Hysterographium

The genus Hysterographium Corda
Corda, Icon. Fung. Hucusque Cognitorum 5: 34 (1842)

by Eric W.A. Boehm

The genus Hysterographium. A-B. Hysterographium flexuosum (EB 0098, USA).

C-D. Hysterographium fraxini (EB 0100, USA).

Scale bar (habitat) = 1 mm; Scale bar (spores) = 20 μm.

Fig. 4 from Boehm et al. 2009b.

Fragosa Cif., in Ciferri & Fragoso, 1926
Hysteriopsis Spreg., 1906
Hysterium Tode ex Fries (pro parte), 1823
Polhysterium Speg., 1912

Although the genus Hysterographium has been removed from the Hysteriaceae (Boehm et al. 2009a, b), and is currently recognised as Pleosporomycetidae gen. incertae sedis, it is included here. This is because it forms the basis for a number of new combinations within the family (e.g., in the genera Oedohysterium, Hysterobrevium and Gloniopsis, see below). While Corda (1842) included phragmosporous and dictyosporous species in the genus Hysterographium, De Notaris (1847) restricted the genus to species with muriform ascospores only. Zogg (1962), among others, maintained the genus as Hysterographium Corda emend. De Not., however a change in authorship is not warranted (Barr 1990). Clements & Shear (1931) regarded Hg. fraxini (Pers. : Fr.) De Not. as the type. The genus is characterized by pigmented dictyospores, with one to several longitudinal septa, ovoid to ellipsoid-fusoid, relatively broad, usually constricted at the first-formed septum. Zogg (1962) extensively revised the synonymy of the genus and accepted four species: Hg. flexuosum (Schwein.) Sacc. (see Fig. 4A-B in Boehm et al. 2009b) and Hg. fraxini (Pers.) De Not. (Fig. 4C-D in Boehm et al. 2009b), the type, both with large dictyospores, prominently constricted at the median septum, the former with slightly longer, narrower spores. Zogg (1962) also accepted Hg. mori (Schwein.) Rehm and Hg. subrugosum (Cooke & Ellis) Sacc., with smaller, fewer-celled dictyospores, short and squat in the former, longer and more slender in the latter, both also constricted at the median septum. Since then, an additional three species have been described: Hg. minus N. Amano from Japan (Amano 1983), Hg. spinicola Doidge from South Africa, recollected from the thorns of Acacia and validated by van der Linde (1992), with a brick-red epithecium and spores only slightly longer than those of Hg. mori, and, lastly, Hg. pulchrum Checa, Shoemaker & Umaña from Costa Rica, also with a red pigment in the hamathecium (Checa et al. 2007), here transferred to Oedohysterium, as Od. pulchrum (Boehm et al. 2009b). Lastly, Barr (1975) removed Hysterium nova-caesariense Ellis from synonymy with Hg. flexuosum (Zogg 1962) and placed it as Ostreichnion nova-caesariense (Ellis) M.E. Barr in the Mytilinidiaceae. Likewise, Hysterium formosum Cooke, synonymized by Zogg (1962) under Hg. mori, was accepted as Ostreola formosa (Cooke) M.E. Barr, also in the Mytilinidiaceae (Barr 1990).

