Microbotryum violaceum (Pers.:Pers.) G.Deml & Oberw.   
   (= Ustilago violacea (Pers.) Roussel)   

Kingdom: Fungi
Phylum: Basidiomycota
Subphylum: Pucciniomycotina
Class: Microbotryomycetes

British distribution: Evidently widespread, and locally frequent, but much confused with related species.
World distribution: Europe, N. America, no doubt elsewhere.

The Microbotryum violaceum complex encompasses a number of very closely related, partially to completely host-specialised taxa, a number of which have been claimed to be separate species (see below). This account deals with M. violaceum in the restricted sense of recent British literature, i.e. a parasite on Silene species — in Britain particularly of Ragged Robin, Silene flos-cuculi (= Lychnis flos-cuculi) and of Nottingham Catchfly, S. nutans, but formerly regarded as a parasite of a number of species of the plant family Caryophyllaceae. This account has been revised with materials at hand to reflect current taxonomy, but may not be complete or up to date.

Microbotryum violaceum in anthers of Ragged Robin
Microbotryum violaceum in anthers of Ragged Robin (Silene flos-cuculi), Aberlady Bay, East Lothian, 1986.

Long considered to be an 'anther smut' in the large genus Ustilago, this fungus is now regarded as a member of a small class, the Microbotryomycetes, which are not true smuts at all, but related instead to the rusts (Pucciniomycetes).

Previously regarded as occurring widely in flowers of members of the Pink Family (Caryophyllaceae), the host range of the species is now believed to be more restricted, but, due to confusion with related species (see below) and uncertainty about species-concept, this host range remains uncertain. In the sense of the current British Basidiomycete checklist (Legon et al., 2005), it is largely or perhaps entirely, confined to species of Silene (including Lychnis). However, the taxonomy of Microbotryum remains highly confused and M. violaceum may well be better regarded as a single species, with a number of host-specialised variants. Alternatively, in the very narrowest sense, true M. violaceum may be restricted to Nottingham Catchfly, Silene nutans.

The common 'pucciniomycetaceous smut' in the anthers of Red Campion (S. dioica) and White Campion (S. latifolia), formerly included under this species, is now separated as M. lychnidis-dioicae.

As in the case of the true anther smuts, the fungus completely takes over the anthers of the host, which burst open to release the purple, powdery teliospores instead of pollen. These spores are then, in the main, spread by the normal insect pollinators for the host species. Infection is evidently systemic, and infected plants usually show somewhat reduced vigour, though this is often not obvious.

Microbotryum violaceum in anthers of Nottingham Catchfly
Microbotryum violaceum in anthers of Nottingham Catchfly, close view

Microbotryum violaceum in anthers of Nottingham Catchfly (Silene nutans), Isle of Wight, May 2004.

The host is normally heterostylous, with the stamens exserted in two positions, the anthers being cream or pink-brown (colour controlled by the heterostyly?). Infected plants were noticably less vigorous and the anthers remained clustered in the mouths of the corollas.

There is, in the literature, a Ustilago silenes-nutantis, apparently not transferred to Microbotryum, originally described on this host, and correctly treated by Vánky (2004) as included in M. violaceum. It is evident that the name was originally published as a result of mistaken assignation of the original application of "Ustilago violacea", the type specimen of the species actually being on Silene nutans (Lutz et al., 2005).

The fungus may need further study, including its apparent control or suppression of heterostyly in the host.


Taxonomy (part 1)
Mordue & Ainsworth (1984), in their authoritative review of British smuts, recognised just the one species in this complex, as Ustilago violacea, and cited as hosts a number of species within the Pink Family (Caryophyllaceae). They noted that it showed host specialisation within the species and that a number of further species had been named within the complex, but preferred to maintain a broad species concept – still a reasonable view!

