New sequestrate fungi from Guyana: Jimtrappea guyanensis gen. sp. nov., Castellanea pakaraimophila gen. sp. nov., and Costatisporus cyanescens gen. sp. nov. (Boletaceae, Boletales)

Background Armillaria is a globally distributed mushroom-forming genus composed primarily of plant pathogens. Species in this genus are prolific producers of rhizomorphs, or vegetative structures, which, when found, are often associated with infection. Because of their importance as plant pathogens, understanding the evolutionary origins of this genus and how it gained a worldwide distribution is of interest. The first gasteroid fungus with close affinities to Armillaria—Guyanagaster necrorhizus—was described from the Neotropical rainforests of Guyana. In this study, we conducted phylogenetic analyses to fully resolve the relationship of G. necrorhizus with Armillaria. Data sets containing Guyanagaster from two collecting localities, along with a global sampling of 21 Armillaria species—including newly collected specimens from Guyana and Africa—at six loci (28S, EF1α, RPB2, TUB, actin-1 and gpd) were used. Three loci—28S, EF1α and RPB2—were analyzed in a partitioned nucleotide data set to infer divergence dates and ancestral range estimations for well-supported, monophyletic lineages.ResultsThe six-locus phylogenetic analysis resolves Guyanagaster as the earliest diverging lineage in the armillarioid clade. The next lineage to diverge is that composed of species in Armillaria subgenus Desarmillaria. This subgenus is elevated to genus level to accommodate the exannulate mushroom-forming armillarioid species. The final lineage to diverge is that composed of annulate mushroom-forming armillarioid species, in what is now Armillaria sensu stricto. The molecular clock analysis and ancestral range estimation suggest the most recent common ancestor to the armillarioid lineage arose 51 million years ago in Eurasia. A new species, Guyanagaster lucianii sp. nov. from Guyana, is described.ConclusionsThe armillarioid lineage evolved in Eurasia during the height of tropical rainforest expansion about 51 million years ago, a time marked by a warm and wet global climate. Species of Guyanagaster and Desarmillaria represent extant taxa of these early diverging lineages. Desarmillaria represents an armillarioid lineage that was likely much more widespread in the past. Guyanagaster likely evolved from a gilled mushroom ancestor and could represent a highly specialized endemic in the Guiana Shield. Armillaria species represent those that evolved after the shift in climate from warm and tropical to cool and arid during the late Eocene. No species in either Desarmillaria or Guyanagaster are known to produce melanized rhizomorphs in nature, whereas almost all Armillaria species are known to produce them. The production of rhizomorphs is an adaptation to harsh environments, and could be a driver of diversification in Armillaria by conferring a competitive advantage to the species that produce them.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0877-3) contains supplementary material, which is available to authorized users.

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“…To date, gasteroid fungi have only been documented as ectomycorrhizal (ECM) or saprotrophic in their ecology (e.g. [11, 21–26]).…”

Section: Introductionmentioning

confidence: 99%

Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster

et al. 2017

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“…Like Longistriata, all three new genera are endemic to tropical South America but their macro-and microscopic characteristics are notably different. Jimtrappea guyanensis is characterized by the white peridium, unchanging tissues, short columella, smooth subfusiform, reddish brown basidiospores and prominent dextrinoid cystidia (Smith et al 2015). The white peridium, the unchanging tissues, smooth subfusiform basidiospores, and prominent cystidia of J. guyanensis contrast with the yellow peridium and unique basidiospores morphology of L. flava.…”

Section: Discussionmentioning

confidence: 97%

“…The monotypic genus Afrocastellanoa from tropical Africa (Orihara and Smith 2017) is distinct from Longistriata because it is characterized by whitish basidiomata, globose to subglobose basidiospores with warty to spiny spore ornaments and its phylogenetic relationship with the epigeous genus Porphyrellus. Recently, Smith et al (2015) (Smith et al 2015). Like Longistriata, all three new genera are endemic to tropical South America but their macro-and microscopic characteristics are notably different.…”

Section: Discussionmentioning

confidence: 99%

“…Castellanea pakaraimophila is similar to L. flava because both have subglobose basidioma and a short stipe but L. flava has a bright yellow peridium. The two species can also be easily differentiated by their spores because C. pakaraimophila has smooth, subfusiform basidiospores whereas L. flava has ellipsoid spores with distinct longitudinal striations (Smith et al 2015). Costatisporus cyanescens is easily differentiated from L. flava by its grayish yellow peridium and the dark blue staining reaction on the peridium.…”

Section: Discussionmentioning

confidence: 99%

“…The ecology of Jimtrappea, Castellanea and Costatisporus are also different from Longistriata. These three genera are apparently endemic to the Guiana Shield and are associated with the ECM tree genera Aldina, Dicymbe and Pakaraimaea (Smith et al 2015).…”

Section: Discussionmentioning

confidence: 99%

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Longistriata flava (Boletaceae, Basidiomycota) – a new monotypic sequestrate genus and species from Brazilian Atlantic Forest

Sulzbacher¹,

Orihara²,

Grebenc³

et al. 2020

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A new monotypic sequestrate genus, Longistriata is described based on collections from the Neotropical forest of Atlantic forest in Paraíba, Northeast Brazil – an area known for its high degree of endemism. The striking features of this new fungus are the hypogeous habit, the vivid yellow peridium in mature basidiomes, broadly ellipsoid basidiospores with a distinct wall that is ornamented with longitudinal striations and lageniform cystidia with rounded apices. Phylogenetic analysis, based on LSU and tef-1α regions, showed that the type species, Longistriata flava, is phylogenetically sister to the monotypic sequestrate African genus Mackintoshia in Boletaceae. Together these two species formed the earliest diverging lineage in the subfamily Zangioideae. Longistriata flava is found in nutrient-poor white sand habitats where plants in the genera Coccoloba (Polygonaceae) and Guapira (Nyctaginaceae) are the only potential ectomycorrhizal host symbionts.

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Diversity, Biogeographic Distribution, Ecology, and Ectomycorrhizal Relationships of the Edible Porcini Mushrooms (Boletus s. str., Boletaceae) Worldwide: State of the Art and an Annotated Checklist

Gelardi¹

2020

Mushrooms, Humans and Nature in a Changing World

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New sequestrate fungi from Guyana: Jimtrappea guyanensis gen. sp. nov., Castellanea pakaraimophila gen. sp. nov., and Costatisporus cyanescens gen. sp. nov. (Boletaceae, Boletales)

Cited by 32 publications

References 71 publications

Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster

Resolved phylogeny and biogeography of the root pathogen Armillaria and its gasteroid relative, Guyanagaster

Longistriata flava (Boletaceae, Basidiomycota) – a new monotypic sequestrate genus and species from Brazilian Atlantic Forest

Diversity, Biogeographic Distribution, Ecology, and Ectomycorrhizal Relationships of the Edible Porcini Mushrooms (Boletus s. str., Boletaceae) Worldwide: State of the Art and an Annotated Checklist

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