similar organ types borne in the same whorl is termed connation. Fusion between different organ types borne in adjacent whorls is termed adnation.

The outer two types of floral organs (collectively the perianth) are modified leaf-like structures, termed sepals (collectively the calyx, or sometimes the first whorl) and petals (collectively the corolla, or the second whorl). In many monocots and magnoliids the perianth organs are morphologically indistinguishable from each other, and are collectively termed tepals, rather than differentiated into sepals and petals. Enclosed within the perianth are the stamens, which are collectively termed the androecium, or sometimes the third whorl, though they are often borne in two or more distinct whorls.