Fungal Lifehistory Strategies

Saprotrophism

One of the most obvious and essential activities of fungi today is the degradation of plant and animal tissue. Without this activity, life on Earth would cease. As a result of the carbon cycle, atmospheric CO2 is fixed into organic molecules in plants via photosynthesis. Then after the plant dies, it is ultimately degraded by fungi (and bacteria); this process in turn releases the CO2 back into the atmosphere.

One of the oldest examples of saprophytism comes from Late Devonian specimens of the progymnosperm wood mor-photaxon Callixylon (Stubblefield et al., 1985a). Inside many of the secondary xylem tracheids are numerous hyphae (FIG. 3.76), some branching and exhibiting intercalary swellings (FIG. 3.77). The surface of some filaments is smooth, whereas others have numerous rounded knobs. In addition to these specimens in the wood, some of the cells of the vascular rays contain spherical structures, which were interpreted as fungal resting spores or ergastic deposits. In some areas of the wood, the tracheid walls are characterized by erosion troughs, which represent areas that have been delignified by the enzymatic activities of the fungus. The patterns produced on the tracheid walls in Callixylon are similar to those formed by living basidiomycetous fungi responsible for white rot (Otjen and Blanchette, 1986). In this particular example, the fossil fungi cannot be identified with certainty, but features of the degradation process provide information about the level of fungus-plant interaction. The production of lignified, secondary tissues (wood) by vascular plants had evolved in some groups by the

Plants That Provide Wood
FIGURE 3.76 Callixylon tracheid containing fungal hyphae (Devonian). Bar = 35 pm.

Givetian (Middle Devonian). Today, fungi continue to be the primary decomposers of lignin in the ecosystem. The presence of wood-rotting fungi in Callixylon, one of the oldest known trees (Meyer-Berthaud et al., 1999), provides compelling evidence that this important saprophytic association between fungi and vascular plants arose around the same time that wood development began. Fossil evidence of this association also provides a proxy record of the type of decay process and the basidiomycetes that were responsible for it. For example, white rot (degradation of both cellulose and lignin) and brown rot (degradation of only the cellulosic part of the wall) can be distinguished by observing tracheid cell walls in fossil wood.

As noted earlier, wood-rotting fungi in several Paleozoic and Mesozoic woods from Gondwana produced symptoms of white pocket rot similar to those seen in extant wood. One of the interesting aspects of the fungi responsible for white pocket rot is their apparently long geologic history. The woody plants they infected in the Paleozoic and Mesozoic are long extinct, but the fungi appear to have produced the same features in

Saprophytism Relationship
FIGURE 3.77 Septate hypha with terminal chlamydospore in Callixylon wood (Devonian). Bar = 12 pm.

wood for several hundred million years. Does this mean that the relationships between certain types of fungi and woody plants coevolved as the fungi continued to adapt to new plant hosts? Perhaps the enzymatic system responsible for selective wood degradation evolved several times or in multiple groups of fungi, or perhaps the microenvironment of wood is so similar in all gymnosperms that fungi, once adapted to this habitat, showed little change. It may be possible to answer questions such as these in the near future by using molecular or isotopic techniques applied to modern and fossil wood-rotting fungi.

Parasitism

Simply stated, parasites live at the expense of other organisms (FIGS. 3.78, 3.79). Living fungi demonstrate a variety of interactions with their hosts, including those that obtain nourishment without causing death (biotrophs), those that absorb nutrients from dead tissues (necrotrophs), those that cause disease (pathogens), those in which the partners provide mutual benefits (mutualists), and a variety of intermediate levels of interaction. Of all the potential levels of

FIGURE 3.78 Seedling of Picea baltica with Gonatobotryum piceae (arrow) at the base of the unfolding cotyledons (Eocene). Bar = 1 mm. (Courtesy A. Schmidt.)
Gonatobotryum
FIGURE 3.79 Gonatobotryum piceae, young conidiophores showing apical conidiogenesis (Eocene). Bar = 50pm. (Courtesy A. Schmidt.)

interaction between fungi and other organisms, parasitism is perhaps the most difficult to demonstrate and distinguish from saprotrophism in the fossil record. Without clear evidence of some host response to the infection, this type of interaction appears similar to saprophytism and even mutualism when examined in fossils. In some instances, the plant host may show several different responses to fungal invasion, further complicating our understanding of specific interactions (Oliver and Ipcho, 2004). One of the best examples of host response in living plants involves the production of swellings or appositions on the inner surface of cell walls (FIG. 3.80). In extant plants, such structures form in response to the invasion of fungi and are regarded as a mechanism by the host to isolate the fungus from uninfected cells nearby. Examples of cell wall appositions in tissues heavily infected with fungal hyphae are known from Late Pennsylvanian coal ball material of Illinois (Stubblefield et al., 1984a). In the Rhyme chert plant, Nothia aphylla, three different fungal endophytes were found in the plant axes (FIGS. 3.81, 3.82)

Endophytes Wood
FIGURE 3.80 Section of Araucarioxylon wood showing wall appositions (arrows) (Triassic). Bar = 50 |im.
Paleozoic Fungi Taylor
FIGURE 3.81 Cortical cell in rhizoidal ridge of Nothia aphylla containing numerous fungal spores (Devonian). Bar = 30 |im.

