Tuberculate ectomycorrhizae of angiosperms: The interaction between Boletus rubropunctus (Boletaceae) and Quercus species (Fagaceae) in the United States and Mexico

Abstract

Tuberculate ectomycorrhizae (TECM) are unique structures in which aggregates of ectomycorrhizal roots are encased in a covering of fungal hyphae. The function of TECM is unknown, but they probably enhance the nitrogen nutrition and disease resistance of host plants. Trees in the Pinaceae form TECM with species of Rhizopogon and Suillus (Suillineae, Boletales). Similar tubercules are found with diverse angiosperms, but their mycobionts have not been phylogenetically characterized. We collected TECM in Mexico and the USA that were similar to TECM in previous reports. We describe these TECM and identify both the plant and fungal symbionts. Plant DNA confirms that TECM hosts are Quercus species. ITS sequences from tubercules and sclerotia (hyphal aggregations that serve as survival structures) matched sporocarps of Boletus rubropunctus. Phylogenetic analyses confirm that this fungus belongs to the suborder Boletineae (Boletales). This is the first published report of TECM formation in the Boletineae and of sclerotia formation by a Boletus species. Our data suggest that the TECM morphology is an adaptive feature that has evolved separately in two suborders of Boletales (Suillineae and Boletineae) and that TECM formation is controlled by the mycobiont because TECM are found on distantly related angiosperm and gymnosperm host plants.

Boletus rubricitrinus belongs in Pulchroboletus (Boletaceae).

“…S e q u e n c e a l i g n m e n t , d a t a s e t a s s e m b l y, a n d p h y l o g e n e t i c a n a l y s i s. Sequences obtained in this study were run using the BLASTn algorithm (Boratyn et al 2013) to identify related sequences. These sequences were combined with sequences from the literature (Morris et al 2008, Smith & Pfister 2009, Gelardi et al 2014, Frank et al 2017 for phylogenetic analysis (Tab. 1).…”

“…The sequence FM999554.1 was from an uncultured environmental sample from a beech-maple forest in Ohio, USA (Burke et al 2009). The sequence FJ480444.1 was from a bright orange sclerotium collected in Massachusetts, found near the sclerotia of a Boletus rubropunctus Peck specimen (Smith & Pfister 2009); Smith and Pfister postulated that despite being present in ancestral bolete lineages, sclerotium growth was lost by many taxa in the Boletales, and has resurfaced as a convergent trait in the suborders Boletineae and Suillineae. This indicates the first-known sclerotium-forming species in the Hypoboletus group.…”

Fungal Planet description sheets: 951–1041

“…However, sequences of these taxa were < 91 % similar across the ITS. ITS sequences provide important insight into the ecology of this new species because they match a sequence from orange sclerotia collected beneath oaks in Massachusetts (Smith & Pfister 2009). Sclerotia of ecto mycorrhizal fungi are rarely reported in the literature (Smith et al 2015) but several other species of ectomycorrhizal Boletales have been shown to form sclerotia, including B. rubropunctus (Smith & Pfister 2009) and Leccinum holopus (Müller & Agerer 1990).…”

Bolete diversity in two relict forests of the Mexican beech (Fagus grandifolia var. mexicana; Fagaceae)

“…Although a significant proportion of ectomycorrhizal fungi might exhibit host specificity (Newton and Haigh, 1998; Ishida et al, 2007), fortunately from a conservation perspective, several of the bolete species that we report in this study have other hosts in addition to the Mexican beech. Boletus rubropunctus —the most abundant species—has been thoroughly studied in several Quercus hosts (Smith and Pfister, 2009). Boletellus betula, B. miniato‐olivaceus, B. russellii, Strobilomyces confusus, Tylopilus eximium, T. felleus, Leccinum rugosiceps, Retiboletus retipes , and Pulveroboletus ravenelii have been found in temperate subhumid forests of Hidalgo, where Pinus, Quercus , and Alnus are the dominant tree genera (Rodríguez‐Ramírez, 2007).…”

“…In this paper, we focus on the species diversity and composition of the bolete (Basidiomycetes: Boletales) ensemble growing in two monodominant Mexican beech forests in the state of Hidalgo, central Mexico. Given that most boletes are obligate ectomycorrhizal symbionts, their biogeographical distribution depends on that of their host plants (Ortíz‐Santana et al, 2007; Halling et al, 2008; Smith and Pfister, 2009). As symbionts in forest ecosystems, boletes are intimately involved in basic processes such as nutrient uptake and cycling, and the decomposition of organic matter.…”