Population, habitat and genetic correlates of mycorrhizal specialization in the ‘cheating’ orchids Corallorhiza maculata and C. mertensiana

Abstract

Unlike photosynthetic plants, several distantly related nonphotosynthetic plants are highly specialized toward their mycorrhizal fungi. It is unknown whether this specialization varies geographically or is influenced by the environment. We have investigated these questions in the nonphotosynthetic orchids Corallorhiza maculata and C. mertensiana by amplifying fungal internal transcribed spacer (ITS) fragments from widespread mycorrhiza samples and then discriminating putative fungal species using ITS restriction fragment length polymorphisms (RFLPs). Three fungal species were found across 27 plants representing seven populations of C. mertensiana; 20 species were found across 104 plants and 21 populations of C. maculata. All fungi belonged to the Russulaceae, an ectomycorrhizal family. Partitioning of Simpson's diversity showed that 48% of the variance in occurrences of fungal species coincided with population boundaries in C. mertensiana, vs. 68% in C. maculata. This differentiation coincided with geography but not habitat in C. mertensiana. In contrast, likelihood ratio tests showed strong associations between fungal occurrence and both habitat and phenotype in C. maculata. For example, C. maculata populations growing under oaks had no fungi in common with nearby populations growing under conifers, and those above 2000 m had no fungi in common with those below 2000 m. However, plant genetic differentiation may underlie some of these patterns. C. mertensiana and C. maculata never shared fungal species, even when growing intermixed at the same site, demonstrating genetic control that was independent of habitat. Similarly, intermixed normal and pale-coloured variants of C. maculata had no fungal species in common. These results demonstrate fine-scale genetic influences and geographical mosaicism in a mycorrhizal interaction.

Symbiotic germination and development of the myco‐heterotrophic orchid Neottia nidus‐avis in nature and its requirement for locally distributed Sebacina spp.

“…The molecular data concerning the identities of the two N. nidus-avis fungi suggest that this orchid, similar to other MHP orchids including Cephalanthera austinae (Taylor & Bruns, 1997), Rhizanthella gardneri ( Warcup, 1985) and several Corallorhiza species (Taylor & Bruns, 1999a;McKendrick et al, 2000a), associates with a narrow taxonomic group of fungi. The finding that N. nidus-avis 1 was the predominant fungal associate of both seedlings and adults in the UK study sites agrees with a number of previous studies showing that adults and seedlings of some orchids target the same fungi (Masuhara & Katsuya, 1994;McKendrick et al, 2000a).…”

Evidence for mycorrhizal races in a cheating orchid

“…This represents high specificity relative to typical photosynthetic plants, which often associate with fungi from tens of families in both the Ascomycota and Basidiomycota (Molina et al 1992). However, across 104 C. maculata individuals, 20 different Russula species were found; hence, the association is not one-to-one at the fungal species level (Taylor & Bruns 1999). The latter study also suggested that specificity is structured within C. maculata.…”

“…DNA of plants and endogenous mycorrhizal fungi were simultaneously extracted from rhizome tissue and stored at Ϫ20°C over GeneClean glassmilk as described in Taylor & Bruns (1999).…”

Diversity and classification of mycorrhizal associations

“…Nutrient exchange in these associations is unidirectional because the plant functions as a very large sink for fungal nutrients, but cannot, or does not, provide a significant contribution to the growth or nutrition of the associated fungus (Table 2). Mycorrhizal associations where fungi do not seem to receive any benefits from plants have been called epiparasitic, myco-heterotrophic, or cheating associations (Furman & Trappe, 1971;Leake, 1994 ;Taylor & Bruns, 1999). Associations where only the plant receives substantial benefits from nutrient exchange are defined here as 'exploitative mycorrhizas'.…”