Chapter 4b Ascomycete survey

The Fifth Kingdom - Chapter 4b

A Survey of Ascomycetous Holomorphs

New Phylogenetic System: * = covered in this treatment

Phylum 6 Ascomycota -- with three Subphyla
    Subphylum Taphrinomycotina
         Class Taphrinomycetes
               Order Taphrinales*
          Class Schizosaccharomycetes*
          Class Pneumocystidiomycetes
          Class Neolectomycetes
     Subphylum Saccharomycotina
            Class Saccharomycetes
               Order Saccharomycetales* - see Chapter 6
     Subphylum Pezizomycotina
          Class Pezizomycetes (operculate discomycetes)
                Order Pezizales*
          Class Dothideomycetes
                Order Dothideales*
                Order Capnodiales*
                Order Myriangiales
                Order Pleosporales*
                Order Botryosphaeriales
                Order Hysteriales
                Order Patellariales
           Class Eurotiomycetes
                Order Eurotiales*
                Order Onygenales*
                Order Coryneliales
                Order Mycocaliciales
                Order Chaetothyriales
                Order Pyrenulales
                Order Verrucariales
           Class Laboulbeniomycetes
                Order Laboulbeniales*
                Order Pyxidiophorales
           Class Lecanoromycetes
                many orders of Lichens - see Chapter 7
           Class Arthoniomycetes
                Order Arthoniales
           Class Leotiomycetes
                Order Helotiales*
                Order Erysiphales*
                Order Rhytismatales*
                Order Cyttariales*
                Order Thelebolales
           Class Sordariomycetes
                Order Sordariales*
                Order Ophiostomatales*
                Order Diaporthales*
                Order Coniochaetales
                Order Chaetosphaeriales
                Order Hypocreales* (includes Clavicipitales*)
                Order Microascales
                Order Melanosporales
                Order Coronophorales
                Order Xylariales*
                Order Trichosphaeriales
                Order Phyllachorales
                Order Meliolales*
                Order Lulworthiales
                Order Calosphaeriales

click on this line to see a new page explaining the classification

Hotlinks to Traditional Orders: Taphrinales - Pezizales - Elaphomycetales
Sphaeriales - Sordariales - Diatrypales - Hypocreales
Diaporthales - Leotiales - Cyttariales - Rhytismatales - Clavicipitales
Erysiphales - Onygenales - Eurotiales - Ophiostomatales
Meliolales - Laboulbeniales - Dothideales

Now to put anamorph and teleomorph together, and talk about the whole fungus (the holomorph). If you have any queries about anamorph-teleomorph connections in ascomycetes, there is now a web site at which you can look them up. Here is the URL - http://www.cbs.knaw.nl/databases/anateleo.html
Enter Peziza and see how many different connections you retrieve. Try Acremonium (a hyphomycete with single, generalized phialides) and see how many holomorphs come up. Why do you think there are so many?

I will briefly survey the more important orders of ascomycetes, linking the different life-forms together in as many cases as possible. Although 50 orders of ascomycetes (quite a few of them almost entirely lichenized) were recognized in one recent classification, you may be relieved to discover that I will show examples of only 19, and provide a key to only 17 (mainly non-lichenized orders - see Chapter 7 for some of the others)

I have also added a page (click here) which is essentially copied from the Myconet Web page established and maintained by Dr. Ove Eriksson. This gives the most recent classification of Ascomycetes, which is (of course) much more complex than the one I use in this chapter. Students should at least be aware of the full complexity of the situation, even if they - or their professors - choose not to expose them(selves) to its full rigour.

(1) Order Taphrinales Subphylum Taphrinomycotina: 9 genera, 120 species. This is an outlying group which causes serious diseases of some plants in the Rosaceae (e.g., Taphrina deformans causing peach leaf curl) and the Amentiferae (e.g., Taphrina populina on poplar).

Here is Taphrina deformans attacking peach leaves in New Zealand. But the same picture could also have been taken in North America or Europe. The leaves become thickened, distorted and often yellow or reddish in colour.

This fungus has four unique or unusual features.

(A) The assimilative mycelium is dikaryotic -- this would immediately distinguish it from most other ascomycetes (and indeed raises questions about the taxonomic position of this order).

(B) It produces an exposed layer of asci on the surface of the host leaf (right). Since there is no surrounding or supporting fungal tissue, there is nothing we could call an ascoma.

(C) The ascospores often bud in a rather yeast-like manner, even while still inside the ascus (right and bottom right).

(D) When the asci open to release their spores, they tend to split across the tip, rather than around it (bottom, left), so they are not like the rest of the operculate group -- compare them with the asci of the Pezizales, the next order. As you may have guessed by now, this group sits uneasily among the other ascomycetes, and one eminent authority grouped the Taphrinales with the smut fungi (see order Ustilaginales in Chapter 5c); both are yeast-like when grown in axenic culture.
The anamorph of Taphrina, the phase in which it grows in culture, is a single- celled budding yeast named Lalaria.

Compare its features for yourself with some of the orders that follow.

<a href="http://images.google.ca/images?q=Taphrina">WEB IMAGES</a>

Taphrina populina (left) attacks leaves of poplar.

Taphrina amentorum (below) attacks the green fruits of Alnus (alder), turning them bright red. This illustration is from a wonderful book, Fungi of Switzerland - Volume 1 - Ascomycetes by Breitenbach and Kraenzlin. I recommend this book to all mycologists. The series is undoubtedly the best of its kind, with excellent illustrations of macroscopic and microscopic features, as you see here, plus detailed descriptions on the facing pages. Check it out...

