Nano Interventions: Fungi as Farmers, Plants as Mushroom Hunters- mycorrhizal evolution and its relationship to plants

This is the first part of a multi-part series that will discuss mycorrhizae and their importance to all living beings, specifically for landscape design and ecological restoration applications. This first discussion was written more than 10 years ago by me for an Evolutionary Biology class at Appalachian State University under the mentorship of Dr. Zack Murrell, but nonetheless introduces mycorrhizae as possibly the shepherd of phototrophs to land more than 350-450 million years ago.

Photo courtesy of www.mberg.com.auimagesmycorrhiza.png

A conditional “friendship” between plants and fungi (mycorrhizae) has received a lot of attention recently (note: this was written 10 years ago!) for its application in sustainable agriculture and habitat restoration, along with the fact that this relationship gives us an indirect view into the window of plant’s colonization of land. There is no debate that mycorrhizae benefit plants, however, there is some debate over how mycorrhizae evolved. The debate lies in whether fungal associations with plants evolved and are evolving simply in parallel to plants due to similar adaptive necessities such as similar environmental pressures or if mycorrhizae and plants coevolved with reciprocal gene-for-gene changes (Cairney 2000).

Introduction

Mycorrhizae literally translates to “fungus-root.” This mutualism between plant and fungus involves a fungus colonizing the cortical tissue of a plant's roots. The fungus benefits the plant host because it helps the plant indirectly absorb nutrients. For example, mycorrhizae can break down molecules into elemental forms that otherwise  are unusable by plants, such as phosphorus. In addition, mycorrhizae can benefit plants by providing protection from pathogens and also offer the plant assistance in retrieving water. In return, the fungus gets carbohydrates, a necessary compound for metabolism, from the plant which is produced through photosynthesis (Cairney 2000).

This mutualism with fungi was essential for phototrophs to come onto land and proliferate (Pirozynski and Malloch 1975). One other example of fungi as "farmers" and plants as "mushroom hunters" aside from mycorrhizae can be demonstrated in lichens (fungi and cyanobacteria or green algae associations), which can withstand harsh environments because of their symbiosis and maintain permanent relations (Hawksworth 1988). Similarly, mycorrhizae helped plants conquer the terrestrial environment and are responsible for not only the diversity of plants today, but also that of fauna, due to their dependence on plants (Simon et al. 1993).

White Pine seedlings grown in sterile conditions (left),
White Pine seedlings grown in forest soil with mychorrhizae.
 Photo courtesy of www.msu.educourseisb202

About 90% of extant land plants form symbioses with fungi (Cairney 2000). In phototrophs that have secondarily reverted back to the aquatic environment, their ability to form relationships with fungi is lost, providing more evidence that phototrophs evolved onto land with the aid of fungal associations (Pirozynski and Malloch 1988). Today, Atlantic white cedar fluctuate their levels of mycorrhizal "infection" during drought and flooding (Cantelmo and Ehrenfeld 1999), which indicate how plants regulate their fungal needs and also may be reminiscent of the first plant’s journey to land. Also, plants that do not form mycorrhizal relations are mostly in highly disturbed habitats or in wet or aquatic habitats where mineral resources are adequate and the diffusion of oxygen prohibits the growth of fungi (Fitter and Peat 1993). Even algae living in tidal zones form mycophycobiosis during low tides to cope with the desiccating stress (Kohlmeyer and Kohlmeyer 1979). Lastly, fossil evidence agrees with molecular data in that arbuscular mycorrhizae form a monopyletic group and arose around 353-462 million years ago, around the same time plants colonized land (Redecker et al 2000).

Arbuscular mycorrhizae.

Photo courtesy of terroirists.nettagmicrobiology

Types of Mycorrhizae


Arbuscular mycorrhizae (AM) are mychorrhizae that actually penetrate the plant's cortical tissue and are the most numerous type of mycorrhizae in present-day plants. However, AM consists of only 130 species (Morton 1990) and shows generality to plant hosts (Perry 1998). AM’s include fungi in the phylum Zygomycota, more specifically the order Glomales, and the plant hosts include most angiosperms, some gymnosperms, Pteridophytes and various lower plants (Smith and Read 1997). These AM associations occur mostly at mid-latitudes where phosphorus for plant consumption is limited (Read 1991). Fossil and molecular evidence significantly indicate that the ancestors of extant plants formed AM relationships (Cairn 2000) and today’s plants who do not have AM have lost their relationship with their ancestral host plant (Barker et al. 1998). Gehrig et al. (1996) have found a fungus endocytobiont, Geosiphon pyriforme, to be related to an ancestral form of Glomales, thus forming a monophyletic group, and is probably most like the Glomus fungi that first aided plants to adapt to land life. In addition, molecular clock analysis suggests that the phylogenetic radiation of ancient Glomales paralleled the colonization of land (Redecker et al 2000).

Ectomycorrhizae.
Photo courtesy of farm3.static.flickr.com

Another type of mychorrhizae, Ectomycorrhizae (ECM), form a sheath around the outside of the root of the plant and are only on woody trees and shrubs (Cairney 2000). ECM fungi permit their host to acquire phosphorus, nitrogen and organic material (Read 1991). ECM have a great importance in shaping the ecosystems of forests and involve fungi that belong to the phylums Basidiomycota, Ascomycota and Zygomycota (Cairney 2000). Interestingly, however, ECM extant plants can also form AM associations, depending on the soil conditions (Smith and Read 1997). In addition, some ECM capable plants only form AM associations at the seedling stage, providing even more evidence that all land plants that exist at the present evolved from an ancestral AM condition (Cairney 2000).

