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Why do harmless, wood-decay Mycena fungi suddenly invade live plant roots?

Annual Review Article 2020

The project involves growing trials with trees and Mycena fungi to attempt to determine the genetic reasons why fungi become either parasites/”blind passengers” on plants or their beneficial partners.

By Christoffer Bugge Harder, postdoctoral fellow, PhD, Lund University

Nitrous bonnet (M. leptocephala) Photo: Thomas Kehlet

Fungi are of major importance for plants and humans. Whereas plants, as is well known, are themselves able to make the carbohydrates essential for their lives through photosynthesis, fungi – like animals – need to procure them from other organisms. 

Most fungi get their carbohydrates from plants, and broadly speaking they have two different life strategies (ecologies) for doing so: they can live as decayers (saprotrophs) of dead wood and litter; or they can get what they need directly from living plants. 

In the latter case, they can then choose to live either in mutually beneficial symbiosis with those plants (as mycorrhizae formers), providing them with other nutrients, such as nitrogen and phosphorus, “in exchange for” the carbohydrates they need, or as parasites that simply feed off their host.

Mycena fungi, especially the Arctic species, have proven to have the largest genomes of any that are known from macroscopic fungi (mushrooms and toadstools)

The saprotrophic fungi have developed an enormous arsenal of enzymes for decaying the highly complex carbohydrates (lignin and cellulose) that make up trees. 

Furthermore, most of the world’s plants have their specific fungal parasites, and around 95% of them enter into a form of symbiosis with mycorrhizal fungi in which the fungus’s extended cells (hyphae) grow into the plant’s roots in various ways. 

Brownedge bonnet (M. olivaceomarginata) Photo: Thomas Kehlet

The ability to form mycorrhizae is known only from fungi.

But where other ”unique” characteristics (for example, being able, as some plants do, to fix nitrogen from the atmosphere) have usually arisen only once or a few times in the history of life, saprotrophic fungi have developed the ability to enter into symbiosis with trees at least 78 known times, independently of one another, in the fungal world in the period from 100 million to 20 million years ago. 

This suggests that fungi can ”change ecology” quite easily, and that symbiosis can occur with relatively few genetic modifications. 

The problem, however, is that species that have been separate from each other for 20-100 million years will always have a large number of other genetic differences in addition to those that have anything to do with any differences in their ecology.

The Kobbe inlet in South West Greenland (south of Nuuk) where a large number of fungi was collected last autumn, to be used for genome sequencing. Photo: Christoffer Bugge Harder

Are Mycena fungi in the middle of the process of ”learning” to enter into symbiosis with plants?

Lilac bonnet (Mycena pura) Photo: Arne Aronsen

This is where Mycena fungi are interesting to study. Traditionally, it was believed that they were all saprotrophic, but it turns out they excel at invading plant roots – especially birch trees, as well as Arctic herbs and shrubs. 

A recently published article described laboratory trials showing that the lilac bonnet species was able to transfer phosphorus to birch trees, and that different strains within one and the same species of other Mycena fungi exerted a widely varying effect on the birch host: some clearly harmed their host plant, others were ”blind passengers” with no obvious negative or positive influence, and yet others were beneficial for the birch’s growth. 

This suggests that the evolution of Mycena fungi is ”in full swing”, so to speak, which means we do not need to go back 20-100 million years to find a point in time where symbiontic fungi separated from saprotrophic fungi.

Growing trials in the laboratory – and an Arctic link in the open air?

Fig. 1 Radiographs (X-rays, A,C) and photographs (B,D) of silver birch (Betula pendula) germinated and inoculated with lilac bonnet (Mycena pura) for seven weeks. The dark areas on the radiographs (A,C) show how the fungus has transferred radioactive phosphorus (32P) to the birch plant. From Thoen et al., In vitro evidence of root colonization suggests ecological versatility in the genus Mycena.
New Phytologist 2020, DOI: 10.1111/nph.16545

My project’s methods consist of growing birch plants together with different species/strains of Mycena fungi with known traits (harmful, ”blind passengers” or beneficial). 

I then extract RNA (material from the genes that are expressed) from fungi and plants, read (sequence) it, and compare it with the DNA from the genomes of Mycena fungi that I already know. 

The idea is to identify the few crucial genetic differences that describe how Mycena fungi that are closely related still have different ecologies. 

Additionally, on a collecting expedition to Greenland I was able to obtain various fungal cultures, which I am using to obtain more genomes from arctic Mycena fungi and their close relatives. 

Mycena fungi, especially the Arctic species, have proven to have the largest genomes of any that are known from macroscopic fungi (mushrooms and toadstools) – three to ten times larger than all other known genomes. 

One theory is that adaptation to harsh environments such as the Arctic is causing fungi to ”experiment” more with their genes/genomes and seek out new ecological niches, and by comparing the genomes 1:1 with those from the same species found in more temperate regions, it is possible in the same way to identify the crucial few genetic differences.

Around 60% of all enzymes that human beings exploit commercially derive originally from fungi, while, on the other hand, parasitic fungi cause the loss of one seventh of the world’s total crop yield

Fig. 2 The three main ways of life (ecologies) for fungi in relation to plants. Decayers get all their nutrition by decaying dead plants; parasites suck (primarily) carbon from live plants for their own benefit, harming the plant in the process; and symbionts take carbon from the plant, which receives nitrogen and phosphorus “in exchange”, with mutual benefits for both parties. Note that fungi are also found as “blind passengers” (see text for further explanation), penetrating a plant root and surviving without obviously harming or benefiting it.
Fig.: Christoffer Bugge Harder Design: Kontrapunkt

Perspectives

Fungi and their live host plants have influenced each other’s development, and the saprotrophic fungi also play a very big role in the conversion of carbon in dead plant matter in the world’s ecosystems. 

The traits of these fungi are also of major economic importance for humankind: around 60% of all enzymes that human beings exploit commercially derive originally from fungi, while, on the other hand, parasitic fungi cause the loss of one seventh of the world’s total crop yield. 

If we can identify just a few genetic modifications that are able to cause dramatic differences in whether a fungus harms or benefits its plant host, it would be of considerable general interest to society.