Sordariomycetidae: Soil Fungi A-Plenty

I'm pretty sure I've commented before that, although most of us tend to associate the word 'fungi' with mushrooms and other eye-catching fruiting bodies, the vast majority of fungal diversity is minute and tends to go unnoticed. Nevertheless, despite their obscurity, many of these microfungi are crucial to our own continued existence. These are the decomposers, the organisms that break down fallen plant matter and animal wastes in their own search for nourishment and so contribute to the release of locked-up nutrients back into the environmental cycle.

Neurospora growing on sugar cane waste, from here.

The group of fungi that I drew for today's post, the Sordariomycetidae, is primarily made up of these minute decomposers. Sordariomycetids have already made an appearance here at Catalogue of Organisms, in a post from ten years ago on black mildews. Depending on how broadly the group is circumscribed, the Diaporthales could also be included. Due to a simple morphology that provides few distinct characters, the Sordariomycetidae are primarily defined on the basis of molecular phylogenies. The difficulty of classifying microfungi by morphology alone is underlined by cases where species previously classified within the same genus have proven to belong to entirely distinct fungal lineages.

In general, the vegetative body of most Sordariomycetidae consists of little more than disassociated hyphae embedded in their substrate, with the only distinct structures being the reproductive fruiting bodies. These are perithecia: that is, globular or flask-shaped fruiting bodies with a single small opening or ostiole at the top through which the mature spores are released. In some cases, the internal structure of the mature perithecium will simply dissolve, freeing the spores to escape through the ostiole in the manner of a miniature puffball. In others, the spores become entangled in a long strand or seta that is then extruded through the ostiole like toothpaste being squeezed out of a tube.

Perithecium of Chaetomium extruding spore-bearing setae, from here.

Sordariomycetids are found in almost every habitat imaginable: as well as soil- and dung-dwelling forms, they may also be found in aquatic and even marine habitats. Perhaps the best-known sordariomycetid is Neurospora crassa, red bread mould, which is widely used in laboratories as a model organism for genetic research. Indeed, it was investigations into N. crassa in the 1950s that first led to the proposal of the 'one gene, one enzyme' model that became a cornerstone of molecular genetics.

If They Only Wood (Taxon of the Week: Diaporthales)

Perithecia (fruiting bodies) of Cryphonectria cubensis, the cause of eucalyptus canker. Photo by Edward Barnard.

Most people, when they think of fungi, will think of mushrooms. However, the majority of fungi do not produce such large and obvious structures as mushrooms; the majority of fungi are microscopic decomposers, whose minute fruiting bodies would be easily overlooked by those not looking for them. But tiny as these organisms are, they can have a significant effect on your life.

The Diaporthales are one order of these microfungi. They are a well-defined order of ascomycetes with brown or black perithecia (almost entirely enclosed fruiting bodies with only a single pore at one end and the spores produced inside) submerged either within a stroma (mass of hyphal tissue) or in the surrounding substrate on which they are growing (Rossmann et al., 2007). In many Diaporthales, the opening pore of the perithecia is on a long neck that may or may not also be submerged; it is the combination of round perithecium and elongate neck that lead the authors of one recently-described genus to dub it Lollipopaia (Inderbitzin & Berbee, 2001).


Pycnidia of Cryphonectria parasitica protruding from chestnut bark. Pycnidia resemble perithecia, but differ in containing asexually- rather than sexually-produced spores. Photo from here.

Most Diaporthales are decomposers of rotting wood. As such, they rarely come to humanity's attention, though it probably wouldn't take us long to notice if they disappeared. A small but significant number of Diaporthales, however, have earned a great deal of attention from humans because, while they grow on wood just like their relatives, they don't have the courtesy to wait for the tree to die first. The most famous (or notorious, depending on your preferred choice of adjectives) of Diaporthales is undoubtedly Cryphonectria parasitica, the cause of chestnut blight and famed as the bane of the American chestnut, C. dentata. According to Wikipedia, C. dentata may have made up as much as a quarter of the forest in the Appalachian region of eastern North America prior to the arrival of chestnut blight around 1905; by 1940, it was almost extinct. To this day, the position of the American chestnut across most of its original range remains tenuous; complete extinction has been staved off by the chestnut's ability to produce subsidiary shoots from its base, meaning that a number of trees survive despite being reduced to the central boles. However, complete regrowth is likewise prevented by the fungus attacking any new shoots before they achieve significant growth. Meanwhile, attempts to breed blight-resistant strains of American chestnut are hampered by the tree's slow growth rate.


