Jimtrappea guyanensis
Jimtrappea guyanensis T.W. Henkel, M.E. Sm. & Aime, in Smith et al., IMA Fungus 6(2): 305 (2015)
Etymology: Guyana and –ensis (Latin adj. B) = adjectival suffix indicating origin or place; referring to the country of known occurrence of the species.
Diagnosis: Reminiscent of a Tylopilus species, but lacking a stipe and with a loculate gleba. Peridium pale, delicate. Basidiospores pinkish to reddish brown, smooth, and cystidia strongly dextrinoid in Melzer’s solution.
Basidiomata subglobose to ovate and irregularly lobed, occasionally appearing fused, (6–)11–21 mm tall, (3–)8–29 mm broad, subfirm to soft and gelatinous with age; surface off-white to pale cream (4A1–4A2, 5A2) throughout, unchanging with pressure or slightly browning, with occasional humic stains, glabrous macroscopically, under hand lens a tightly appressed hyphal mat; base subtended by delicate white hyphal cords and occasionally concolourous ectomycorrhizas. Peridium in longitudinal section extremely thin (< 0.25 mm), light creamish white, single-layered, delicate, separable. Gleba nearly white (6A1) initially, with age light pink (6A2–6A3) to greyish pink (6B2–6B3), eventually variably darker pink (6C4–7C4, 7D5, 8B3–8B4), unchanging with exposure, moist, spongy, under hand lens of compact, folded locules that gelatinize with maturity; in longitudinal section columella a short basal structure 1–4 mm wide, off-white, gelatinous, opaque; upward-radiating sterile veins short (1–2 mm), less evident at maturity. Odour faintly fragrant, clay-like. Taste slightly bitter, astringent. Macrochemical reactions not obtained.
Peridium 94–200 μm thick, single-layered, of interwoven repent hyphae, these laterally branching, uninflated to inflated, 1–7 μm wide, occasionally swollen at septa, with irregular extracellular encrustations, granulose-guttulate, hyaline in KOH and H2O, interspersed with golden brown, opaque conductive hyphae; terminal cells cylindrocapitate, infrequently subventricose, or rarely cylindrical or with distinct angles, occasionally with short side branches, 7–81 μm long, 2–16 μm wide at apex, 2–7 μm centrally, 2–6 μm at base, with brownish yellow, densely granulose contents in KOH, and occasionally with globose, hyaline extracellular encrustations and swollen at the basal septum. Glebal trama hyaline, of tightly packed, parallel to slightly interwoven hyphae diverging toward hymenium; hyphae cylindrical, infrequently swollen at septa or branch points; cells 8–82 × 2–8 μm, hyaline in KOH, thin-walled, often heavily gelatinized and separating in mature specimens; contents not evident or sparsely guttulate-granulose; conductive hyphae frequent in subhymenial region, 2–7(–9) μm wide, golden-brown, opaque. Hymenium lining locules composed of a palisade of basidioles, basidia and cystidia arising from dichotomously branching subhymenial hyphae. Basidia abundant in younger specimens, increasingly rare to absent with age, subclavate to clavate, tapering evenly toward base, or rarely cylindrical, 23–50 μm long, 7–12 μm broad at apex, 6–9(–12) μm at centre, (3–)4–6 μm at base, thin-walled, hyaline in KOH and H2O, unreactive in Melzer’s solution; contents not evident or opaque granulose-guttulate; guttules refractive, variably-sized, solitary to numerous; sterigmata two, three, or four per basidium, straight, even, 1.5–2 × 1–2 μm. Basidiospores statismosporic, smooth, subfusiform to fusiform, occasionally amygdaloid, bilaterally symmetrical in all views, (13–)14–18(–20) × 6–8 μm (mean = 16.0 ± 1.6 × 6.9 ± 0.6 μm; Qr = 1.88–2.83(–3.25), Qm = 2.34 ± 0.25; n = 120), initially light pinkish brown, more reddish brown at maturity in KOH and H2O, inamyloid; sterigma detaching irregularly from basidium and leaving a pedicel (0.5–)1–3.5(–5) μm long at basidiospore base; wall 0.3–0.9 μm thick, nearly smooth under light microscopy, under SEM surface of short, irregular layers. Cystidia abundant in young specimens, less frequent with maturation, arising from lower subhymenium, not projecting above hymenial palisade, cylindrical, sublanceolate, or subventricose, rarely cylindroclavate, (30–)34–72(–88) μm long, 5–9 μm broad at apex, 6–12 μm at centre, 4–6(–8) μm at base, thin-walled, faintly grey and highly refractive in KOH and H2O, strongly dextrinoid in Melzer’s; contents initially granulose-guttulate, later a uniform, highly refractive cytoplasm, deliquescing into locules with advanced age. Clamp connections absent.
Habit, habitat, and distribution: Solitary or in small groups semi-emergent on mineral soil/humic layer interface on the forest floor, or hypogeous deeper within mineral soil, in forests on lateritic or white sand soils under Aldina insignis, Dicymbe altsonii, D. corymbosa, D. jenmanii, or Pakaraimaea dipterocarpacea; known from the Upper Potaro and Upper Mazaruni River Basins of Guyana.