(Krings et al., 2007a). Parts of the rhizome have hypodermal cells with thickened walls (FIG. 3.83) (Krings et al., 2007a). Other parts show areas that are devoid of cells (FIGS. 3.84, 3.85), or include degraded cells, suggesting that the host may have responded to infection through programmed cell death. Both responses are seen in living plants and function to prevent further spreading of the parasite. The production of resinous material (FIG. 3.86) is another response to fungal invasion of living plant tissue. This type of host response has been noted in wood of Callixylon newberryi from the Upper Devonian and may be more widespread in fossil woods, but as yet underreported.

Pathogenic fungi are believed to be responsible for the symptoms found in Late Triassic tree trunks in the Petrified Forest of Arizona (Creber and Ash, 1990) (FIG. 3.87). In cross section the fossil wood shows numerous tubes associated with

FIGURE 3.82 Nothia aphylla rhizoid with swollen area containing endophytic fungi (Devonian). Bar = 60 |im.
Endophytic Fungus
FIGURE 3.83 Partial section of Nothia aphylla rhizoidal ridge and host response to fungal attack in the form of zigzag line (arrows) of secondarily thickened cell walls (Devonian). Bar = 500 ^m.
Roots Attacked Actinomycetes
FIGURE 3.84 Nothia aphylla rhizoidal ridge axis showing rhiz-oids and space where tissue is lacking (Devonian). Bar = 60 |im.
Parenchyma Elm
FIGURE 3.85 Section of Nothia aphylla rhizoidal ridge showing void in response to fungal attack (Devonian). Bar =100 pm.
FIGURE 3.86 Ray parenchyma cells of Callixylon newberryi containing globules (Devonian). Bar = 25 pm. (From Stubblefield etal., 1985a.)

areas of disrupted cells. Similar symptoms are known in living trees and are associated with the extant fungi Heterobasidion and Armillaria. The large number of trees with similar symptoms at the same stratigraphic level suggests that perhaps the forest was attacked on a large scale, much like the action of modern Dutch Elm disease (Creber and Ash, 1990).

FIGURE 3.87 Geoffrey Creber (left) and Sidney R. Ash.

Another interesting host response which has been observed in fossils is hypertrophy, an abnormal increase in cell size. A charophyte alga (Chapter 4) from the Rhynie chert, Palaeonitella cranii, shows greatly enlarged cells in response to infection by the fossil chytrid Krispiromyces discoides (FIGS. 3.88, 3.89) (Taylor et al., 1992). The consistent presence of this chytrid embedded in the walls of the hypertrophied algal cells indicates that the alga was alive when infection took place, and that the abnormal increase in cell size represents a host response (FIG. 3.90 ). Interestingly, identical examples of hypertrophy have been reported in the extant charophyte Chara (Karling, 1928). Other forms of chytrid parasites are reported in and on various other fungi in the Rhynie chert (FIG. 3.91) (Hass et al., 1994). For example, chlamydospores associated with the AM fungus Glomites rhyniensis contain papillae extending from the inner surface of the spore wall (FIG. 3.92) which are identical to those produced in living glomeromycotan (FIG. 3.93) spores attacked by chytrids (Boyetchko and Tewari, 1991). Other spores have minute holes like those produced by certain actinomycetes (Lee and Koske, 1994). These examples of mycoparasitism (FIG. 3.94) underscore just a few of the microbial dynamics that occurred in and around the freshwater pools of the Rhynie ecosystem in the Early Devonian.

FIGURE 3.88 Section of hypertrophoid cell of Palaeonitella with chytrid (Krispiromyces discoides) (arrow) penetrating cell wall (Devonian). Bar = 80 pm.

FIGURE 3.89 Krispiromyces discoides (see FIG. (Devonian). Bar = 25 pm.

FIGURE 3.90 Two hypertrophoid cells of Palaeonitella cranii. Arrow indicates normal cell size of axis (Devonian). Bar = 275 pm.

FIGURE 3.89 Krispiromyces discoides (see FIG. (Devonian). Bar = 25 pm.

FIGURE 3.90 Two hypertrophoid cells of Palaeonitella cranii. Arrow indicates normal cell size of axis (Devonian). Bar = 275 pm.