Four of the seven species were surveyed in Boehm et al. (2009b), with multiple isolates: Hg. mori (8), Hg. subrugosum (3), Hg. fraxini (2) and Od. pulchrum (1), falling into no fewer than three separate clades, two within the Hysteriaceae (Clades A and D in Fig. 1, Boehm et al. 2009b) and one far removed from the family. The latter clade includes the type species for the genus Hysterographium, namely Hg. fraxini, represented by isolates from Switzerland (CBS 109.43), deposited by Zogg in 1943, and from Canada (CBS 242.34), deposited by Lohman in 1934. Hysterographium fraxini forms a well-supported clade distant from the Hysteriaceae, but remains within the Pleosporomycetidae (Boehm et al. 2009a, b). As this is substantiated by two geographically disparate isolates from two different continents, deposited by two reputable workers, it is significant. The implication is that the genus Hysterographium must follow the type species and be removed from the Hysteriaceae. Species with pigmented dictyospores remaining within the Hysteriaceae, previously classified in Hysterographium, must therefore be accommodated in other genera. In this study, these would include the following species, for which we have sequence data: Hg. mori (= Hysterobrevium mori comb. nov.) Hg. subrugosum (Gloniopsis subrugosa comb. nov.) and Hg. pulchrum (= Oedohysterium pulchrum comb. nov.). The remaining species for which we do not have sequence data, namely Hg. minus, Hg. spinicola and Hg. flexuosum, must remain as species of Hysterographium, until such time that sequence data are available. The removal of the genus Hysterographium from the Hysteriaceae was unexpected, as it was not premised on what were once assumed to be syapomorphic character states (Zogg 1962); nevertheless, molecular data support its exclusion from the family (Boehm et al. 2009a, b). Clearly more representatives of Hg. fraxini, as well as of Hg. flexuosum, Hg. minus and Hg. spinicola, for which we are missing data entirely, must be sampled before a clearer picture emerges.

It can be concluded that the genus Hysterographium sensu Zogg (1962) is a highly polyphyletic assemblage of unrelated species, spanning multiple clades not only within the Hysteriaceae, but also with the type, Hg. fraxini, forming a distant clade outside of the family (Boehm et al. 2009a, b). To summarize, molecular data have necessitated the break up of the genus Hysterographium, because the type, Hg. fraxini, no longer resides within the Hysteriaceae (Boehm et al. 2009). This break up has resulted in: (1) the new genus Hysterobrevium (see below), which includes both species with hyaline dictyospores, previously classified as Gloniopsis (Hb. constrictum and Hb. smilacis), and species with pigmented dictyospores, previously classified as Hysterographium (Hb. mori) in Clade A; (2) the inclusion in Gloniopsis of both hyaline (Gp. praelonga) and pigmented (Gp. subrugosa, Gp. arciformis, Gp. kenyensis) dictyospores in Clade D; (3) the inclusion in Oedohysterium of pigmented dictyospored species previously classified in Hysterographium (Od. pulchrum), also in Clade D; and, lastly, (4) the removal of Hysterographium, with the type Hg. fraxini, from the Hysteriaceae, currently placed as Pleosporomycetidae gen. incertae sedis.

As the taxonomy of Hysterographium, Hysterobrevium and Gloniopsis is currently in flux, we chose to provide the following dichotomous key, whereby all hysteriaceous fungi, bearing transversely and longitudinally septate dictyospores, whether pigmented or hyaline, are identified together, with the caveat that unrelated taxa share the same key.

Key to the species of Hysterographium, Hysterobrevium and Gloniopsis

1. Dictyospores, usually shorter than 25 μm → 2

1. Dictyospores mostly longer than 25 μm → 6

2. Dictyospores pigmented, thin-walled, fragile, pronouncedly arcuate or bent, 3-5(-7)-septate, with 1-2(-3) vertical septa, which are mostly associated with the mid-cells, these much larger and swollen than the end-cells, no septal constrictions, (10-)12-18(-22) x 6-10 µm; Kenya → Gloniopsis arciformis E.W.A. Boehm, G.K. Mugambi, S.M. Huhndorf & C.L. Schoch

2. Not with the above combination of characters → 3

3. Dictyospores hyaline at maturity → 4

3. Dictyospores pigmented at maturity → 5

4. Dictyospores highly symmetric in outline and septation, with thickened walls, gelatinous sheath present when young, absent at maturity, (1-)3(-4)-septate, with 1(-2) vertical septa, that may pass through one to two cells; (11-)13-20(-23) x 5-12 μm; Japan, New Zealand → Hysterobrevium constrictum (N. Amano) E.W.A. Boehm & C.L. Schoch

4. Dictyospores asymmetric, with acuminate ends, with a gelatinous sheath when young, mostly 3-5(-9)-septate and with 1(-3) vertical septa, passing through multiple mid-cells, prominently constricted at the median septum, sometimes constriced at multiple septa, (13-)15-26(-31) x (4-)5-9(-10) μm; cosmopolitan → Hysterobrevium smilacis (Schwein.) E.W.A. Boehm & C.L. Schoch