Pneumocystis carinii, Class Pneumocystidiomycetes, the causal agent of a lung disease that affects many AIDS sufferers, fits into the Subphylum Taphrinomycotina.

Series Unitunicatae-Operculatae

(2) Order Pezizales Class Pezizomycetes Subphylum Pezizomycotina: 150 genera, 900 species. The 'operculate discomycetes' -- we'll look at 7 of the 15 families currently recognized.

(a) Family Pezizaceae. Classic 'cup-fungi' producing apothecial ascomata that are usually shaped more like saucers or goblets, usually without stalks, and found growing on wood, dung or soil. They vary so much in colour, texture and ornamentation that most discomycete specialists split the Pezizaceae into several tribes or even families. Their asci have a diagnostic pop-open lid or operculum, and the tips of the asci are amyloid (sometimes expressed as I⁺ -- this means giving a blue, starch-like reaction in an iodine solution known as Melzer's reagent).

A small species of Peziza (right, as seen through the dissecting microscope) often crops up on soil in greenhouses, frequently preceded by its blastic-synchronous Chromelosporium anamorph (the whitish fuzz at lower left).

Microscopic detail of both reproductive phases is given in the diagrams (right).

The Chromelosporium anamorph of Peziza is shown here under phase-contrast illumination.

Larger species of Peziza, producing thin, rather brittle apothecial ascomata several centimetres across, with light brown or orange hymenia, can be found on the ground in Spring and Fall (right).

(b) Family Sarcosomataceae.

	This family contains wood-inhabiting fungi with apothecia that are often stalked (stipitate), relatively tough, and brightly coloured. The asci are sub-operculate, and non-amyloid. The scarlet cups of Sarcoscypha coccinea (left), growing from buried hemlock branches, brighten up the early Spring in Canadian woodlands.
	The brightly coloured, stalked apothecia of Cookeina (left) are a common sight in the Neotropics, and may provide a camouflaged perch for the tiny but equally colourful poison arrow frog, as this National Geographic cover shows.

Urnula (below) is another striking example of the Sarcosomataceae.

(c) Family Pyronemataceae.

Aleuria aurantia, the orange peel fungus (below),
is common along the edge of logging roads on Vancouver Island.

The picture above is from Fungi of Switzerland Volume 1 by Breitenbach and Kraenzlin. Note how the field picture is flanked by details of the diagnostic microscopic features. This book is the best of its kind, and belongs on every mycologist's shelf.

Another example of the Pyronemataceae from this magnificent book is Humaria hemisphaerica (above),

Scutellinia scutellata (right), [Pyronemataceae] its orange apothecia rimmed with dark hairs (which give it the common name 'eye-lash fungus', and with non-amyloid asci, is one of the commonest cup-fungi, growing on rotten wood. Anamorphs don't seem to be produced by many members of this family.

Caloscypha fulgens is a common spring discomycete in western North America. It is easily recognized by its brilliant orange apothecia which soon become externally tinged blue or greenish-blue. These specimens grew in May along a trail in John Dean Park near my home.

The phase contrast photomicrograph below shows asci and ascospores of
Caloscypha fulgens.

There are 8 globose, uniseriate ascospores.

Some genera, such as Genea (right), produce closed but hollow ascomata. The asci are cylindrical or clavate, and are arranged in an extensive flat hymenium lining the ascoma, but they do not shoot their spores. These apparently contradictory features show that members of this family are becoming sequestrate (their fruit bodies do not liberate spores at maturity) and hypogeous (they produce their ascomata underground).

Geopora cooperi, here seen bisected, is also sequestrate and hypogeous, but now the air space inside the fruit body is much less than in Genea: another step on the way to becoming a truffle (see below, and Family Tuberaceae).

This evolutionary process is diagrammatically illustrated here. The fourth and final step sees the elimination of air spaces altogether, and is a solid truffle of the genus Tuber, Family Tuberaceae -- see family (g) below.

Evolution toward the sequestrate and hypogeous condition is not restricted to the Pyronemataceae, but can also be seen operating in several other families of the operculate discomycetes.

4 sequestrate evolution.gif (27453 bytes)

(d) Family Ascobolaceae.

Students who have followed the succession of fungal fructifications appearing on horse dung will be familiar with the two most important genera of this largely coprophilous (dung-inhabiting) family -- Ascobolus and Saccobolus. Both produce minute, translucent apothecia (seen under the low power of the dissecting microscope, top right; higher power, lower right).

The dark dots are mature asci, which are broad, and project from the hymenium when mature, so that their tips may become oriented toward the light.

The 8 ascospores have a purple or brown outer wall layer. Ascobolus (left), like most other ascomycetes, shoots ascospores individually. Saccobolus (right) atypically sticks all eight together in a bundle, and they are expelled as a single projectile, which gives them extra range. I haven't seen any anamorphs in this family, though a few are known.

(e) Family Helvellaceae.
These mostly spring-fruiting fungi have large and unusually configured apothecial ascomata. All are stalked, with beige to brown, hymenium- covered caps. Helvella species (H. elastica, below, left; H. crispa, below, right) have a drooping flap on either side, and are called saddle fungi. Abbott and Currah (1997) gave a good revision of this family.

This is Helvella lacunosa...

...and this is a cross section of its stipe - surely one of the most interesting of any fungus. Its structure gives it a lot of the stiffness of a girder, for a minimal investment in materials.

The ascomata of Gyromitra species (left), are among the largest ascomycete fructifications, and some species contain the toxin gyromitrin, a precursor of the deadly monomethylhydrazine.
By causing some fatal poisonings, the Spring-fruiting Gyromitra esculenta (far left) has earned its place in Chapter 22 on poisonous mushrooms.

