Variation with and without sex in mycorrhizal fungi

Abstract

Most land plants acquire a substantial part of their mineral nutrients through a symbiosis with mycorrhizal fungi. The major groups of mycorrhiza differ both in their morphology, the types of integration between fungus and plant, their evolutionary history and the packaging of their genetic material (Smith and Read 1996). Arbuscular mychorrhizal fungi (AMF) form an endosymbiosis with tree-shaped structures in host root cells called arbuscles that are responsible for most of the exchange of assimilates and nutrients. Most grasses, many herbal plants and shrubs as well as most tropical trees form AM. The great majority (>95%) of fine roots of boreal forest are ectomycorrhizal (Taylor et al. 2000) and nutrient absorption is primarily via the fungus. In her paper to Oikos, Kytoviita (2000) refers to an overview of the frequency of sex among symbiotic organisms by Law and Lewis (1983), where they make a differentiation between endosymbionts and ectosymbionts. Endosymbionts should experience a more predictive environment inside the host plant and therefore less adaptive value in pursuing sex and recombination. The conclusion from Law and Lewis (1983) that selective forces suppress sex in Frankia, Rhizobium and cyanobacteria is partly related to the fact that they lack meiosis, although conjugation, the equivalent of sex in the protista, does occur. The example of Chlorella algae does not hold for scrutiny since both species that do and do not exhibit a endophytic life style are asexual. Ectomycorrhizal fungi (EMF) are capable of going through mating and meiosis. However, the comparison between EMF and their basidiomycetous relatives among saprotrophs and pathogens shows no obvious difference in the frequencies of sexual and asexual species among these groups. The only group that really meets the reduced sex in endosymbiont hypothesis are the AMF. Ectomycorrhizal relatives in the genus Endogonae are reported to exhibit sexual life cycles, the conclusion being that a endosymbiotic mycorrhizal lifestyle with relative little contact with a hostile soil environment would favour asexuality and an ectomycorrhizal lifestyle with a more substantial part of the mycelium outside the actual fine roots would not. To make the comparison, it is interesting to note that plant parasitic fungi do not always engage themselves in producing genetically variable offspring. In fact, clonality or asexual populations is a very common life-history trait among many saprotrophic and pathogenic fungal species as well as in mycorrhizal fungi; EMF are known to produce asexual chlamydospores. Examples of clonal propagation are asexual spores, e.g the rust spores of rust fungi or conidia of the form genus Fusarium, or budding yeast cells (for review see Brown 1999). Most plant pathogenic species proliferate through vegetative growth, which may continue for many centuries and result in large territorial clones (Smith et al. 1992, Anderson and Kohn, 1995). In fact, the proper question to ask is why is asexual reproduction is so common in fungi? Two features of the fungal mycelium may help to understand this: (1) In heterokaryotic fungal species, deleterious mutations can be complemented by a fully functional allele in another nucleus. This would slow down erosion of asexual genomes. (2) In animals and higher plants where reproduction is confined to reproductive tissue, mutations in the somatic tissue will normally be irrelevant for generating variation in subsequent generations. By contrast, each fungal nucleus is capable of founding a new mycelium. Mutation in the mitotic phase is therefore a powerful way to generate variation in a fungal population. Kytdviita puts forward the thesis that AMF, in lacking sexual structures and known sexual reproduction, also should be highly uniform in the genetic material.