5. Dictyospores thin-walled, obovoid, with obtuse ends, 3-(5-7)-septate, with 1-2(-3) vertical septa, usually associated with mid-cells, but occasionally present obliquely in end-cells, constricted at the median septum, sometimes at additional septa, (12-)14-22(-26) x (5-)7-10(-11) μm; cosmopolitan → Hysterobrevium mori (Schwein.) E.W.A. Boehm & C.L. Schoch

5. Dictyospores thin-walled, very fragile, obovoid, 3(-4[rarely])-septate, highly gutulate when young, spore apices asymmetric, the upper obtuse, the lower acuminate and sometimes drawn out, often with oblique septa in end cell(s), hardly constricted at the septa, measuring (12-)15-18(-19) x 5-7(-8) μm; Kenya → Gloniopsis kenyensis E.W.A. Boehm, G.K. Mugambi, S.M. Huhndorf & C.L. Schoch

6. Red pigment present in hamathecium and/or centrum; dictyospores pigmented → 7

6. No red pigment present, spores pigmented or hyaline → 8

7. Dictyospores, 22-25(-27) x 5-6 μm, with (5-)6 transverse and 1 vertical septum in either cell or both cells adjacent to the primary septum; typically with red pigment in the hamathecium; neotropical (Costa Rica) → Oedohysterium pulchrum (Checa, Shoemaker & Umaña) E.W.A. Boehm & C.L. Schoch

Note: Od. pulchrum is accommodated in the genus Oedohysterium and is present in both keys.

7. Dictyospores 25-28 x 11-13 μm, with 5-6 transverse and mostly one longitudinal septum; hamathecium brick-red; on Acacia thorns, South Africa → Hysterographium spinicola Doidge

8. Dictyospores hyaline or turning brown tardily → 9

8. Dictyospores pigmented in the ascus → 10

9. Dictyospores hyaline turning yellow in age, obovoid, ends usually obtuse, 5-7(-10)-septate, with 2-3 longitudinal septa, constricted at the median and often other septa, gelatinous sheath when young, (16-)20-32(-34) x (6-)9-12(-15) μm; cosmopolitan → Gloniopsis praelonga (Schwein.) Underw. & Earle

9. Ascospores irregularly biseriate, ellipsoid, hyaline but becoming brown tardily, with the upper half generally wider than the lower half, sometimes surrounded by a gelatinous sheath, with 7-13 transverse and 1-3 longitudinal septa, constricted at the median transverse septum; 25-49 x 8-17 μm; Japan → Gloniopsis macrospora N. Amano

10. Dictyospores usually less than 38 µm long → 11

10. Dictyospores 30-80 μm long → 12

11. Dictyospores (22-)25-34(-45) x (6-)8-12(-17) μm, mostly with 7-11 transverse and 1-2 vertical septa; cosmopolitan → Gloniopsis subrugosa (Cooke & Ellis) E.W.A. Boehm & C.L. Schoch

11. Dictyospores 26-38 x 10-15 μm, with 6-13 transverse and 1-3 vertical septa, obovoid, ends obtuse; Japan → Hysterographium minus N. Amano

12. Dictyospores (25-)30-45(-51) x (10-)12-15(-22) μm, with 7-9 transverse and 2-3 vertical septa, obovoid, ends obtuse; cosmopolitan → Hysterographium fraxini (Pers. : Fr.) De Not.

Note: Hysterographium fraxini, the type species for the genus Hysterographium, lies outside of the Hysteriaceae, as Pleosporomycetidae incertae sedis (Boehm et al. 2009).

12. Ascospore outline ellipsoid, fusoid, ends slightly acuminate, (30-)40-65(-80) x (8-)10-18(-19) μm, with 7-15 transverse and 1-3 vertical septa; cosmopolitan → Hysterographium flexuosum (Schwein.) Sacc.

Hysterographium fraxini (Pers. : Fr.) De Not.

de Notaris. 1847. Giorn. Bot. Ital. II, 5 - 52.

