Myco-heterotrophy: when fungi host plants

Abstract

Background: Myco-heterotrophic plants are partly or entirely non-photosynthetic plants that obtain energy and nutrients from fungi. These plants form a symbiosis with arbuscular mycorrhizal, ectomycorrhizal or saprotrophic fungi to meet their nutrient demands.

Scope: This Botanical Briefing summarizes current knowledge about myco-heterotrophy, discusses its controversial aspects and highlights future directions for research.

Conclusions: Considerable recent progress has been made in terms of understanding the evolutionary history, germination and nutrition of myco-heterotrophic plants. Myco-heterotrophic plants: (1) are diverse and often ancient lineages that have coevolved with fungi, (2) often demonstrate unusually high specificity towards fungi during germination and maturity, and (3) can either cheat common mycorrhizal networks supported by neighbouring photosynthetic plants to satisfy all or part of their energetic and nutritional needs, or recruit free-living saprotrophic fungi into novel mycorrhizal symbioses. However, several fundamental aspects of myco-heterotrophy remain controversial or unknown, such as symbiotic costs and physiology.

Fig. 1

Examples of myco-heterotrophic and partially myco-heterotrophic plants from different angiosperm families: (A) Pterospora andromedea, (B) Sarcodes sanguinea (both Pterosporeae; Monotropoideae; Ericaceae), (C) Voyria clavata (Gentianaceae), (D) Cephalanthera damasonium (Orchidaceae), (E) Kupea martinetugei (Triuridaceae), and (F) Afrothismia hydra (Thismiaceae).

Fig. 2

A model for the evolution of myco-heterotrophic plants in which speciation of plant lineages and simultaneous specialization of plants to fungi leads to phylogenetic tracking (Merckx and Bidartondo, 2008). (A) A community of generalist mycorrhizal mutualists. Black squares represent mycorrhizal plants in two distant lineages, ((a,b),c) and (w,x). Circles represent mycorrhizal fungi in two distant lineages, ((1,2),3) and ((9,8),7). For instance, 1 and 2 are sister taxa and their closest relative is 3. All plants must be linked to fungi and all fungi must be linked to plants. Double-ended arrows show mutualistic mycorrhizal links where plants provide carbon to fungi and fungi provide mineral nutrients to plants. (B) A mycorrhizal community where plant species x (grey) has lost the ability to photosynthesize so it cannot provide carbon to fungi thereby breaking down the mycorrhizal mutualism. Myco-heterotrophic plants depend on fungi that link them to photosynthetic plants. Single-ended dashed arrows show non-mutualistic mycorrhizal links where fungi provide carbon to plants. Myco-heterotrophic plants have a reduced mycorrhizal range and only associate with related fungi 1, 2 and 3. (C) Speciation of the non-photosynthetic plant lineage x into x′ and x′' leads to further specialixation on fungal lineages; x′ depends on fungus 3 and x′ depends on fungi 1 and 2. The fungi and the photosynthetic plants remain generalist mycorrhizal mutualists. (D) Speciation of plant lineage x′' into y and z. Plant y specializes on fungal host 2 and plant z specializes on closely related fungal host 1. This form of phylogenetic tracking by myco-heterotrophic plants towards pre-existing fungal lineages produces an evolutionary pattern of delayed co-speciation.

Fig. 3

Mean δ¹⁵N and δ¹³C values (± s.d.) in leaf tissue of autotrophic, partially myco-heterotrophic and fully myco-heterotrophic plants, as indicated, from two different sites: a beech forest in Germany and a bamboo forest in Japan. Data consolidated from Gebauer and Meyer (2003), Zimmer et al. (2007, 2008) and Ogura-Tsujita et al. (2009). Fully myco-heterotrophic plants are significantly enriched in ¹⁵N and ¹³C compared with autotrophic plants at both sites. The green orchid Cephalanthera damasonium shows similar but slightly less pronounced enrichments in ¹⁵N and ¹³C. At the Bavarian site, Orthilia secunda (Ericaceae) is significantly enriched in ¹⁵N, but not in ¹³C, compared with autotrophic plants. However, at sites where ground-level irradiance is low, a significant myco-heterotrophic gain of ¹³C was detected for this species (Zimmer et al., 2008). Abbreviations: A.pl., Acer platanoides (n = 5); A.ps., Acer pseudoplatanus (n = 9); C.d., Cephalanthera damasonium (n = 5); C.m., Convallaria majalis (n = 12); F.s., Fagus sylvatica (n = 14); G.c., Gastrodia confusa (n = 5); G.p., Gynostemma pentaphyllum (n = 4); M.h., Monotropa hypopitys (n = 4); M.n., Melica nutans (n = 5); N.n., Neottia nidus-avis (n = 14); O.s., Orthilia secunda (n = 5); P.k., Piper kadsura (n = 5); S.a., Sorbus aucuparia (n = 7); T.a., Thelypteris acuminata (n = 5).