It is vital for morel-hunters to be able to distinguish the convoluted head of Gyromitra, the false morel, from the ridged and pitted head of the delicious true morel (see below)

...and here's a March 2000 collection we made of Gyromitra infula on a rotten log (note that superficially, it looks more like a Helvella, but is distinguished by its spores, which have an apiculus at each end.

Occasionally you may find a specimen that looks as if a mould is growing on it. Sometimes there really is a mould attacking it, but it's also likely that what you're seeing is a deposit of the fungus's own ascospores, as is the case with the Gyromitra esculenta below, which was sitting in very still air (the beautifully ellipsoidal spores, each containing polar oil droplets, are shown in the second photo).

(f) Family Morchellaceae.
While Gyromitra is one of the few lethally toxic fungi, its cousin, Morchella, the true morel (below, left) is one of the finest of all edible fungi. The left-hand picture below is of my first morel of the year 2000 (Morchella angusticeps, found near Lake Wenatchee, Washington State). Species of Morchella have a broad, hollow stalk, and a pitted and ridged, sponge-like, more or less conical or ellipsoidal head. Since the hymenium doesn't cover the ridges (as you can see in the transverse section, below centre), it seems likely that a morel is a compound ascoma, each pit representing an individual apothecium. The anamorph of the morel is a blastic-sympodial hyphomycete, Costantinella, which I have often found in the Fall growing on soil beside trails in Algonquin Park, Ontario (below, right).

Morels have a broad geographic range, but are common in relatively few areas, of which Michigan is perhaps the best-known. People throng to the woods in May to hunt this elusive delicacy, and Boyne City holds an annual morel-hunting championship. When Dutch elm disease was killing millions of elm trees, morels sometimes fruited profusely around recently dead trees. In recent years they have also been collected in large numbers on burned over areas of western forests. Morels are discussed as a a delicacy in Chapter 18.

Just to confuse the issue, a second genus of Morchellaceae, Verpa, also fruits in May. Species of Verpa aren't toxic, but neither are they good to eat. Verpa bohemica (left), found at Lake Wenatchee, like the morel above, is called the wrinkled thimble-cap.

Verpa bohemica (above, and far left), looks like a morel, but it is easy to tell the difference by bisecting the fruit bodies vertically. While the cap and stalk of the true morels (the two right-hand specimens in each picture) are firmly united, the cap of Morchella semilibera (first from left, next to the Verpa) is, as its name implies, half-free, and that of Verpa is attached only at the apex, as you can see in the sectioned fruit bodies in the lower photograph. In addition, the stipe of Verpa (far left) is 'stuffed' with cottony mycelium, while those of the Morchella species are completely hollow.

(g) Family Tuberaceae Order Pezizales Class Pezizomycetes...

...the truffles. Here, the evolutionary process still active in the Geneaceae, Otideaceae, etc. has run its course. The ascomata are sequestrate, hypogeous and solid (no air spaces any more -- as you can see in this bisected specimen of Tuber aestivum, which a truffle dog brought to me at Scheggino in Italy)

The asci, produced in a highly convoluted hymenium, are rounded and thin-walled (those of Tuber albidum are shown at left) with no trace of an operculum or other shooting mechanism, and usually contain only 1-3 spores.

The ascospores of truffles have complex, highly ornamented walls. They come in two basic patterns - spiny (left) and lacunose (right). These SEM pictures show single ascospores of (left) the black truffle, Tuber melanosporum (the French favourite) and (right) the white truffle, Tuber magnatum (which the Italians prefer). You might be interested in my own ratings, given in Chapter 18).

Only by examining a series of microscopic characters, and considering some intermediate forms that trace the probable course of evolution in the group (a set of diagrams given earlier) can we tell that these fungi are related to the 'operculate discomycetes.'

Although it doesn't make taxonomy any easier, we must now logically place these hypogeous (underground) families with their epigeous (above-ground) forebears in the order Pezizales. The hypogeous habit has necessitated the evolution of new methods for passive spore dispersal, in which some agency other than the fungus supplies the energy for dispersal. Members of the Tuberaceae, especially species of the genus Tuber (the true truffles), have achieved this by developing what can only be called fascinating smells. These odours are released when the ascospores are mature, and lead many mammals unerringly to the ascomata, which they unearth and consume, subsequently depositing the still-viable spores elsewhere. Tuber is dependent, not only on mammalian vectors, but on the roots of oak and hazelnut trees, with which it establishes a symbiotic ectomycorrhizal relationship (see Chapter 17). Tuber melanosporum and Tuber magnatum are, respectively, the black and white truffles of French and Italian haute cuisine, perhaps the most highly esteemed (and certainly the most expensive) of all edible fungi, and so are discussed in detail in Chapter 18.

Molecular studies (Urban et al., 2004) have shown that certain species of Tuber have previously unknown hyphomycetous anamorphs resembling Geniculodendron, with branched conidiophores and blastic-sympodial conidiogenesis.

(3) Order Elaphomycetales:

1 family, 2 genera, 21 species. At first sight the hypogeous ascomata of Elaphomyces (left) look just like truffles; and they're even called 'deer truffles'...

...but they have no hymenium - the basically spherical, non-shooting asci (two stained asci are shown here) are produced randomly throughout the interior of the ascoma. Elaphomyces no longer offers much in the way of visual clues about its possible epigeous ancestors, so only molecular techniques can help us decide its relationships. These techniques are what placed a strange new fungus from the forests of Guyana right next to Elaphomyces...