Hysterium fraxini Pers., 1801
Hysterographium acerinum Peck, 1913 (Barr, 1990, to H. flexuosum)
Hysterographium baccarinii Scal. (in herb. Saccardo)
Hysterium elongatum Wahlenb., 1812
Hysterographium elongatum (Wahlb.) Corda, 1842
Hysterographium lexuosum Maire, 1930, non (Schw.) Sacc.
Hysterographium fraxini var. minutulum Sacc.
Hysterographium fraxini var. oleastri Desm., 1853
Hysterographium naviculare Karst., 1880
Hysterographium oleae Schwarz, 1933
Hysterographium rehmianum Berl. et Vogl, 1886

Cosmopolitan. On live bark & dead wood of: Populus, Juglans, Corylus, Fagus, Quercus, Cotinus, Acer, Cornus, Fraxinus, Syringa, Olea, Ligustrum, Jasminum, Phillyraea, Bignonia, Catalpa, & Viburnum.

Ellis & Everhart (1892): "Hysterothecia scattered or gregarious, erumpent, elliptical, black, obtuse above, 1-1.5mm long, 0.5-0.75mm wide, lips swollen, smooth, partially open so as to expose the narrow disk. Asci clavate rounded above, 150-200 x 30-40 μm, eight spored with filiform paraphyses. Ascospore biseriate, oblong-elliptical, scarcely constricted in the middle, seven- to nine-septate & muriform, dark yellow brown measuring 30-40 x 15-18 μm. On dead limbs of Fraxinus, NY, PA, IA & Canada. Probably common throughout the USA."

Bisby (1944): "Hysterothecia about 1 - 2 x 0.5mm, erumpent through the cortex, rarely superficial on the wood, dull black, sometimes forming ‘fairy rings'; asci 125 - 200 x 25 - 40 μm, with eight (or fewer) spores; the ascospores are irregularly biseriate, 30 - 50 x 12 - 20 μm, golden to chestnut brown, surrounded by a gelatinous envelope, ellipsoid with ends somewhat narrowed, with or without constriction at the center, having five to ten cross-septa, each locule with none to three longitudinal divisions; paraphyses filiform, branched above & forming a brown epithecium. Nearly all British collections from ash (Fraxinus) branches. European & North American collections appear identical."

Barr (1990): "Ascomata 1 - 2 mm long, 330 μm dia., ellipsoid, widely erumpent; surface smooth, lacking longitudinal striae, longitudinal slit usually depressed; peridium 40 - 45μm wide. Asci 90 x 25 - 30 μm. Ascospores (25-) 30 - 45 (-51) x (10-) 13 - 15.5 (-22) μm, obvoid, ends obtuse, 7 - 9 septate, with 2 - 3 longitudinal septa, constricted at median first-formed septum. Anamorphs coelomycetous; conidiomata developed within periderm of steam-sterilized ash twigs; conidiogenous cells 8 - 12 x 1 - 2 μm, as short branches; conidia 4.5 - 5 x 0.1 - 1.2 μm, hyaline, cylindric (Hysteropycnis fraxini Hilitzer, Lohman, 1932). On woody branches, chiefly Fraxinus, cosmopolitan. Zogg (1943, 1962) studied the development of this species in culture. Infection studies, utilizing pure cultures derived from single ascospores, resulted in the formation of the anamorph &/or the telomorphs on a wide range of woody plants, both gymnosperms & angiosperms. Zogg concluded that H. fraxini was a non-specialized facultative saprobe that was able to spread from dead to living tissues."

van der Linde (1992): "Fruitbodies single or in small groups, superficial, elliptical with rounded ends, straight or slightly curved, usually not branched, 1.5 - 2.0 x 0.2 - 0.5 mm. These dimensions are slightly smaller than those given by Zogg (1962) for this species. Pseudoparaphyses hyaline, septate, thickend apically, branched to form an epithecium. Asci irregularly biseriate, cylindric-clavate, 8-spored, 110 - 120 x 30 - 35 μm. Ascospores dark olive brown, dictyosporous with 5 - 8 transverse septa & 3 longitudinal septa, soemtines slightly curved, 40 - 45 x 12 - 15 μm."

webassets/Hg-fraxini-flexuosum-spores.jpg

Hysterographium fraxini (Pers. : Fr.) De Not. Left: Ellis & Ellis (1985); Zogg (1962), pgs. 34, 35, 131. 2^nd from right Hg. faxini (No. 1, top) & Hg. flexuosum (No. 2, bottom).

