A Brief Taxonomic Overview
by Eric W.A. Boehm
Morphology: Hysteriaceous fungi classified in or previously affiliated with the Hysteriaceae, Gloniaceae and Mytilinidiaceae possess unusual fungal fruiting bodies or ascomata, structures that set them apart from other ascomycetes, which typically possess flask-shaped (perithecia), closed (cleistothecia) or open (apothecia) ascomata. Among hysteriaceous fungi, the ascomata is typically elongated to some degree, and opens by a longitudinal slit-like structure that runs parallel to the long axis of the fruitbody. Being bitunicate ascomycetes and therefore members of the loculoascomycetes, in this group the ascomata are termed pseudothecia. In the Hysteriaceae, the pseudothecium is termed a hysterothecium. It is carbonaceous, long-cylindrical, cuniform or boat-like (navicular), immersed to erumpent to entirely sessile, sometimes slightly elevated, but always firm-walled, stout, and equipped with a longitudinal, invaginated slit or sulcus that runs the length of the fruitbody. Hysterothecia are capable of opening partially to reveal a lenticular, disk-like hymenium or closing tightly in response to relative humidity suggesting a perennial nature to the fruitbody. In contrast, in the Mytilinidiaceae, the pseudothecium is an upright globoid to mussel- or clam-shaped (conchate) or hatchet-shaped (dolabrate) structure, strongly laterally compressed, standing on edge, carbonaceous, but, most importantly, thin-walled and fragile, sometimes borne on a narrow stalk. In this family the pseudothecium is apically provided in most species with a prominent narrow keel or cristate apex that runs longitudinal to the long axis of the fruitbody (Zogg 1962). In the Gloniaceae, the hysterothecia are also modified, but here they form laterally fused, bifurcating or radiate, stellate composites, often associated with subicula. Molecular data indicate that the Hysteriaceae (Hysteriales) resides close to the Pleosporales, within the Pleosporomycetidae (Dothideomycetes), whereas the Mytilinidiaceae (Mytilinidiales) is more distant, and instead finds close association with the new family Gloniaceae (Boehm et al.2009a, b). Ascospores are highly diverse, ranging from pedicillate amerospores (Farlowiella), hyaline and pigmented didymospores (Psiloglonium, Glonium, Actidiographium & Actidium), hyaline and pigmented phragmospores (Hysterium, Mytilinidion [subgen. Eumytilnidion], Gloniella), pigmented dictyospores (Hysterographium, Hysterocarina, Ostreichnion, & Ostreola), elongated scolecospores (Mytilinidion [subgen. Lophiopsis]), to filiform spores (Lophium & Glyphium). Spore morphology, based on septal configurations, pigmentation, symmetry etc., has historically been considered synapomorphic character states, and thus useful to delineate genera (Zogg 1962). However, recent molecular evidence (Schoch et al. 2007; Boehm et al. 2009a, b; Mugambi & Huhndorf 2009) has called this into question. The new data underscores the propensity for spore morphology to be highly homopleisious, and therefore not a sound basis for reconstructing natural phylogenetic relationships within this group of fungi. As such, the newly revised genus Gloniopsis and the newly described genus Hysterobrevium now include both hyaline and pigmented dictyospores; likewise, the newly described genus Oedohysterium includes both phragmospores and dictyospores within a single genus (Boehm et al. 2009b). The hysterothecium, the defining feature of the Hysteriaceae, has evolved convergently no less than five times within the Pleosporomycetidae (e.g., Anteaglonium, Farlowiella, Glonium, Hysterographium and the Hysteriaceae). Similarly, thin-walled mytilinidioid (e.g., Ostreichnion) and patellarioid (e.g., Rhytidhysteron) genera, previously in the Mytilinidiaceae and Patellariaceae, respectively, transferred to the Hysteriaceae, have also evolved at least twice within the subclass (Boehm et al. 2009b). As such, character states traditionally considered to represent synapomorphies among these fungi, whether they relate to spore septation or the ascomata, in fact, represent symplesiomorphies, and most likely have arisen multiple times through convergent evolutionary processes in response to common selective pressures.