Three views of American chestnut (Castanea dentata). On the left, American chestnut trees as they could still be found in 1910. In the centre, American chestnut as it survives today - an understorey regenerating shrub, prevented from reaching full growth by the inevitable onset of blight. On the right, the intermediary stage in a grown chestnut felled by the fungus. Images from Ellison et al. (2005).

When chestnut blight was recorded in European chestnut trees (Castanea sativa) in Italy in 1938, people expected a repeat of the American experience. And at first, that was almost exactly what happened - chestnut blight spread rapidly through western Europe, slowed only by the more scattered distribution of its host (C. sativa was not originally native to most parts of Europe, but introduced by the Romans; as a result, it does not form continuous forests in Europe as C. dentata did in America, but is largely only found where it has been deliberately planted by humans). However, during the 1950s and 1960s, reports started coming in of stands of chestnuts that appeared to be coping surprisingly well despite the obvious presence of blight (Heiniger & Rigling, 1994), with the damage from the blight extending only a short way into the wood (as it does in the Asian chestnut Castanea crenata, the original host of the fungus). What was more, when fungal hyphae from these wimpier infections were transplanted into further chestnut trees amongst more normal raging infections, the more virulent infections began to heal. The reduced virulence turns out to be due to a virus infecting the fungus - the disease being cured by a disease of its own. The spread of reduced virulence among chestnut blight in Europe has massively reduced the European epidemic. Attempts to implement the same cure in North America, however, have mostly resulted in failure (Milgroom & Cortesi, 2004). Transmission of reduced virulence between fungal colonies is slow and ineffecient, and in most cases seems to require direct human intervention to be truly effective. While this direct intervention is feasible with the more scattered European chestnut, it offers little hope of restoring the prior forests of American chestnut.

Other species of Diaporthales cause diseases in other crop trees and plants (including butternut canker caused by Sirococcus clavigignenti-juglandacearum, which I'm sure is a terrible thing to be afflicted by, even if it does sound like the name of some sort of confectionary). Dogwood anthracnose is caused by Discula destructiva, recently shown to be an anamorphic (asexual) member of the Diaporthales. Cytospora species attack Eucalyptus, while Greeneria uvicola causes bitter rot in grapes. If you feel enticed to explore the systematics and characteristics of the various subgroups of Diaporthales, there's an impressively detailed coverage on the U.S. Department of Agriculture's Diaporthales page, including a big interactive tree where clicking on a clade brings up descriptions and images to help you while away the hours.

REFERENCES

Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliott, C. R. Ford, D. R. Foster, B. D. Kloeppel, J. D. Knoepp, G. M. Lovett, J. Mohan, D. A. Orwig, N. L. Rodenhouse, W. V. Sobczak, K. A. Stinson, J. K. Stone, C. M. Swan, J. Thompson, B. Von Holle & J. R. Webster. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3 (9): 479-486.

Heiniger, U., & D. Rigling. 1994. Biological control of chestnut blight in Europe. Annual Review of Phytopathology 32: 581-599.

Inderbitzin, P., & M. L. Berbee. 2001. Lollipopaia minuta from Thailand, a new genus and species of the Diaporthales (Ascomycetes, Fungi) based on morphological and molecular data. Canadian Journal of Botany 79: 1099-1106.

Milgroom, M. G., & P. Cortesi. 2004. Biological control of chestnut blight with hypovirulence: a critical analysis. Annual Review of Phytopathology 42: 311-338.

Rossmann, A. Y., D. F. Farr & L. A. Castlebury. 2007. A review of the phylogeny and biology of the Diaporthales. Mycoscience 48: 135-144.

Reference Review: The Trials of Anamorphic Taxa

Skovgaard, K., S. Rosendahl, K. O’Donnell & H. I. Nirenberg. 2003. Fusarium commune is a new species identified by morphological and molecular phylogenetic data. Mycologia 95(4): 630-636.