Hysterographium flexuosum (Schw.) Sacc.

Saccardo. 1883. Syll. Fung. II: 781.

Hysterium flexuosum Schw., 1822

Hysterium ceanothi Phill. et Hark., 1884a
Hysterographium ceanothi (Phill. et Hark.) Berl. et Vogl., 1886
Lophium naviculare Schw., 1834
Hysterium nova-caesariense Ellis, 1877*
Hysterographium nova-caesariense (Ellis) Ell. et Ev., 1892*
Mytilidion nova-caesariense (Ellis) Rehm (in Sacc., 1883)*
Hysterium prominens Phill. et Hark., 1884a
Hysterographium prominens (Phill. et Hark.) Berl. et Vogl., 1886
Hysterium vulvatum Schw., 1834
Hysterographium vulvatum (Schw.) Sacc., 1883
Hysterographium acerinum Peck (from Barr, 1990)
Hysterographium magellanicum Speg. (from Messuti & Lorenzo, 2003)
Hysterographium fuegianum Speg. (from Messuti & Lorenzo, 2003)
Hysterographium fuegianum f. intermedium Rehm. (from Messuti & Lorenzo, 2003)

Note: Hysterographium nova-caesariense (Ellis) Ell. & Ev. was transferred by Zogg (1962) to Hysterographium flexuosum (Schw.) Sacc. However, Barr (1975) transferred Hysterium nova-caesariense to Ostreichnion nova-caesariense (Ellis) Barr. Barr adds an additional synonym Hysterographium acerinum Peck [Bull. NY State Mus. 167: 43 (1913)]. Somewhat rare. Living bark & old wood of Pinus, Salix, Betula, Fagus, Quercus, Prunus, Gleditschia, Acer, Ceanothus, Vitis, Garrya, Cornus, & Andromeda. Uncommon. North America, Europe (Germany), & South Africa.

Ellis & Everhart (1892) for H. vulvatum: "Hysterothecia erumpent-superficial, scattered or gregarious, 1-3mm long, straight or flexuous; lips at first closed, then open so as to leave a wide furrow between them, mostly with 1-2 deep striae on each side, often apparently double i.e., with one set within another. Asci oblong, clavate, obtuse, paraphysate, 8-spored, 110-112 x 20-25 μm, with stipe 30-35 μm long. Ascospores irregularly biseriate, broad-fussoid, slightly curved, multi-(10 -15) septate & muriform, strongly constricted in the middle, the upper part broader, olive-brown measuring 50-62 x 15-20 μm. Common on dead, dry mostly decorticated limbs of oak & other deciduous tress."

Barr (1990): "Ascomata 1-2 (-3) mm long x 330-385 μm wide x 330-440 μm high; surface longitudinally striate; peridium 52-75 μm wide, to 90 μm wide at base. Asci 100-130 (-180) x 20-30 (-38) μm. Ascospores (30-) 40-65 (-80) x 10-18 μm, ellipsoid fusoid, ends acute, 7-15 septate, with 1-3 longitudinal septa, wall usually verruculose. Anamorph in culture coelomycetous or conidiogenous cells developing on surface hyphae, 5 - 8 x 1.5 μm; conidia 3-4 x 1.3-1.5 μm (Lohman, 1932, as Hysterographium vulvatum). On decorticated wood, cosmopolitan. Although Zogg included Hg. acerinumas a synonym of Hg. fraxini based upon the type description, the original collection has narrower ascospores than those of Hg. fraxini & the ascomata are longitudinally striate, characteristic of Hg. flexuosum."