The two pictures on the left [from Miller et al. (2001) Mycol. Res. 105: 1268-1272] show a fungus that clearly has a volva and a stipe (stalk). It was discovered only in 1998 and described in 2001. It doesn't look like Elaphomyces (see picture above), and was almost described as a basidiomycete, a member of the Tulostomataceae (the stalked puffballs). But repeated molecular results from different collections showed that it is in fact an ascomycete very closely related to Elaphomyces, and has apparently evolved major new characters as a way of dealing with a very wet environment -- it needed to get its spores not only out of the soil, but above it. We welcome Pseudotulostoma to the known fungi.

Series Unitunicatae-Inoperculatae

Although none have lids (opercula), the asci of this group are not as uniform in appearance or structure as we might like (below). Most have thicker walls at their tips, pierced by a fine pore. Inside the apices, many have diagnostic sphincter-like rings, which control the expulsion of the spores. Some of those rings are amyloid (they stain blue in iodine), others don't react with iodine, and are called chitinoid. Some asci don't have rings at all, and in the lichenized Lecanorales (G) (now placed in the Class Lecanoromycetes), the ascal apex is extremely thick and pierced by a narrow canal. The true relationships among these orders have yet to be fully worked out.

4 inoperc asci.gif (21448 bytes)

(4) Order Sphaeriales Class Sordariomycetes: 225 genera, 1300 species. Many members of this group produce dark, brittle, globose to pear-shaped individual perithecial ascomata with prominent ostioles. Others have many perithecial cavities immersed in a single stroma to form a compound fructification, as in Xylaria below The asci often have an apical ring or sphincter, which is usually, though not always, amyloid (stains blue in iodine). Thread-like, sterile elements called paraphyses are present between the asci in the hymenium of some members, absent from others. Ascospores can be light or dark, simple or septate, with or without germ pore or slit, sometimes with gelatinous sheaths or appendages.

The compound fructification of Xylaria, a common wood-inhabiting genus, has hundreds of perithecial ascomata just below the surface, as a you can see in the transversely cut specimen (below, left). Each perithecium contains many asci, as you can see in the section (below, centre).

xylaria1.jpg (11976 bytes)

inoperc2.jpg (2203 bytes)

The asci are inoperculate, with an amyloid apical ring (stained blue - above, right) and contain 8 darkly pigmented, asymmetrical spores, which will eventually be shot out through the ostiole.

Xylaria hypoxylon is another common and easily recognized species. The upper part of the compound ascoma is covered with the whitish conidia of the blastic-sympodial anamorph (which, strange to say, has not been named). This species is often seen on fallen, rotting branches.

This order also includes such pathogens as Entoleuca mammata (formerly Hypoxylon pruinatum) (below), which causes poplar canker, a disease that kills millions of trees every year. The extensive, more or less elliptical cankers (below, left) develop groups of perithecial ascomata (light circular patches, below, right) after the tree cambium has been killed.

For more information about the Xylariaceae, please consult the web site built by Jack Rogers, an authority on this group, at http://mycology.sinica.edu.tw/Xylariaceae/
This deals with all the main genera, and has many useful illustrations and keys.

The genus Annulohypoxylon has recently (2005) been erected for species of Hypoxylon distinguished by molecular characteristics and by the presence of: (1) a discrete carbonaceous layer enclosing each perithecium, and (2) ostiolar discs.

(5) Order Sordariales Class Sordariomycetes: 5 families, 75 genera, 600 species. This is a generally saprobic group producing solitary perithecial ascomata, and found on dung or decaying plant remains. Their asci sometimes have non-amyloid apical sphincters, and sometimes lack any apical apparatus. Several members of this order are important tools in fungal genetics and biochemistry. First and foremost is Neurospora, which has justifiably been called the 'Drosophila of the fungus world'. It was on Neurospora crassa that the science of haploid genetics was founded. The uses of Neurospora and Sordaria mutants are explored in Chapter 10.

Neurospora has Chrysonilia anamorphs (left) that closely resemble the Monilia anamorphs of Monilinia (Sclerotiniaceae, Leotiales).

When I was in China some years back, I noticed the vivid yellow-orange fruiting of Chrysonilia on the husks of corn cobs thrown away near the great wall at Badaleng.

This slide prep. shows the branched blastic-acropetal chains of conidia formed by this fungus (stained blue).

Many species of Sordaria and Podospora fruit on herbivore dung, and shoot their ascospores from perithecial ascomata whose necks, like that of the Sordaria on the left, are phototropic (point toward the light). Look for the apical ring mechanism in the Sordaria asci (right), seen under phase contrast illumination.

Different species of Podospora have 4, 8 (as on the left), 16, 32, 64, 128, 256, 512, 1024 or 2048 ascospores per ascus.

How many do you think there are in each of the two asci of Podospora tarvisina on the right?

The various combinations of tubular and gelatinous ascospore appendages in Podospora not only help in species identification, but also stick the spores to grass after they have been shot away from the dung on which the ascomata develop. Some species of Podospora have Phialophora anamorphs.

Podospora has been analyzed from the molecular point of view and found to be a polyphyletic genus. Species bearing plates of agglutinated hyphae (see middle left-hand photo above) were found to be monophyletic, and have been moved to Schizothecium.