Fusarium is a genus of filamentous soil fungi (shown above in a diagram from here) that is best known as a cause of a selection of nasty diseases of crop plants. It is an anamorphic genus - that is, it includes taxa that reproduce asexually. Fungal taxonomy maintains a complicated system of classifying asexual anamorphs separately from sexual teleomorphs, at least at the generic level (for instance, Fusarium anamorphs are associated with various teleomorphs of the family Nectriaceae - Rossman et al., 1999). In the past, there were separate families and higher for anamorphic taxa, but these have largely been abandoned. This system remains in place despite the fact that some "individual" hyphal masses (inasmuch as one can recognise an individual in fungi) may reproduce both asexually and sexually. In a previous post, I commented that the double taxonomy system was due to a "combination of history, theory and a certain degree of pragmatism". Anamorphs are usually completely different in appearance to teleomorphs, and there is generally no way to tell easily whether a given teleomorph corresponds to a given anamorph (usually, the only way to make a connection is to luck out and find one of the double-dipping hyphae I refered to a moment ago). Even when a connection is made, there is not necessarily a one-to-one relationship between anamorph and teleomorph - one anamorph may correspond to more than one teleomorph. There are even cases known where an anamorphic taxon is found worldwide, but its apparent teleomorph is only known from a very restricted location. A theoretical component can be invoked, too - species concepts are supposed to reflect gene flow, and gene flow is generally not occurring between anamorphic and teleomorphic lines. There are issues with the double taxonomy system, of course - perhaps most significantly, anamorphic taxa seem to be something of the poor cousins of mycology. Despite their being far more abundant in the environment, anamorphs seem to receive only a fraction of the attention given to their more glamorous teleomorphic counterparts.

I think it's worth noting that almost all anamorphic taxa are treated as essentially artificial form-taxa. Thus, while Fusarium seem to all fall within the Nectriaceae, there is no assumed guarantee that taxa with a Fusarium anamorph necessarily form a monophyletic unit. One teleomorphic genus may include members with a number of different anamorphic forms, that each may be shared with members of other teleomorphic genera. Attempts to try to restrict anamorphic genera phylogenetically, such as Sampaio et al. (2003), are relatively few and far between.

With that background explanation dealt with, on to the description of Fusarium commune Skovgaard et al., 2003. One of the big problems with taxonomy of anamorphic is that, well, there's often not that much to work with. All the flashy characters, the colourful mushrooms, the pungent truffles, the wierd-shaped fruiting bodies, are sexually-reproducing structures of teleomorphs. When a fungus is not actively fruiting, one collection of hyphae looks much like another. And conidia, the structures that give off asexually-produced spores in anamorphs, are often not much more than budding extensions of hyphae. As a result, useful morphological characters of anamorphs are few and often somewhat vaguely distinguished.

It should therefore come as no surprise at all that when molecular data was applied to anamorphs, it seemed that the amount of diversity present had been significantly underestimated. Convergence in anamorphs is rampant, and two morphologically near-identical samples may easily turn out to be very distant phylogenetically. So when morphological taxonomy has proven insufficient, in steps the substitute of molecular taxonomy. And that, I'm afraid, is where my hackles start to raise themselves just a little.

The use of molecular data in taxonomy is a much-abused field. Generally speaking, molecular data cannot resolve species. Any analysis of molecular data results in a branching tree, but species identifications are supposed to be about identifying gene flow in networks. There is no magic figure for "x% genetic divergence = different species". A single species with a large, widespread population (say, a wide-ranging bird species) may feature a large amount of genetic divergence without barriers to gene flow. In contrast, a cluster of short-range endemic species (e.g. snails that don't move about much at all) may have very little genetic variation within or even between populations without gene flow occurring between them. So any use of molecular taxonomy should be approached with extreme caution.