Historical Overview: Due to the seemingly transitional nature of the ascoma, neither fully open nor closed, hysteriaceous fungi have been placed in the discomycetes and pyrenomycetes about equally by various mycologists throughout the 19th Century (Bisby 1923). In his Systema Mycologicum, Fries (1823) initially considered hysteriaceous fungi to belong to the pyrenomycetes and placed them in the Phacidiacei, but later (Fries 1835) placed them in his new class Discomycetes, stating: “Transitum sistunt ad Discomycetes, sed discum verum non monstrant.” Chevallier (1826) recognised the unique nature of the hysterothecium and established the Hysteriineae, which he considered as pyrenomycetes distinct from Fries’ Phacidiei. Corda (1842), on the other hand, retained the Phacidiei within the Hysteriaceae, and divided the family into a number of subfamilies. De Notaris (1847) considered the Hysteriaceae to belong to the pyrenomycetes and used spore pigmentation to classify hysteriaceous fungi into the Phaeosporii and the Hyalosporii. Saccardo (1873) initially followed Fries, but later (1874) placed hysteriaceous fungi in the pyrenomycetes, and carried de Notaris’ (1847) spore classification scheme further by dividing the Hysteriaceae into nine sections based on pigmentation and the morphology of spore septation (Saccardo 1883). Ellis & Everhart (1892), in their North American Pyrenomycetes, tentatively included the Hysteriaceae, but stated that they had not at first intended to do so due to the transitional nature of the hysterothecium. In Rabenhorst’s Kryptogamen-Flora, Die Pilze, Rehm (1896) compromised and placed the Hysteriales as an order intermediate between the pyrenomycetes and the discomycetes. Mytilinidioid fungi have also historically been classified within the family Hysteriaceae, due to perceived similarities in ascocarp morphology, specifically its means of longitudinal dehiscence (Fries 1823, De Notaris 1847, Saccardo 1875, 1883, Ellis & Everhart 1892, Massee 1895, Rehm 1896, von Höhnel 1918, Bisby 1923). Modern authors have likewise included mytilinidioid fungi within the Hysteriaceae, placing the family in the Pseudosphaeriales (Nannfeldt 1932, Gäumann 1949), the Dothiorales (Müller & von Arx 1950, von Arx & Müller 1954), the Dothideales (von Arx & Müller 1975), and in a separate order Hysteriales, closely related to the Pleosporales (Miller 1949, Luttrell 1955). The Hysteriales were placed in the subclass Loculoascomycetes by Luttrell (1955), due to the presence of bitunicate asci, corresponding to the Ascoloculares first proposed by Nannfeldt (1932).
Duby (1862) was the first to propose that hysteriaceous fungi be divided into two sections, the Hystériées and the Lophiées, the latter to accommodate mytilinidioid forms. One hundred years later, Zogg (1962) proposed two families: the Hysteriaceae s. str. to accommodate thick-walled hysteriaceous forms, and the Lophiaceae (Zogg 1962, von Arx & Müller 1975) to accommodate thin-walled, mytilinidioid fungi. Barr (1990a) made the argument for retention of the earlier name Mytilinidiaceae over the Lophiaceae, despite the proposal to conserve the latter (Hawksworth & Eriksson 1988). Luttrell (1953) studied ascomatal ontogeny and hamathecial development in Glonium stellatum Muhl. and concluded that the Hysteriaceae possess the pseudoparaphysate Pleospora-type centrum, in which cellular, septate pseudoparaphyses grow downwards from the cavity roof, initially anchored at both ends, and occupy the locule prior to the formation of asci (Luttrell 1951). Luttrell (1973) held a wide concept of the Hysteriales, but did not recognise the family Lophiaceae, instead proposing a subfamily, the Lophioideae, within the Hysteriaceae to accommodate mytilinidioid forms. Barr (1979) however maintained the two-family distinction. The Mytilinidiaceae was placed in the Melanommatales based on a thin-walled peridium of scleroparenchymatous cells enclosing a hamathecium of narrow trabeculate pseudoparaphyses, asci borne in a peripheral layer and with ascospores typically showing bipolar symmetry (Barr 1987, 1990a). Later, Barr & Huhndorf (2001) noted that the family was somewhat atypical of the Melanommatales, in that, as a consequence of reduced locule space attributed to lateral compression, they possess a basal, rather than peripheral, layer of asci and a reduced hamathecium at maturity. More recently, the Melanommatales have been included within the Pleosporales (Lumbsch & Huhndorf 2007). Barr (1983) eventually abandoned the Hysteriales and placed the Hysteriaceae within the Pleosporales due to the presence of cellular pseudoparaphyses, asci borne in a basal rather than peripheral layer and ascospores typically showing bipolar asymmetry. Eriksson (2006) removed the Mytilinidiaceae from the Hysteriales and considered it as Dothideomycetes et Chaetothyriomycetes incertae sedis, leaving the Hysteriaceae as the sole family in the Hysteriales.