However, six British species are recognised in the recent Basidiomycete checklist (Legon et al., 2005), and seven by Spooner & Legon (2006). These are:
M. violaceum (sensu stricto), on "various Caryophyllaceae, especially Lychnis flos-cuculi" [i.e. Silene flos-cuculi in current taxonomy] (Legon et al., op. cit.). It may be that M. violaceum is entirely confined, in Britain, to the genus Silene as currently defined (see Stace, 2010), but this or closely similar taxa are reported elsewhere also on Dianthus, Gypsophila and Petrorhagia (Vánky 1994, 1998, 2004). Type material was on Silene nutans (see above).
M. dianthorum, on pinks (Dianthus species), notably Carnations (D. caryophyllus cultivars and/or hybrids). At least formerly an economically serious plant disease in glasshouses, but seemingly not recently reported. As M. dianthorum has not been recorded on our native Dianthus species, it presumably has been an ephemeral introduction.
M. lychnidis-dioicae, a common species on Red Campion (Silene dioica) and White Campion (S. latifolia). The fungus on Red Campion has recently been further separated as M. silenes-dioicae, though this is probably better considered to be a genetic variant within the broader species.
M. major, on Breckland Catchfly (Silene otites). The host plant is nationally rare, confined to the Breckland of East Anglia, and like most other special species of this unique and once wonderful area, has suffered a catastrophic decline through habitat destruction. There appear to have been no British records of M. major for many years.
M. saponariae, recently found on Soapwort (Saponaria officinalis) and evidently an introduction, as is its host.
M. silenes-inflatae, on Bladder Campion (Silene vulgaris) and Sea Campion (S. uniflora). ["S. inflata", also given as a host in recent British mycological literature cited above, is merely an old synonym of S. vulgaris.] It should be noted that the recently described M. lagerheimii also occurs on these hosts and is cited from Britain on the latter (see below), and that M. violaceo-irregulare, with verrucose-reticulate spores, is known on Silene vulgaris in Europe (but is montane).
M. stellariae, on Myosoton and Stellaria species, common on Lesser Stitchwort (Stellaria graminea).

At the time of writing, this is also the list of accepted British species in the complex as given in the British Mycological Society GB Checklist of Fungal Names.

Additionally, Spooner & Legon give a British record for M. duriaeanum (alternatively placed in the genus Haradaea), in capsules of Sticky Mouse-Ear (Cerastium glomeratum) and having larger spores than the M. violaceum complex, 11–15 µm in diameter, known in Europe on other chickweeds. Several further Microbotryum species (mostly alternatively placed in the genus Bauhinus) are now known in Britain on members of the related Dock and Knotweed Family, the Polygonaceae, and also on scabious species (Knautia, Succisa).

The spores of M. violaceum have spores 6–11 µm in diameter, with raised meshes on the surface that are rounded to regularly polygonal and up to 1 µm in diameter (details from Vánky, 1994, 1998, 2004). M. dianthorum has slightly smaller meshes, and both M. lychnidis-dioicae and M. silenes-inflatae have meshes that are irregularly polygonal. Vánky (2004) considered these differences to be small, and pointed out that further published species names fall within this group, recommending that it would be better to recognise "M. violaceum, sensu lato" until there was further clarification, e.g. molecular work that includes type material. Vanky (1994) provided scanning electron micrographs of spores of most of the then recognised European species.

M. stellariae is distinguishable by smaller spores, 5–8 µm in diameter.
M. major takes over not only the anthers of its host but also the ovaries and much of the base of the flower.
Spooner & Legon (op. cit.) describe the British collection of M. saponariae as having a somewhat darker spore mass than related species and spores 6.2–7.5 µm in diameter.

