Грушанка малолистная

The mycoheterotrophic habit (i.e. probable hyperparasitism: see Björkman 1960) has arisen at least twice in Ericaceae, in Monotropoideae and Pyroloideae (Zimmer et al. 2007; Hynson et al. 2013; Lallemand et al. 2016; Tedersoo & Brundrett 2017; c.f. Cullings 1994). The relationship between fungi and Ericaceae is closest in the echlorophyllous and mycoheterotrophic Monotropoideae. Here the underground parts can be massive and the roots thick, some 200-600 µm across, often with a thick fungal mantle (already evident in germinating seedlings), a Hartig net, and fungal pegs (Imhof et al. 2013). Basidiomycetes are often the fungi involved (Bruns et al. 2002; Garbaye 2013). In Pyroloideae Pyrola aphylla is a full mycoheterotroph at times as are albino variants of P. japonica, other members of the subfamily are mixotrophic or fully heterotrophic (Hynson et al. 2009b; Selosse & Weiß 2009; Bowler et al. 2017; Matsuda et al. 2020), indeed, P. aphylla (a form of P. picta) may have small green leaves and the fungi associated with it show no particular specificity, as in other more photosynthetically conventional species of Pyrola (Hynson & Bruns 2009; Johansson et al. 2017). Both carbon and nitrogen move from the ECM fungal associate to chorophyllous Pyroloideae and echlorophyllous Monotropoideae alike (Zimmer et al. 2007; Tedersoo et al. 2007a; Matsuda et al. 2012; Johansson et al. 2015; Lallemand et al. 2016); Hynson et al. (2016) discuss nitrogen metabolism, while Kranabetter and MacKenzie (2010) noted the distinctiveness of the nitrogen metabolism in Pyroloideae when compared with that of other Ericaceae with ERM, emphasizing their probably mixotrophic nutrition. In some taxa shoots do not appear above ground every year, the phenomenon of vegetative dormancy in which mycorrhizae can play a role (Shefferson et al. 2018; Hurskainen et al. 2018). Lallemand et al. (2016) discussed the evolution of the mycoheterotrophic habit and of mixotrophy in this clade (which includes Arbutoideae) in terms of predispositions, although it was unclear what these might be.

Hashimoto et al. (2012) found that in Pyrola asarifolia from Hokkaido, Japan, non-ECM fungi (Sebacinales-Serendipitaceae: Weiß et al. 2016) were associated with the plant as it germinated, at that stage the plant-fungus relationship being rather like that between orchids and fungi; different fungi were associated with the roots of the adult plant, and these were ECM fungi also associated with Betulaceae growing in the same area. However, the duration of the subterranean, non-photosynthetic stage and other details of this early relationship are poorly known (Hynson et al. 2013; see Johansson et al. 2017 and references for some details). Pyrola japonica s.l. included more or less aphyllous and mycoheterotrophic and leafy, "normal" haplotypes (Shutoh et al. 2016), and Matsuda et al. (2020) suggested that three different forms of this species had different mycorrhizal preferences, especially for different species of Russula. Moneses uniflora showed geographical variation in the extent of partial mycoheterotrophy it showed (Hynson et al. 2015). See also Johansson et al. (2017) for discussion about Swedish taxa. Of course, mixotrophic and mycoheterotrophic species are also found in Orchidaceae (q.v. for more discussion), as are echlorophyllous seedlings.