Fig. 1. Biodiversity of the Hysteriaceae & Mytilinidiaceae. Taxa are arranged in paired photomicrographs, where bars in the upper figures are 1 mm, whereas bars in lower figures are 10 μm. Hysteriaceae: Fig. 1A & G: , Hysterium pulicare (Lightf.: Fr.) Pers. (BPI 878723); B & H: Hysterium angustatum Alb. & Schw. (BPI 878724); C & I: Hysterium insidens Schw. (EB 0335); D & J: Hysterium sinense Teng (BPI 878730); E & K: Hysterographium mori (Schw.) Rehm (BPI 878731); F & L: Hysterographium subrugosum (Cooke & Ellis) Sacc. (BPI 878735); M & S: Hysterographium flexuosum (Schw.) Sacc. (EB 0098); N & T: Gloniopsis praelonga (Schw.) Zogg (BPI 878725); O & U: Psiloglonium clavisporum (Seaver) Boehm, Schoch & Spatafora (BPI 878726); Gloniaceae: P & V: Glonium circumserpens (Nyl.) Kantvilas & Coppins (BPI 878739); Mytilinidiaceae: Q & W: Mytilinidion thujarum (Cooke & Peck) Lohman (EB 0268); R & X: Lophium mytilinum Pers. : Fr. (BPI 878736). BPI desigations refer to voucher specimens deposited with the US National Fungus Collections.
The Molecular era: More recently, Boehm et al. (2009a) presented the first combined use of DNA and amino acid sequence data to reconstruct the phylogeny of hysteriaceous fungi. This study was based on a wide taxon sampling strategy, and employed four nuclear genes, namely the nuSSU and nuLSU, Transcription Elongation Factor 1 (TEF1) and the second largest RNA polymerase II subunit (RPB2). A number of specific conclusions were reached: (1) Multigene phylogenies provided strong support for the monophyly of the Hysteriaceae and of the Mytilinidiaceae, both within the Pleosporomycetidae. However, sequence data also indicated that both families were not closely related within the subclass. (2) Although core groups for many of the genera in the Hysteriaceae were defined, the genera Hysterium, Gloniopsis, and Hysterographium were demonstrated to be polyphyletic, with affinities not premised on spore septation and pigmentation. (3) The genus Glonium was also shown to be polyphyletic, but along two highly divergent lines. Glonium lies outside of the Hysteriaceae, and instead finds close affinities with the family Mytilinidiaceae, for which was proposed the Gloniaceae fam. nov. (Boehm et al. 2009a), to accommodate the type,G. stellatum Muhl., and related forms. (4) The genus Psiloglonium was reinstated within the Hysteriaceae, with P. lineare (Fr.) Petr. as type, to accommodate didymospored species segregated from Glonium. (5) The genera Mytilinidion and Lophium formed a strongly supported clade within the Pleosporomycetidae, thus defining the monophyletic Mytilinidiaceae, adjacent to the Gloniaceae, for which was proposed the Mytilinidiales ord. nov. (Boehm et al. 2009a). (6) The genus Farlowiella, previously in the Hysteriaceae, was placed as Pleosporomycetidae gen. incertae sedis. (7) The genus Ostreichnion, previously in the Mytilinidiaceae, was transferred to the Hysteriaceae. (8) The genus Rhytidhysteron, previously in the Patellariaceae, was transferred to the Hysteriaceae. These taxonomic changes present a number of challenges for understanding evolution within this group of fungi. The lack of agreement between morphological character states, previously considered synapomorphic (e.g., Zogg 1962), and recent molecular data based on the nuSSU, nuLSU, TEF1 and RPB2 (Boehm et al. 2009a), had resulted in a highly polyphyletic core set of genera for the Hysteriaceae (e.g., Hysterium, Hysterographium, Gloniopsis, and Glonium). This presented us with a complicated picture of past speciation