Index Fungorum number: IF812360
Notes: Jimtrappea guyanensis is recognized in the field by the white peridium, unchanging tissues, pink, loculate gleba, and short columella. Micromorphologically J. guyanensis is distinguished by the smooth, subfusiform, reddish brown basidiospores and prominent dextrinoid cystidia. Smooth basidiospores are relatively rare among sequestrate Boletaceae, and the dextrinoid cystidia of J. guyanensis are unprecedented among sequestrate Boletales with smooth basidiospores (e.g. Dodge 1931, Smith & Singer 1959, Pegler et al. 1989, Pacioni & Sharp 2000, Lumyong et al. 2003, Nouhra et al. 2005, Yang et al. 2006, Desjardin et al. 2008, Moreau et al. 2011, Moreau et al. 2013, Lebel et al. 2012, Orihara et al. 2012a, b, Trappe et al. 2013, Hayward et al. 2014). In the phylogenetic analysis reported here, J. guyanensis was putatively related to the South-East Asian sequestrate Durianella echinulata, albeit without bootstrap support (Figure 1). These two species are distinct morphologically as D. echinulata is characterized by highly ornamented spores, a blue colour change upon exposure, and a rough, warted peridium (Desjardin et al. 2008). Additionally, J. guyanensis is putatively related to a cluster of Tylopilus species, including the type species of that genus (T. felleus), but without bootstrap support (Figure 1).
Jimtrappea guyanensis is micromorphologically most similar to the tropical African monotypic sequestrate genus Mackintoshia, originally described as a member of Agaricales (Pacioni & Sharp 2000), but now known to belong to Boletaceae based on ITS and 28S rDNA data (Fig. 1; Nuhn et al. 2013, Tedersoo & Smith 2013). Mackintoshia persica is characterized by prominent cystidia, smooth basidiospores, and a putative symbiotic association with ECM Caesalpinioideae (Pacioni & Sharp 2000). The subfusiform basidiospores and dextrinoid cystidia of J. guyanensis contrast with the ellipsoid basidiospores and non-dextrinoid cystidia of M. persica (Castellano et al. 2000, Pacioni & Sharp 2000). Although there is no bootstrap support for the placement of either M. persica or J. guyanensis in the phylogenetic analysis, they were resolved in highly divergent clades and on relatively long branches, suggesting no close relationship (Figure 1).
Basidiospores of the Asian and Australasian genus Rossbeevera are nearly smooth except for broad longitudinal ridges that give them a slight to distinct polar angularity that is lacking in J. guyanensis (Lebel et al. 2012, Orihara et al. 2012b). Rossbeevera species also lack cystidia and have basidiomata that turn blue with exposure (Lebel et al. 2012, Orihara et al. 2012b). Additionally, Rossbeevera is phylogenetically distant from J. guyanensis (Figure 1), resolving in a well-supported, previously recovered “leccinoid” clade with other sequestrate and non-sequestrate taxa (Nuhn et al. 2013, Wu et al. 2014). The fusoid, smooth, pedicellate basidiospores of J. guyanensis also resemble those of species of Hysterangium (Hysterangiales) which otherwise differ in having a dendroid columella, a dark greenish or brown gleba with gel-filled locules, and in lacking cystidia (Castellano et al. 1989).
Species in a few other temperate sequestrate genera of Boletales have large, fusoid, smooth basidiospores that could potentially be confused with those of J. guyanensis, but differ, in addition to lacking cystidia, in the following ways: Alpova species have gel-filled locules and are associated primarily with Alnus; Melanogaster species have a black gleba with gel-filled locules; Rhizopogon species have an olivaceous to dark brown gleba and are associated with Pinaceae; and Truncocolumella species have a greenish brown gleba, a dendroid columella, and are associated with Pinaceae hosts (Trappe et al. 2009).
Figure 1. Maximum likelihood (ML) phylogram (-ln = 57979.037507) based on RPB1, RPB2, and 28S ribosomal DNA sequences depicting phylogenetic relationships of the Boletaceae and new sequestrate Guyanese taxa (in red bold). ML bootstrap support values greater than 70 are shown above the nodes. Other sequestrate taxa are indicated in bold with solid black dots preceding their binomials. Previously identified clades with multiple species from the same higher taxon are collapsed into triangles for visual simplification as is a clade of outgroup taxa from several non-Boletaceae lineages of Boletales.
Figure 2. Basidiomata of Jimtrappea guyanensis. A. Holotype (Henkel 9163). B–C. Longitudinal sections. B. Off-white immature gleba (Henkel 9540). C. Pink mature gleba (Henkel 9689). Scale bars = 10 mm.
Figure 3. Microscopic features of Jimtrappea guyanensis (holotype; Henkel 9163). A. Basidiospores. B. Bisterigmate basidium, basidioles, and cystidium. C. Four-sterigmate basidium with developing basidiospores. D. Hymenium section showing basidia, basidiospores, and dextrinoid, subcylindrical cystidia (in Melzer’s). E. Dextrinoid, sublanceolate cystidium (in Melzer’s). F. Opaque, hyaline cystidium (in KOH). B–C, F = phase contrast. Scale bars = 10 μm.
Figure 4. Scanning electron micrographs of basidiospores of Jimtrappea guyanensis (holotype; Henkel 9163).
Key reference:
Smith, M. E., Amses, K. R., Elliott, T. F., Obase, K., Aime, M. C., & Henkel, T. W. 2015. New sequestrate fungi from Guyana: Jimtrappea guyanensis gen. sp. nov., Castellanea pakaraimophila gen. sp. nov., and Costatisporus cyanescens gen. sp. nov. (Boletaceae, Boletales). IMA fungus, 6(2), 297–317.
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