Chaetomium (left) is an important cellulolytic genus that damages fabrics and paper, especially in the tropics. It differs from most other Sordariales in that its asci, though cylindrical, deliquesce or autolyse at maturity. Since they don't shoot their spores, they have no apical ring mechanism, and the mucilaginous, lemon-shaped ascospores ooze out of the ascoma into a characteristic mass of coiled (left) or dichotomously branched hairs that develop on the top of the ascoma. Dispersal must be by rain or arthropods. Chaetomium has Botryotrichum anamorphs

(6) Order Diatrypales Class Sordariomycetes: 20 genera, 125 species. The bark on dead branches of trees often develops eruptions that mark the extensive immersed stromata (compound ascomata) and the grouped ostioles of such common genera as Diatrype (in surface view, right, and cut away, below, left, to show the perithecial cavities) and Quaternaria. Diatrypalean asci (seen in a squash, below, right) have a tiny amyloid apical ring, and the ascospores, also very small, are characteristically sausage-shaped (allantoid).

Another informative pair of illustrations, of Diatrype disciformis (above), from the highly recommended Fungi of Switzerland. The reference is at the end of the chapter.

(7) Order Hypocreales Class Sordariomycetes: 80 genera, 550 species.
This order is recognized by its brightly coloured, simple or compound, perithecial ascomata -- usually yellow, orange or red -- which are fleshy or waxy in texture, and usually borne on supporting layers of mycelium (subicula) or in stromata. Four genera are especially well-known.

1) Nectria (27 species) has bright red, superficial perithecia (right) containing 2-celled (didymosporous) ascospores. Some species cause cankers and die-backs of trees.

Nectria sensu lato has a variety of conidial anamorphs, all of them phialidic. The erumpent sporodochia of one commonly encountered phialidic anamorph, Tubercularia, cause a condition known as coral spot (below, left).

The picture on the right shows the yellow-orange Tubercularia anamorph growing beside the dark red Nectria perithecial ascomata. It is interesting and a little unusual to see both phenotypic expressions of the genome being produced simultaneously.

However, the most economically important of the nectriaceous anamorphs are certain Fusarium species (below, right), many of which cause destructive wilt diseases of higher plants, or produce mycotoxins.

(2) *Gibberella* *also has Fusarium* anamorphs, which are producing the reddish pigment seen in the picture (near right)** Fusarium (far right) produces curved phragmoconidia, frequently with an angled 'foot cell,' from clusters of phialides.
*The picture on the right shows Gibberella* (the dark bodies are its perithecia) and its Fusarium anamorph (reddish-orange) growing together on a corn cob.**

One species of Gibberella causes a disease of rice called 'foolish seedling' in which seedlings grow too rapidly and consequently fall over. The active principle, a plant growth hormone called gibberellic acid, has been extracted and is now widely used to stimulate plant growth.

(3) Hypomyces. In this series of five pictures, we zoom in on Hypomyces lactifluorum, an orange fungus which, like other species of the genus, parasitizes basidiiomycetes, in this case the agaric genera Lactarius and Russula...

...producing a layer of tissue that completely covers the gills and suppresses their development...

...then developing thousands of bright orange-red perithecial ascomata all over the surface of the subiculum.

The Hypomyces completely envelops the aborted mushroom and its colour gives the host-parasite combination the name 'lobster fungus'. Strangely enough, this monstrosity is edible, though I regret to have to tell you that it does not taste like the divine crustacean.

Here is the ostiolar region of one Hypomyces perithecial ascoma.

Note the pseudoparenchymatous wall of the perithecium, and some of the narrow asci which have been squeezed out during the preparation of the slide...

...and here are two of the extremely characteristic spindle-shaped, 2-celled, colourless ascospores. If you look carefully you'll see the septum in the lower spore, and that the spores are rather rough-walled or verrucose.

Twenty-one species of Hypomyces that grow on fruit bodies of various basidiomycetes produce anamorphs belonging to the hyphomycete genus, Cladobotryum, which has an unusual blastic-retrogressive method of forming conidia
(see Chapter 4a).

If you need to identify a species of Hypomyces, there is now a fine new fully illustrated resource on the web, at: http://nt.ars-grin.gov/taxadescriptions/hypomyces/

(4) Hypocrea forms fleshy stromata on wood (right). The dark spots are the ostioles of the embedded perithecial cavities.

The asci are typically 16-spored, the ascospores uniseriate, as you can see in the second picture

The teleomorph of Hypocrea is recorded far less often than its green-spored, phialidic anamorph, Trichoderma (lower right) which, because some species are broad-spectrum mycoparasites, and others produce cellulases and antibiotics, is one of the most important genera of moulds in forest soils. It is now being exploited in biological control of pathogenic fungi (see Chapter 14), and in the production of enzymes which can convert cellulose to glucose (Chapter 24)

Chaverri and Samuels (2003)give a detailed treatment of Hypocrea species with Trichoderma anamorphs.

4 Trichoderma.jpg (12460 bytes)

The diagrams below show the wide range of anamorphs found in the Nectria-like members of the Hypocreales. They all have phialides as their conidiogenous cells, though the different ways in which these are arranged, and the varying shape and septation of the conidia, place them in many different anamorph-genera (named in the drawing).

(8) Order Diaporthales, Class Sordariomycetes: 90 genera, 500 species. Here several beaked, perithecioid ascomata are usually immersed in a single stroma (as in Diaporthe impulsa, right).
Paraphyses are often absent; and the asci become free inside the ascoma, and then autolyse. This rather paradoxical situation suggests that evolution is in active progress here. Two important genera stand out. Cryphonectria (Endothia) parasitica causes chestnut blight, which has almost extinguished an important species of North American tree in about 50 years: you can read the full story in Chapter 12. Because of this near-extinction, you will probably not be able to find specimens of Cryphonectria, but another member of this order, Gaeumannomyces graminis, which causes 'whiteheads' or, take-all' of wheat, is common. It rots the roots of afflicted plants, and causes premature drying out of the plant, sometimes reducing yields to zero. Anamorphs are coelomycetous.