Ericoid mycorrhizae (ERM) occur in extremely nutrient poor soils and at high latitudes and altitudes (Read 1991). The fungi in this association have extensive coils of hyphae that cover the epidermal cells of the plant host and involve specifically Ericad plants (the Heather family) and Ascomycete fungi (Cairney 2000). ERM’s have good saprotrophic abilities permitting them to provide nitrogen and phosphorus and tolerate toxic cations that are in acidic soils (Smith and Read 1997).

Photo courtesy of the botany department at WVU

Conclusion


Coevolution is the reciprocal genetic change among a species or populations (Thompson 1999), while parallel evolution is the result of similar pressures acting on species and results in similar yet independent outcomes. Which evolutionary process acted on plants and fungi in mychorrizal associations? Currently evidence for pure coevolution is lacking (Cairney 2000). However, Juenger and Bergelson (1998) propose that the coevolution is more “diffuse” and at a “guild” level of selection. Cairney (2000) has looked at this very question in his paper, The Evolution of Mycorrhiza Systems. He believes that coevolution did occur, but he sees no evidence that gene-for-gene coevolution is occurring in extant species and that it is simply parallel evolution at the present day.

Despite the lack of direct evidence that coevolution is occurring today in mycorrhizae, I think that coevolution is indeed occurring today. If coevolution were a continuum, then I would suggest the exant fungal and plant species are to a lesser degree coevolving because I believe there is some gene-for-gene reciprocation. Mycorrhizal associations can help a plant survive and reproduce, excluding certain genomes that cannot fully exploit this symbiosis. Generalities occur in fungal associations because of common ancestral lineages and does not infer that parallel evolution is occurring. It is exhibited that in certain environmental conditions certain mycorrhizal associations take place, which could support parallel evolution. Perhaps it is not, since a basis for the two organisms to come together in symbiosis must have been established at some point to permit the relationship. I suggest that mycorrhizal associations are still coevolving, to a degree, in which genetic give and take must take place. It is important when creating fungal phylogenies of those that form mycorrhizae to include plant hosts and vice versa, for mycorrhizae associations were and are the essential associations for plants to survive. 


With the current prevalence and severity of habitat destruction and the overpopulation that permits limited resources, soil structure will never be perfect everywhere on Earth. However, for native plants and ecosystems to become or remain healthy and supporting, mycorrhizae are and will be the mechanism of survival for all life forms. In the future, man will foresee and artificially create these associations for habitat restoration and crop production and this application will be an important factor that will enable humans to feed one another and rebuild plundered ecosystems.

Barker, S.J. Tagu, D. Delp, G. 1998. Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol. 116: 1201-1207

Cairney, J.W.G. 2000. “Evolution of mycorrhiza systems.” Natuwissenschaaften. 87:467-475

Cantelmo, A.J. and Ehrenfeld, J.G. 1999. Effects of microtopography on mycorrhizal infection in Atlantic white cedar pine. Mycorrhiza. 8: 175-180

Fitter, A.H. and Peat, H.J. The distribution of arbuscular mycorrhizas in the British flora. New Phytol. 125, 845-854     

Fitter, A.H. and Moyerson, B. 1996. Evolutionary trends in root-microbe symbioses. Phil Trans R Soc Lond B. 351:1367-1375

Gehrig, H. Schubler, A. Kluge, M. 1996. Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc, is an ancestral member of Glomales: evidence by SSU rRNA analysis. J Mol Evol. 43: 71-81

Hawksworth, D.I. 1988. Coevolution of fungi with algae and cyanobacteria in lichen symbioses. Coevolution of Fungi with Plants and Animals. Academic Press. 125-148

Heijden, M.G.A. van der. Boller T. Wiemken A. Sanders I.R. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology. 79: 2082-2091.

Juenger, T. Bergelson, J.1998. Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution. 52: 1583-1592

Kohlmeyer, E. and Kohlmeyer J. 1979. Marine Mycology: the Higher Fungi, Academic Press

Morton, J.B. Benny, G.L. 1990. Revised classification of arbuscular mycorrhizal fungi. Mycotaxon. 37:471-492

Perry, David. 1998. A movable feast: the evolution of resource sharing in plant-fungus communities.Trends in Ecology and Evolution. Vol.13, issue 11: 432-434

Pirozynski, KA and Malloch, DW. 1975. The origin of land plants: a matter of mycotrophism. BioSystems. 6:153-164

Read, D.J. 1991. Mycorrhizas in ecosystems. Experientia. 47:376-309

Thompson, J.N. 1999 The evolution of species interactions. Science. 284:2116-2118

Redecker, D. Kodner, R. Graham, L.E. 2000. Glomalean fungi from the Ordovician. Science. 289: 1920-1921.

Simon et al. 1993. Origin and diversification of endomycorrhizal fungi and the coincidence with vascular plants. Nature 363: 67-69

Smith M.D. and Read D.J. 1997. Mycorrhizal symbiosis. Academic Press, London

Thompson, J.N. 1999. The evolution of species interactions. Science. 284: 2116-2118.