events for the family (Boehm et al. 2009a), which necessitated the second study (Boehm et al. 2009b). Essentially, in this latter study, the challenge was to reconcile discrepancies between morphological and molecular data, in order to more accurately reflect natural phylogenetic relationships within the family. As a result, the revised Hysteriaceae, bears little resemblance to the original concept of the family (Zogg 1962). Molecular data necessitated that we break-up what were once thought to be stable genera (Boehm et al. 2009b). Thus, two species of Hysterium were transferred to Oedohysterium (Od. insidens and Od. sinense), and two species of Gloniopsis to Hysterobrevium (Hb. smilacis and Hb. constrictum). While Hysterographium, with the type Hg. fraxini, was removed from the Hysteriaceae (Boehm et al. 2009), some of its species remained within the family, transferred here to Oedohysterium (Od. pulchrum), Hysterobrevium (Hb. mori) and Gloniopsis (Gp. subrugosa). New species were described (e.g., Gp. arciformissp. nov. and Gp. kenyensis sp. nov.) which would previously have been classified in Hysterographium, but are now accommodated in Gloniopsis. Molecular data necessitated that both Gloniopsis and Hysterobrevium include hyaline and pigmented dictyospores, and the genus Oedohysterium, both phragmospores and dictyospores. This, then, not only de-emphasised spore morphology as a synapomorphic character state for this group of fungi, but, in addition, sets a precedence for the inclusion of dissimilar spore configurations within a single genus. Likewise, the genus Glonium sensu Zogg (1962) was divided into Psiloglonium in the Hysteriaceae and Glonium in the Gloniaceae (Boehm et al. 2009a), and, more recently, Anteaglonium in the Pleosporales (Mugambi & Huhndorf 2009). These taxonomic changes were unexpected, as they were not premised on past assumptions of synapomorphy related to spore morphology (Zogg 1962). Molecular data thus underscores the potential for morphology to be difficult to interpret, and even unhelpful in phylogenetic inference and reconstruction for this group of fungi (Schoch et al. 2006, Boehm et al. 2009, Mugambi & Huhndorf 2009).
Dichotomous Keys: In an effort to facilitate species identification, a number of dichotomous keys were presented in Boehm et al. 2009b and are also presented here, with illustrations. These keys take into consideration taxonomic changes brought about by DNA and amino acid sequencing studies (Schoch et al. 2006; Boehm et al. 2009a, b; Mugambi & Huhndorf 2009), and attempt to provide a morphological basis for the many new relationships revealed by molecular data. Although the keys are based on those first presented by Zogg (1962), they considerably expand upon them to include a number of new species and genera described since the original publication (e.g., Darker 1963; Tilak & Kale 1968; Barr 1975, 1990a; Barr & Blackwell 1980; Amano 1983; Speer 1986; Pande & Rao 1991; van der Linde 1992; Kantvilas & Coppins 1997; Lorenzo & Messuti 1998; Messuti & Lorenzo 1997, 2003, 2007; Vasilyeva 2000, 2001; Chlebicki & Knudsen 2001; Checa et al. 2007; Boehm et al. 2009a, b; Mugambi & Huhndorf 2009). In addition to incorporating new species and genera, the revised keys also take into consideration variation in ascospore measurements as presented by different authors, and include widened distribution reports as well. These keys should also facilitate the description of new species, especially those resulting from investigations into the tropical hysteriaceous biota.