Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids

Abstract

Summary• Dust seeds that germinate by obtaining nutrients from symbiotic fungi have evolved independently in orchids and 11 other plant lineages. The fungi involved in this 'mycoheterotrophic' germination have been identified in some orchids and non-photosynthetic Ericaceae, and proved identical to mycorrhizal fungi of adult plants. We investigated a third lineage, the Pyroleae, chlorophyllous Ericaceae species whose partial mycoheterotrophy at adulthood has recently attracted much attention.• We observed experimental Pyrola asarifolia germination at four Japanese sites and investigated the germination pattern and symbiotic fungi, which we compared to mycorrhizal fungi of adult plants.• Adult P. asarifolia, like other Pyroleae, associated with diverse fungal species that were a subset of those mycorrhizal on surrounding trees. Conversely, seedlings specifically associated with a lineage of Sebacinales clade B (endophytic Basidiomycetes) revealed an intriguing evolutionary convergence with orchids, some of which also germinate with Sebacinales clade B. Congruently, seedlings clustered spatially together, but not with adults.• This unexpected transition in specificity and ecology of partners could support the developmental transition from full to partial mycoheterotrophy, but probably challenges survival and distribution during development. We discuss the physiological and ecological traits that predisposed to the repeated recruitment of Sebacinales clade B for dust seed germination.

Specificity of fungal associations of Pyroleae and Monotropa hypopitys during germination and seedling development

“…Only a few studies on the fungal associates of germinated seedlings have recently been produced (Hashimoto et al . ; Hynson et al . ).…”

“…In contrast, seedlings of Pyrola asarifolia Michx (Ericaceae) were more specific than adult plants (Hashimoto et al . ). Hynson et al .…”

Two widespread green Neottia species (Orchidaceae) show mycorrhizal preference for Sebacinales in various habitats and ontogenetic stages

“…ovata placed within an ECM clade close to Pyrola asarifolia symbionts (AB669633; Hashimoto et al . ; clade/serendipita2 in Tedersoo & Smith ), and OTUs SEB 2 to 6 and 29, frequent in N. ovata , close to an ECM symbiont of Fagus sylvatica (HQ154321; Garnica et al . ; Fig.…”

Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales)

“…These include arbutoid (Richard et al 2005;Kühdorf et al 2014), cavendishioid (Setaro et al 2006), ericoid (see below), jungermannoid (Kottke et al 2003;Newsham and Bridge 2010), orchid (e.g., Warcup and Talbot 1967;Dearnaley et al 2009;Wright et al 2010), and pyroloid (e.g., Tedersoo et al 2007;Vincenot et al 2008;Hashimoto et al 2012) mycorrhizae, as well as ectomycorrhizae (e.g., Selosse et al 2002;Urban et al 2003;Wei and Agerer 2011). Sebacinales are phylogenetically divided into two families, namely, Sebacinaceae (formerly Group or Clade A) and Serendipitaceae (Group/Clade B), which also differ in ecology (including mycorrhizal potential) and cultivability (Weiss et al 2004;Oberwinkler et al 2013;Oberwinkler et al 2014;Weiss et al 2016).…”