I'm glad to say that Skovgaard et al. seem to get it mostly right as far as I can tell. They use 15 different isolates of the new molecular species - a very important step in fending off the spectre of sample contamination. And they also identify some morphological traits supporting the new species. Fusarium commune differs from the closely related F. oxysporum in producing polyphialides and long, slender monophialides when grown in the dark*, while F. oxysporum produces short monophialides only (phialides are the hyphal branches that produce conidia - if I interpret correctly, polyphialides produce spores in multiple axes, while monophialides only have one axis). I am a little mystified as to why there are no samples of F. blasticola, referred to in the article text as very similar to F. commune, included in the molecular analysis. However, Skovgaard et al. do demonstrate the distinction of F. commune from F. blasticola through a pathogenicity test. Fusarium blasticola is a pathogen of Picea (spruces) and Pinus (pines). Despite specimens of these two hosts being grown for five months in soil inoculated with cultures of F. commune, no sign of infection was noticed. Fusarium commune has since been shown to be able to cause infection in Pseudotsuga (the Douglas fir), another commercial conifer (Stewart et al., 2006).

REFERENCES

Rossman, A. Y., G. J. Samuels, C. T. Rogerson & R. Lowen. 1999. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Studies in Mycology 42: 1-248.

Sampaio, J. P., M. Gadanho, R. Bauer & M. Weiss. 2003. Taxonomic studies in the Microbotryomycetidae: Leucosporidium golubevii sp. nov., Leucosporidiella gen. nov. and the new orders Leucosporidiales and Sporidiobolales. Mycological Progress 2(1): 53-68.

Stewart, J. E., M.-S. Kim, R. L. James, J. R. Kasten Dumroese & N. B. Klopfenstein. 2006. Molecular characterization of Fusarium oxysporum and Fusarium commune isolates from a conifer nursery. Phytopathology 96 (10): 1124-1133.

Reference Review: Messing about with Mildews

Before I start, a reminder that I'll be putting up the Boneyard tomorrow evening, so get any posts for it in quick. Don't forget that Saturday comes earlier for us antipodeans than it does for you European and North American sorts!



Hosagoudar, V. B. 2003. Armatellaceae, a new family segregated from the Meliolaceae. Sydowia 55: 162-167.

It seems that this is Fungal Week here at Catalogue of Organisms - I've barely mentioned them in the past, and suddenly two posts on fungi in rapid succession. Not that I'm complaining - fungi are one of my favourite groups of organisms, and few things are more exciting than coming across some bizarre-looking fungus growing from a rotting log in some damp patch of forest. But as with Wednesday's post, today's subjects come from the less obvious but far more numerous sector of fungal diversity.

Black or dark mildews are parasitic fungi found on plants, particularly the leaves. There are a number of largely unrelated families of ascomycetous fungi that cause black mildew (the picture above from here shows a leaf infected by Apiosporum salicinum - I haven't been able to establish if Apiosporium is closely related to the specific family I'm dealing with today, but the general appearance is probably similar). Though parasitic on a number of food species, none of the black mildews is significant enough to have attracted a huge amount of research attention (reading between the lines, I suspect that they are also somewhat overlooked because they are more significant in the tropics than in temperate developed countries). According to Hosagoudar (2003), their growth on leaves raises the temperature in the affected area, increasing respiration and transpiration rates and reducing photosynthetic efficiency and therefore growth.

The greater part of Hosagoudar (2003) is taken up by a whirlwind tour of the taxonomic history of the Meliolaceae, one of the families of black mildews. At the time of Hosagoudar's writing, Meliolaceae was the only family in the order Meliolales, distinguished by the unique combination of features of an ectophytic (living on the surface of leaves) mycelium with lateral appresoria (swollen points on the hyphae that press against the leaf and give rive to hyphae piercing the leaf surface) and phialides (hyphal cells producing successive spherical asexual spores in chains). At the end of the paper, almost as an afterthought, Hosagoudar establishes the family Armatellaceae for a single genus, Armatella, previously included in Meliolaceae, that lacks phialides and also differs from Meliolaceae proper in having 1-septate ascospores as opposed to 3- to 4-septate ascospores.