Messuti & Lorenzo (2003): "Hysterothecia gregarious, closely associated, superficial, straight to flexuous, elliptical with blunt to pointed ends, longitudinally striated, 0.5 - 3.5 x 0.2 - 0.8mm; pseudoparaphyses hyaline, septate, flexuous, branched near the tips to form an epithecium; asci clavate-cylindrical, 8-spored, 100 - 122 x 20 - 40 μm; ascospores yellowish to dark brown, biseriate, with 7 - 15 transverse & 1 - 4 longitudinal septa, muriform, ellipsoid to broadly ellipsoid, constricted at the medium septum, 36 - 65 (-70) x (8-) 9 - 20 μm. Cosmopolitan. In Patagonian Nothofagus forests, Hg. flexuosum is very frequent. Collected on decorticated trunks or wood of Nothofagus alpine, N. antarctica & N. pumilio & on bark of Escallonia serrata, N. antarctica & N. dombeyi." Messuti & Lorenzo add the following as synonyms: Hysterographium magellanicum Speg., Hg. fuegianum Speg. & Hg. fuegianum f. intermedium Rehm.

van der Linde (1992): "Fruitbodies arranged in groups, not closely associated, embedded or ermpent, long, linear with tapering ends, straight, not branched, up to 2.0 x 0.4mm. Pseudoparaphyses hyaline, filiform, branched near tips to form an epithecium. Asci not seen because the material was very old. Ascospores golden to dark brown, usually constricted at median septum, 9- or 10-transverse septa & 1- to 2-longitudinal septa, measuring 52 - 57 x 17 - 20um."

Hysterographium flexuosum (Schwein.) Sacc. (from Zogg 1962, pg. 34, 40). Hg. faxini (No. 1, top) and Hg. flexuosum (No. 2, bottom).

Hysterographium minus N. Amano

N. Amano. 1983. Trans mycol Soc Japan 24: 283-297.

Amano (1983) : "Ascomata aggregated or dispersed, superficial with immersed base, elongated with acute ends, straight or curved, rarely branched, opening by a narrow longitudinal slit, black, carbonaceous 0.5 - 1.0mm long, 130 - 180 μm wide, 180 - 230 μm high. Tissues of ascomatal walls of textura angularis close to textura epidermoidea, 20 - 50 μm tich, composed of thick-walled, brown cells, 3 - 5 μm in diameter. Pseudoparaphyses filiform, branched, anastomosed, hyaline, 1.0 - 1.5 μm thick, enlarged to 2.0 - 2.4 μm in diameter at the apex, in 2% KOH staining greenish white. Asci bitunicate, broadly clavate, stipitate, 8-spored, in 2% KOH staining pale green or greenish white, staining more intensely above, 80 - 105 x 23 - 34 μm. Ascospores irregularly biseriate, ellipsoid, with 6 - 13 transverse septa & 1 - 3 longitudinal septa, slightly constricted at the transverse septa, straight or curved, 26 - 38 x 10 - 15 μm. On decorticated branch of broad-leaved tree. Japan. H. minus resembles H. fraxini but differs in size of ascospores. Taxonomic significance of color reaction of asci & pseudoparaphyses in 2% KOH is not known. It has not been reported before for hysteriaceous fungi."

Hysterographium minus N. Amano. From Amano (1983), pg. 294.

Hysterographium spinicolum Doidge

Doidge. 1924. Bothalia 1: 195-221.

Described by Doidge from South Africa in 1924 from collections made from the thorns of an Acacia sp. Recollected by van der Linde.

van der Linde (1992): "Fruitbodies scattered or in small groups, not closely associated, superficial, long elliptic, straight, not branched, slit showing brick-red epithecium, up to 1.2 x 0.36mm. Pseudoparaphyses hyaline, filiform, septate, brownish & thickened apically, branched to form an epithecium. Asci irregularly biseriate, nearly cylindrical, 8-spored, 135 - 145 x 13 - 17um. Ascospores dark brown, slightly constricted at median septum, 25 - 28 x 11 - 13um, which are slightly larger than the dimensions given by Doidge (1924)."