Leucostoma niveum (above), as illustrated in Fungi of Switzerland - Volume 1 - Ascomycetes, is another member of the Diaporthales.

(9) Order Leotiales Class Leotiomycetes: 13 families, 400 genera, 2000 species. (Note that the Geoglossaceae have now been removed from this Class). A large assemblage termed the 'inoperculate discomycetes.' The apothecial ascomata are superficially similar to those of the Pezizales, but the asci are inoperculate, and usually have amyloid apical rings. This suggests to me that the two major kinds of apothecial ascomata are examples of parallel or convergent evolution. Several of the families in this order are common and well-known, so four of them are dealt with below.

(a) Family Sclerotiniaceae.
Class Leotiomycetes
As the name implies, these fungi often form sclerotia, which may be solid masses of fungal tissue, or may be of mixed origin -- fungal hyphae riddling a mummified host such as a peach, plum, cherry or blueberry, or a catkin (right and below, in Ciboria amentacea). Having overwintered in this guise, they germinate in spring and use the stored energy to produce stalked apothecial ascomata (right). Ascospores (primary inoculum) are shot when the host is in flower, and gain entrance through the stigma.

The illustration above is from Fungi of Switzerland, which I recommend to you all.

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The anamorphs are generally responsible for secondary dispersal, and some cause serious plant diseases. For example, the soft brown rot of peaches (above, left) is produced by a Monilia anamorph of Monilinia. The greyish powder on the surface of the peach (above, left) and the cherry (below) is made up of masses of branched blastic-acropetal chains of conidia (above, right).

The longer I leave the ripe cherries on my cherry tree, the more of them will succumb to the Monilinia soft brown rot, as the conidia being produced on one cherry (far right) infect others
(see Chapter 12).

Monilinia vaccinii-corymbosi causes mummyberry, a serious disease of cultivated blueberry. Shoots infected by this fungus become ultraviolet-reflective, and release a fragrance and sugars - three features that attract pollinators.

These insects then transfer the Monilia conidia to the flowers, initiating new infections.

[Oregon State University has a good web page about this problem: check it out at:
http://plant-disease.ippc.orst.edu/disease.cfm?RecordID=182]

The mummified berries that result from these infections are pseudosclerotia (a mixture of plant and fungal tissue).

The mummified berries overwinter, then germinate to produce Monilinia apothecia that release the primary inoculum (ascospores) to start the cycle again.

Another Monilinia produces spur blight of wild cherry (left), killing back young shoots and forming new conidia on the leaves.

Grey mould of strawberry (left) is caused by Botrytis cinerea, the anamorph of Botryotinia fuckeliana.

Botrytis cinerea (holomorph = Botryotinia) is a very common mould that can also be seen fruiting on dead flower heads and overripe blackberries (below) during damp weather in late summer and fall.

And a bright red flower head of geranium (Pelargonium) (below, left) can turn into a rather sorry looking mess (below, right) in about a week. Botrytis cinerea at work.

Here is a young, branched conidiophore of Botrytis, highly magnified, showing the development of blastic-synchronous conidia on small terminal vesicles.

Many members of the Sclerotiniaceae have distinctive anamorphs (see above and
Chapter 4a), while the teleomorphs are relatively uniform. So some of the holomorph genera erected for the teleomorphs have atypically been distinguished by characters of their anamorphs -- and even named after them. So we have Sclerotinia with Sclerotium (sclerotial) anamorphs, Monilinia with Monilia anamorphs (blastic-acropetal), Botryotinia with Botrytis anamorphs (blastic-synchronous), and Streptotinia with Streptobotrys anamorphs (blastic-sympodial).

Sclerotium, Monilia and Botrytis cause several serious plant diseases (see above and Chapter 12), but when Botrytis grows on overripe grapes in certain areas of France, Germany, Hungary, and South Africa it is called the 'noble rot' in several languages ('pourriture noble', 'edelfaule') because the small quantities of sweet dessert wine that can be made from such shriveled grapes have intense and exquisite flavour, and can be sold for very high prices. Find out what a bottle of Chateau d'Yquem sauternes from France (or a 'Trockenbeerenauslese' from Germany, or a good Tokay from Hungary) costs at your local wine store: be prepared for a shock. The full story and some pictures can be found in Chapter 19.

(b) Family Phacidiaceae Class Leotiomycetes. Some Phacidium spp. cause snow blight diseases of conifers, as these two photos of extensive damage to Abies foliage demonstrate.

If we look more closely, we will see that this family is not typical of discomycetous fungi in general, since the ascomata develop inside host tissue, and are at first covered by a thick roof of dark fungal tissue, as in the diagram (left).

But at maturity the roof splits open and exposes the hymenium. The apical ring in the asci is amyloid (I⁺). Compare this family with the order Rhytismatales, a little lower on the page...How do these orders differ?

Phacidium has coelomycetous anamorphs: those of pathogenic species such as P. coniferarum belong to Apostrasseria (upper left)...

...while those of saprobic species like P. betulinum belong to Ceuthospora (lower left).

The two sets of photomicrographs show vertical sections through the pycnidial conidiomata, and details of the conidiogenous cells and conidia under phase contrast illumination.

Can you tell from these pictures how the two anamorph genera, Apostrasseria (above) and Ceuthospora (below), can be differentiated?