I have rather a problem with this sort of setup. Armatella is separated from the other Meliolaceae solely on typological grounds, without any sort of detailed analysis to establish whether the remaining Meliolaceae are truly more closely related to each other than to Armatella. The most recent Outline of Ascomycota (Eriksson, 2006) accepts Armatellaceae in Meliolales, but the Notes on ascomycete systematics that first recorded Hosagoudar's publication (Eriksson, 2005) had a much more cautious reaction, noting that another genus, Diporotheca, had previously been isolated in its own family from Meliolaceae on the basis of lacking phialides. While Hosagoudar (2003) did mention Diporotheca in his taxonomic overview, no comparison of Armatella to Diporotheca was recorded. It is worth noting that in a later paper that Hosagoudar himself is an author on, Armatella has managed to quietly reinsert itself back into Meliolaceae (Biju et al., 2005)*.

*Two other possibilities must be acknowledged here, though: (A) Hosagoudar is not primary author on the latter paper, and it may be that the chosen classification represents the views of the primary author and not those of Hosagoudar, and (B) the time difference between 2003 and 2005 is small enough that Hosagoudar's contribution to the 2005 paper may have actually occurred before he wrote the 2003 paper, with a delay in the appearance of the 2005 paper at either the collation or publication stage.

My even bigger issue, however, is to ask what exactly is the point of establishing a monogeneric family. The concept of 'ranking' is, in my opinion, one of the biggest issues in classification today, and I currently have something of a hate-hate relationship with ranks. It is a widely-known secret that all taxonomic ranks (with the probable, but controversial, exception of the 'species') are essentially arbitrary concepts, and there is no real reason why a given taxon should be recognised as an order or a family or whatever beyond how it sits in relation to other related taxa that have previously been recognised as orders or families or whatever. Different historical factors in research on different groups of organisms mean that a family of insects is in no way a comparable unit to a family of birds or plants or fungi. I personally try to avoid referring a taxon to a specific rank, at least in the privacy of my own head. The problem that really makes me grit my teeth, however, is that when it comes to trying to discuss biodiversity to other people, ranks prove so irritatingly convenient! Most people who don't have to deal with the details of classification every day find it relatively easy to grasp the concept that each rank corresponds to a certain level of superficial distinction (at least from our own human-centric viewpoint), and that a genus represents a smaller degree of distinction than a family, which is in turn less distinct than an order. Also, try as I might, there's only so many times I can use a variation on "clade" or "group" without becoming repetitive, confusing or both (and besides, I usually end up having to refer to "clade A" and "subclade B", invoking an even more arbitrary sort of ranking to indicate that B is a section of A, even though there's no actual difference between "clade" and "subclade" and, were I to change my focus slightly, I might end up referring to "clade B" and "subclade C").

However, given that where and what an individual author chooses to recognise as a given rank is essentially subjective, what does separating a genus into its own family really tell us? The prior establishment of the genus already tells us that it is a distinctive unit. There is a certain virtue to establishing a different concept of the taxon "Meliolaceae" from the taxon "Meliolales", rather than the previous set-up where there were two names for the exact same thing, but in establishing the taxon "Armatellaceae" to contain only "Armatella", we again have two names for the exact same thing, and that's just cluttering up the nomenclature.

Postscript: Unless I head them off at the pass now, it is entirely likely that someone will weigh in on the comments with the PhyloCode argument (I'm looking at you, Mike)*. Someday I'm going to be forced to actually say something on the whole PhyloCode question, on which I am an inveterate fence-sitter. For now, let it suffice to say that I'm not convinced that introduction of the PhyloCode principles would particularly improve matters in corners of phylospace such as this one where the vast majority of taxa still have not been phylogenetically investigated to a significant degree, and while yes, PhyloCode may stabilise taxon definition, taxon content here would probably continue to leap about like a drunken grasshopper.

*Some of you may know Mike Keesey as the author of the Dinosauricon, which was one of the first major web resources on Dinosauria, and I came to know his by-line well back in my DML days. The link above takes you to his brand-spanking new blog, so take a look!

REFERENCES

Biju, C. K., V. B. Hosagoudar & T. K. Abraham. 2005. Meliolaceae of Kerala, India - XV. Nova Hedwigia 80 (3-4): 465-502.

Eriksson, O. E. (ed.) 2005. Notes on ascomycete systematics. Nos 3912-4298. Myconet 11: 115-170.

Eriksson, O. E. (ed.) 2006. Outline of Ascomycota - 2006. Myconet 12: 1-82.