Fungal parasitism of fossil plants can also be inferred based on particular characteristics of the fungus. For example, in certain epiphyllous fungi growing on middle Eocene (Paleogene) angiosperm leaves from the Claiborne Formation of Tennessee, haustoria and haustorial pores were found in many of the leaves (Dilcher, 1965). Although the possibility exists that these fungi obtained their nourishment

Devonian Plants Fossils
FIGURE 3.91 Spore tightly packed with coenocytic hyphae. Arrow indicates possible discharge papilla of fungus (Devonian). Bar = 10pm. (From Hass et al., 1994.)
FIGURE 3.92 Chytrid (arrow) on surface of chlamydospore. Note host response in form of papilla inside spore wall (Devonian). Bar = 20 pm.

from some other source (e.g., host leaf excretions or exudates from animals), the presence of haustoria like those of modern parasitic fungi, and the reaction of the leaf to this pattern of penetration, suggests that these fungi parasitized the angiosperms on which they grew.

Mutualism

Mutualistic interactions are those symbioses in which both partners benefit from the relationship. Most of those that have been reported in the fossil record involve mycorrhizal fungi

Mycorrhiza Chlamydospore
FIGURE 3.93 Chlamydospore of extant glomeromycotan fungus showing host response in the form of wall papillae. Bar = 100 pm.
Fungi Devonian
FIGURE 3.94 Parasitic or saprotrophic fungi inside glomeromycotan spore (Devonian). Bar = 80 pm.

and vascular plants; lichens are another example of a mutu-alistic association (discussed later). For endomycorrhizal fungi, the existence of such interrelationships in the fossil record has been based on the presence of non-septate hyphae and various forms of vesicles and chlamydospores within the underground rhizomes or aboveground prostrate axes of permineralized vascular plants. Since their initial description in tissues of the Rhynie chert plants, the occurrence of variously shaped spores and hyphae in these plants has been used as the basis for establishing the early occurrence of endomycorrhizal associations. Based on the presence of such structures, Pirozynski and Malloch (1975) hypothesized that such fungal-plant interactions were necessary for the establishment of plants on the land (Chapters 6, 8). According to these authors, the fungi in this mutualistic association would be provided with a carbon source, whereas the land plants would benefit from increased nutrients and more efficient water uptake from the substrate. Some of the chlamydospores and hyphae that are so common in the Rhynie chert plants may also represent the remains of sapro-phytic fungi (Taylor and White, 1989). Others, however, confirm the existence of arbuscular mycorrhizae based on well-defined arbuscules in a restricted zone of the cortical tissues (Taylor et al., 2005c) in both sporophytes and game-tophytes (FIG. 3.95). Although a morphological structure

FIGURE 3.95 Hypha (arrow) extending through gametangi-ophore stalk of Lyonophyton rhyniensis (Devonian). Bar = 35 |im.

cannot be used to conclusively demonstrate a physiological function in a fossil plant, the direct correspondence between arbuscule formation in extant and fossil plants, including location within the host plant and morphology of the arbus-cules (FIG. 3.96), is striking. Other forms of evidence, such as molecular sequence data calibrated to molecular clock assumptions, also support the existence of endomycorrhizal symbioses by the Early Devonian (Simon et al., 1993). It is hypothesized that one selective advantage of mycorrhizae is the ability to increase the plant's uptake of phosphorus via the extended hyphal network. This certainly may have been an important attribute in what must have been a nutrient-poor substrate during the Early Devonian of the Rhynie site. Unfortunately the earliest land plants ( Cooksonia-type organisms) are preserved as impressions or compressions, and so their mycorrhizal status is unknown. Molecular biology does suggest, however, that the Glomeromycota extend well back into the Paleozoic (Berbee and Taylor, 2001; Taylor and Berbee, 2006), and even into the Precambrian based on some accounts (Heckman et al., 2001). By conservative estimates this would mean that by the time of the Early Devonian Rhynie ecosystem, fungal relationships with plants were well established, and this is borne out by morphological and structural features of both the host and the fungus.

Generally the underground organs of fossil plants, unless they are petrified or permineralized, are not studied in great detail. There is sufficient permineralized plant material available today, including roots, however, from many different geologic horizons and representing most of the major groups of plants, that a systematic study looking for endomycorrhizae

FIGURE 3.96 Detail of arbuscules in Aglaophyton major cortical cells (Devonian). Bar = 30 |im.

FIGURE 3.95 Hypha (arrow) extending through gametangi-ophore stalk of Lyonophyton rhyniensis (Devonian). Bar = 35 |im.

FIGURE 3.96 Detail of arbuscules in Aglaophyton major cortical cells (Devonian). Bar = 30 |im.

could be successfully undertaken. Although it is estimated that >90% of all living plants enter into some type of myc-orrhizal symbiosis, there remains little information about the spatial and temporal distribution of mycorrhizae in geologic time. For example, we know a great deal about Carboniferous coal swamp plants. Were they all mycorrhizal, and if not, why not? What is the distribution of mycorrhizae in major groups of plants which are anatomically preserved, that is either as petrifactions or as permineralizations? These and many other questions can have important implications in deciphering the evolution of certain types of paleoecosystems, as well as tracking fungal-plant interactions through time.

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