(c) Family Geoglossaceae Now (surprise) placed in a separate Class Lichinomycetes.
The family name means 'earth-tongues' - they produce unusual stalked, somewhat flattened and tongue-like, or sometimes pileate, ascomata which emerge from the ground. The hymenium doesn't line a cup or saucer, but covers the convex upper surface of the ascoma, which is fleshy and yellow in Spathularia (right), tough and black in Microglossum, Trichoglossum and Geoglossum (below, left).

If you squash a tiny piece of the hymenium of a mature Geoglossum ascoma, you will see the asci, each of which contains a bundle of 8 long, parallel, phragmoseptate brown ascospores (below, centre). A single 7-septate (phragmosporous) ascospore is shown in the right-hand picture (The number of septa in the ascospore is diagnostic).

Cudonia (left and below) is a pileate (bearing a well-differentiated beret-like cap) genus of the Geoglossaceae. C. grisea (left) is common in spring on decaying wood on the Pacific Northwest.

The illustration of Cudonia circinans (below) is from Fungi of Switzerland Volume 1, a work all those who are interested in the ascomycetes should consult regularly. Note its admirable inclusion of both macroscopic and microscopic characters.

Mitrula produces what looks like a small version of Spathularia. One of the common species, Mitrula paludosa (left, approx 3x), grows on dead leaves in bogs or other wet places. This one was in a shallow stream beside the trail to Botanical Beach, Vancouver Island, B.C.

(d) Family Leotiaceae Class Leotiomycetes contains some more normal-looking 'discomycetes' such as Bisporella, which produces those small yellow discoid apothecia so common on fallen, decorticated tree-trunks...

...while Chlorociboria, also fairly common, stains wood a deep green and forms small, vivid green apothecia on rotten logs.

Another rather spectacular member of this order is Bulgaria inquinans, found on wood of deciduous trees. The apothecial ascomata have a rubbery texture, and the hymenium is jet black.

(This picture is from "The Wild Mushroom" by George McCarthy, which I recommend to those with an eye for fine photographs of macrofungi).

Less typical are the spectacular ascomata of Leotia: these are much larger, stalked, jelly-like, and have beret-like convex fertile heads (Leotia lubrica below, left and the beautiful velvety green and translucent yellow Leotia viscosa below, right).

(e) Family Dermateaceae includes Diplocarpon rosae (which, with its Marssonina anamorph, causes black spot of roses - see illustration in Chapter 12), and a common but interesting fungus, Trochila ilicicola, that fruits on dead leaves of holly (Ilex) in our garden. Here are several illustrations that will put you in the picture. Below, left, a scan of a dead holly leaf showing numerous fruit bodies all over the upper surface. Below, right, the closed fruit bodies under the dissecting microscope.

These ascomata have a hinged lid, which opens when the leaf is kept in a damp chamber (below, left). The exposed hymenium contains thousands of asci like that shown below, right.

(f) Family Vibrisseaceae is a small family with filiform (thread-like), multiseptate, fragmenting ascospores. It has interesting stream-dwelling anamorphs (Anavirga).
This illustration of Vibrissea truncorum (below) is from the highly recommended Fungi of Switzerland.

(10) Order Cyttariales Class Leotiomycetes: 1 genus, 10 species.

	The globose compound ascomata appear on the branches of the Southern Beech (Nothofagus) in Chile, Argentina and New Zealand. They seem to be made up of many apothecial ascomata packed together, as the photographs (left and below) show. In South America they are eaten and used to make an alcoholic beverage (see Chapter 18) (photos courtesy M. Wingfield, D. Minter)

(11) Order Rhytismatales Class Leotiomycetes: 70 genera, 400 species.
The ascomata develop immersed in host tissue or a fungal stroma, which ultimately ruptures to expose the hymenium. The asci often have apical rings, but these are small and chitinoid (do not stain blue in iodine). The ascospores are usually long and thin

The genus Lophodermum (right) is sometimes endophytic and asymptomatic in pine needles for much of its life, but eventually fruits after the needles die (see Chapter 11).

The lower picture (right) is of a transverse section of a pine needle that has been colonized by Lophodermium -- the section passes through two ascomata. Note the built-in thin-walled area in the roof of each ascoma, at which it will split open in order to shoot its ascospores.

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Rhytisma acerinum (below) causes 'tar spot' of red maple leaves in Eastern N. America...

...while Rhytisma punctatum (below) produces a similar syndrome on big-leaf maple in Western North America, but the small, individual stromata do not fuse. In this photo, the fungus appears to be prolonging the life of the leaf tissue surrounding its colony.

(12) Order Clavicipitales: 27 genera, 270 species. Now placed in Order Hypocreales, Class Sordariomycetes

This order comprises a group of highly evolved and sophisticated, obligately parasitic fungi with: (a) frequently stalked, all-fungal stromata (below, A,B,D,E), (b) long asci without apical rings, but with thickened tips (below, right, F), and (c) long, thread-like ascospores that in some taxa fragment at or following release (below, right, F). They have some interesting anamorphs, including Tolypocladium, Polycephalomyces, and Neotyphodium (which used to be called Acremonium, until it was realized that the holomorphs were in different Orders).

Three bizarre and spectacular genera, Claviceps, Cordyceps and Epichlo�, will give us a snapshot of this fascinating order.

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(1) Claviceps purpurea (A,B,C above) discharges its ascospores when its main host, rye, is in flower, and infection takes place through the stigma. As the infection progresses, the fungus takes over the food being channeled into seed-production by the host. The ovarian tissues are replaced by a mycelial mat that produces masses of conidia of the Sphacelia anamorph in a sweet-smelling nectar. Insects are attracted to the nectar, and spread the conidia to other host plants. The mycelial mat hardens and becomes a purplish sclerotium -- the ergot -- which replaces the grain (drawings A and B above, and scan below).