Taxonomy (part 2)
Recent years have seen numerous studies of the molecular taxonomy of the Microbotryum violaceum complex. A number of additional, cryptic species have been recognised and named, representing genetic host-specialisation. A broadly based study by Kemler et al. (2006) provides support for accepting several species within the complex, equating with the taxonomic treatment outlined above. Despite little morphological divergence, M. dianthorum forms a well defined taxon infecting the genus Dianthus, and M. saponariae and M. stellariae also stand out. Those species parasitising Silene prove to be more closely related, but M. lychnidis-dioicae appears distinct, as does the single sample of M. major. Less certain is the validity of separating M. silenes-inflatae, on Silene vulgaris and S. uniflora (as S. maritima), from what they regarded as M. violaceum, sensu stricto, on Silene nutans.

There is now a very substantial body of scientific literature comparing strains on different host species, demonstrating further genetic differentiation and isolation (see, e.g. Le Gac et al., 2007; Giraud et al., 2008; De Vienne, et al., 2009), and a number of such strains have been given names as species. However, it is evident that gene flow does occasionally occur between strains and that further strains are liable, even if rarely so, to arise by hybridisation (see, e.g., Devier et al., 2010). Speciation may well be reticulate, producing a series of microspecies that might better be termed "formae speciales" as recognised in rusts, or named as subspecies or simply just as varieties, within a more formal taxonomic treatment of M. violaceum. It would be simplistic to assume that there will only ever be one microspecies adapted to any one host plant throughout its range. One recently named entity, "M. lagerheimii", of apparent hybrid origin, indeed duplicates the host specificity of other taxa and shows broader host range, including Silene vulgaris and S. uniflora. It is cited on the latter for Britain (Devier et al., op. cit.). The impression is that there are currently two schools of thought amongst researchers, those who regard every molecularly distinguishable variant as another species to be named, and those who accept M. violaceum as a single species, at least on Silene, within which there is a degree of genetic specialisation. Outside specialist laboratories, the latter would seem the only practical taxonomy.

•   De Vienne, D.M., Refrégier, G., Hood, M.E., Guigue, A., Devier, B., Vercken, E., Smadja, C., Deseille, A., & Giraud, T., (2009), Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. Journal of Evolutionary Biology 22: 683–698.
•   Devier, B., Aguileta, G., Hood, M.E., & Giraud, T., (2010), Using phylogonies of pheromone receptor genes in the Microbotryum violaceum species complex to investigate possible speciation by hybridization. Mycologia 10: 689–696.
•   Giraud, T., Yockteng, R., López-Villavicencio, M., Refrégier, G., & Hood, M.E., (2008), Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryotic Cell 7: 765–775.
•   Kemler, M., Göker, M., Oberwinkler, F., & Begerow, D., (2006), Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urendiniomycetes). BMC Evolutionary Biology 6 (35). [Available online:].
•   Le Gac, M., Hood, M.E., Fournier, E., & Giraud, T., (2007), Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61: 15–26.
•   Legon, N.W., Henrici, A., Roberts, P.J., Spooner, B.M., & Watling, R., (2005), Checklist of the British and Irish Basidiomycota, Royal Botanic Gardens, Kew.
•   Lutz, M., Göker, M., Piatek, M., Kemler, M., Begerow, D., & Oberwinkler, F., (2005), Anther smuts of Caryophyllaceae: molecular characters indicate host-specific species delimitation. Mycological Progress 4: 225–238.
•   Mordue, J.E.M., & Ainsworth, G.C, (1984), Ustilaginales of the British Isles. Mycological Papers 154, Commonwealth Mycological Institute, Kew.
•   Spooner, B.M., & Legon, N.W., (2006), Additions and amendments to the list of British smut fungi. Mycologist 20: 90–96.
•   Stace, C.A., (2010), New flora of the British Isles, (3rd ed.), Cambridge University Press, Cambridge.
•   Vánky, K., (1994), European smut fungi, Gustav Fischer Verlag, Stuttgart.
•   Vánky, K., (1998), The genus Microbotryum (smut fungi). Mycotaxon 67: 33–60.
•   Vánky, K., (2004), Anther smuts of Caryophyllaceae. Taxonomy, nomenclature, problems in species delimitation. Mycologia Balcanica 1: 189–191.

© A.J. Silverside
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