Saprotrophic fungal mycorrhizal symbionts in achlorophyllous orchids: finding treasures among the 'molecular scraps'?

Abstract

Mycoheterotrophic plants are achlorophyllous plants that obtain carbon from their mycorrhizal fungi. They are usually considered to associate with fungi that are (1) specific of each mycoheterotrophic species and (2) mycorrhizal on surrounding green plants, which are the ultimate carbon source of the entire system. Here we review recent works revealing that some mycoheterotrophic plants are not fungal-specific, and that some mycoheterotrophic orchids associate with saprophytic fungi. A re-examination of earlier data suggests that lower specificity may be less rare than supposed in mycoheterotrophic plants. Association between mycoheterotrophic orchids and saprophytic fungi arose several times in the evolution of the two partners. We speculate that this indirectly illustrates why transition from saprotrophy to mycorrhizal status is common in fungal evolution. Moreover, some unexpected fungi occasionally encountered in plant roots should not be discounted as 'molecular scraps', since these facultatively biotrophic encounters may evolve into mycorrhizal symbionts in some other plants.

Figure 1

Wullschlaegelia aphylla, a mycoheterotrophic orchid unspecifically associated with saprotrophic Mycena and Gymnopus species. (A) Whole plant at flowering time, with reduced, tuberoid root system at that period. (B) Section of mycorrhizal root showing intracellular hyphal pelotons at early stage (p), or late stage (undergoing lysis, lp); among orchids, the colonization of dead cortical cell (cc) is a unique feature to some saprotrophic fungi (picture by A. Faccio, University of Torino).

Figure 2

A phylogeny of Psathyrellaceae (maximum likelihood) shows that several lineages were recruited as mycorrhizal symbionts of the mycoheterotrophic orchids Eulophia zollingeri and Epipogium roseum. Mycorrhizal taxa fall within a clade consisting of Psathyrella candolleana representatives, while others fall within the Coprinellus clade (sequences from references and ; the support values on branches correspond to maximum likelihood bootstrap probabilities, and only values above 70% are shown).

Figure 3

A phylogeny of Mycenaceae (maximum likelihood) shows that several lineages were recruited as mycorrhizal symbionts of the mycoheterotrophic orchids Gastrodia similis, G. confusa and Wullschlaegelia aphylla). Mycorrhizal taxa fall out among species of Mycena, while four additional isolates fall out with Mycena pura (= Prunulus purus), or in more basal positions within, or sister to, Mycenaceae (sequences from references and ; the support values on branches correspond to parsimony bootstrap/maximum likelihood bootstrap probabilities; only values above 70% are shown).