I found the ergots shown above at Whiffin Spit, Sooke, Vancouver Island, on Elymus mollis, a large grass that grows along the shore in the Pacific NorthWest. The largest ergot in the scan above is 4 cm long and almost 5mm wide. These sclerotia fall to the ground in Autumn, overwinter, and germinate the following Spring, each producing several stalked stromata (drawings B and C above, and photos below). Each stroma has a spherical head within which many perithecia develop around the periphery just below the surface.

Because this fungus has a small target, the stigma of the grass flower, which is available only during a narrow time-window, and because spores reach it only by chance, the fungus must disperse a large number of ascospores in a short time. A rough calculation suggests that a single ergot can give rise to 5 stromata, and each of those may contain 100 perithecial cavities, each cavity with 50 asci, and each ascus producing eight ascospores: a total of 5 X 100 X 50 X 8 = 200,000 propagules per ergot.

If the sclerotia are accidentally consumed by cattle, or if rye bread made from ergoty rye is eaten by humans, a large number of alkaloids found in the ergot cause a form of poisoning known as ergotism, or, more picturesquely, St. Anthony's Fire. Human victims frequently hallucinate and feel that they are burning (see chapter 21 for a fuller account of this mycotoxicosis). The alkaloids ergotamine and ergotaline cause contractions of the smooth muscles, and the ensuing restriction of the peripheral blood supply can lead to gangrene and even death. St. Anthony's Fire was fairly common in the Middle Ages, and sporadic outbreaks occurred until recently. Ergot, the only fungal structure in the British Pharmacopoeia Codex, has been used in obstetrics both to induce childbirth and to control post-partural bleeding. Another species of Claviceps brought the genus renewed fame, or perhaps I should say notoriety, as the prime source of LSD (lysergic acid diethylamide), one of the most powerful psychedelic drugs (it is a hundred times more potent than psilocybin, the active ingredient of `magic' mushrooms).

(2) Cordyceps species (drawings D and E, above, and several illustrations below) are bizarre: they generally parasitize insects, spiders and mites, or hypogeous fungi, and their large stromata spring up directly from their victims. These perithecial stromata, arising from an insect larva or pupa (below), are known as vegetable caterpillars, in recognition of the fact that they always incorporate elements from more than one kingdom.

"These strange 'two Kingdom' structures are used in traditional Chinese medicine (right), as a treatment for "general debility after illness, weakness, spitting of blood caused by TB ...chronic coughing and asthma ...night sweating ...anaemia ... malignant tumour."

Cordyceps sinensis (above, right) traditionally bundled with red thread, can be purchased in many Chinese pharmacies, but most people do not know where it comes from. You may be surprised to learn that most of the supply is collected at high altitudes in Tibet.

Yartsa Gunbu, as Tibetans call it, parasitizes the larvae of small white butterflies of the genus Thitarodes (formerly Hepialus). It occurs in alpine pastures at altitudes of 3000-5000 m, but most commonly from 3800 m to 4500 m. In Litang County, collectors are allowed to gather these fungi only in their legal grazing areas. Outsiders have to pay a fee to the local government for the right to collect. Not surprisingly, there are reports of conflicts between locals and unlicensed intruders.

The harvest of Cordyceps sinensis, which is collected in early spring in all grasslands across the Tibetan Plateau, is substantial. Estimates for the present annual harvest in Litang range up to 5,000 kg, representing 5 to 10 million specimens. For comparison, old statistics for Xikang Province report a Cordyceps harvest of 15,000 kg in 1939. Between 1949 and the mid-1980s the annual Cordyceps harvest ranged between 5,000 and 20,000 kg in Ganzi Prefecture. Cordyceps sinensis makes up about 95% of the fungal market in Tibet. Considering that it is worth $30,000/kg retail, this is not surprising. This one fungus contributes about 40% of the rural income in Tibet.

I am grateful to Daniel Winkler (link to his webpages) , who has spent much time working in Tibet, for this first-hand information, and for the picture (left) of a "bu" (Tibetan, short for yartsa gunbu, meaning worm) hunters' camp in Tibet.

During my recent visit to Japan, this specimen of Cordyceps neovolkiana arising from a beetle larva was spotted in a rotten log at Kikuchi Glen near Kumamoto by my guide, Dr. Hitoshi Neda.

For me, this find maintained Japan's reputation as the world centre for Cordyceps. I took two photos through the dissecting microscope with my digital camera and stitched them together after I got home to produce the result seen here.

Before I left Japan I obtained a copy of the classic Japanese book on Cordyceps and related genera, by Shimizu and Kobayasi (ISBN 4-259-53866-7) Its English title is "Illustrated Vegetable Wasps and Plant Worms in Colour" and it contains literally hundreds of superb colour paintings of these fungi. It is a mycologist's and a bibliophile's delight. Some of the paintings could clearly inspire the makers of science fiction movies. Seek it out!

To see some pictures from it, click here

	A few species of Cordyceps don't pick on arthropods, but cannibalistically attack another fungus - actually, it's even another ascomycete - the deer truffle (Elaphomyces). (Left) the large, stalked stroma of Cordyceps capitatus can be seen emerging from the host truffle. (Right) a close-up of the head shows the ostioles of hundreds of perithecial cavities, and a slice of the head (below) reveals their orientation.

Here is another species, Cordyceps ophioglossoides, that also attacks Elaphomyces. Every September for many years, during our mycology field course, we found this species parasitizing Elaphomyces along one of the hiking trails in Algonquin Park, Ontario.&nbs