By Joss Kirk

Fungi are generally cryptic organisms, inhabiting diverse climatic and ecological niches, usually at the microscopic level. Fungi are eukaryotic and heterotrophic like animals, but as a group are able to digest and acquire food from a much larger range of substances, with many secreting an array of digestive enzymes into their environment that can act on tough organic compounds such as lignin and cellulose, and in some cases even minerals (see Figure 1)(Hand 2016).

Figure 1 – A 125 micrometre etching in the mineral lizardite produced by the fungus Talaromyces flavus (Teng, 2016). The fungus produced this etching to harvest iron from the rock, thereby decomposing the rock and harvesting iron in a way that makes it more bioavailable for the rest of the ecosystem. Fungi are one of the most important primary decomposers of both minerals and organic matter.

Due to their inconspicuous nature, the massive extent and importance of fungi is often understated, much like other microorganisms. Indeed, the most recognizable forms of fungi are their macroscopic fruiting forms such as molds and mushrooms, despite these structures just being a small part of the life cycle of only some fungi. Mushrooms themselves are valued as a food source, while yeast and other fungi play an indirect role in food through processes such as leavening and fermentation. The greatest contribution fungi make to our food, however, is through their critical contribution to natural and human-modified ecosystems. This can take many forms, with fungi being actively involved in decomposition and nutrient cycling, both of which will be discussed in this report.

Fungi account for a significant proportion of the biomass of most ecosystems, and some fungal organisms such as lichen (a composite organism of cyanobacteria and fungi) are so prolific that they have been estimated to dominate 6% of the earth’s land surface (Haas and Purvis 2006). One of the most fascinating and vital roles fungi fill in ecosystems, and one that horticulturalists can facilitate and benefit from, is a subterranean symbiosis between fungi and plants known as a mycorrhizal association.

Mycorrhizal associations

Mycorrhizal associations or mycorrhizae are symbiotic associations between a plant and a fungus. They occur in the root zone, with the suffix ‘rhizal’ deriving from the term rhizosphere, which refers to the narrow region of soil surrounding a root that is acted upon by the root’s secretions and associated microorganisms, such as Rhizobia bacteria or, in this case, mycorrhizal fungi. Although the association can be pathogenic, it is usually mutualistic (Johnson et al 2008) and in effect extends a plant’s rhizosphere beyond its normally narrow range. A key structure of fungi of relevance to this association is the mycelium. The mycelium is the main vegetative structure of many fungi and is composed of thread-like structures called hyphae. The hyphae (see Figure 2) form a key part of many fungi’s anatomy, allowing for vegetative growth, feeding, and vegetative reproduction.

Figure 2 – The hyphae of a mold can be seen in this image forming the network of vegetative tissue known as mycelium (Blaylock 2010).

With the exception of some families such as the Brassicaceae and Chenopodiaceae (which cannot form mycorrhizal associations) mycorrhizae are beneficial to many plants or even necessary for their survival. It is an ancient association, with mycorrhizal fungi having been shown to have associated with land plants as early as 400 million years ago (Remy et al 1994). Some fungi have genus specific associations, while others, such as the Amanita, are able to form associations with many different plants (Bakker 2004). The plant hosts, on the other hand, generally partner with multiple fungi (Saari 2005). Although there are many forms of mycorrhizae, the most common are endomycorrhizae (composed primarily of and synonymous with arbuscular mycorrhizae) which are present in 70% to 85% of plant species (Wang and Qiu 2006, Andre et al 2015), including wheat and rice, and ectomycorrhizae, which are present in around 10% of plant families, most commonly woody plants such as eucalypts, oaks and pines (Wang and Qiu 2006).

Arbuscular fungi have hyphae which penetrate cortical plant cells by invaginating the cell membrane (see Figure 3). They tend to be generalists, with one given mycelial network of arbuscular mycorrhizal fungi often associating with numerous plants of various species or even genera. Because of this property, these fungi effectively connect the plants of an ecosystem together. Additionally, they produce a chemical called glomalin which, along with humic acid, is an important component of soil organic matter. Glomalin increases soil quality by improving aggregate water stability and decreasing soil erosion (Rillig 2004). Glomalin is also a significant store of soil carbon, and may be useful for carbon sequestration, but it should be noted that mycorrhizal fungi also actively decompose soil carbon, so their usefulness for sequestration is not yet fully understood (Talbot et al 2008). Because of these useful properties and their generalist nature, arbuscular fungi are often cultivated for addition to soil (McCoy 2018).

Figure 3 – Arbuscular fungus hyphae invaginate the cell membrane of cortical cells in two main ways, with either vesicles (left) or with arbuscules (right). Note that the arbuscule is tree-like in form, hence the prefix ‘arb’, referring to tree (Brundrett et al 1996).

Ectomycorrhizal fungi, the main other type of mycorrhizal fungi, cover the root tip with a structure called a mantle (or hyphal sheaf) and access the root’s epidermal and cortical cells with a structure called a Hartig net (see Figure 4). However, ectomycorrhizal fungi occasionally penetrate plant cells to form an ectendomycorrhizal association. Because they form complex multi-species relationships they are difficult to produce commercially and are not commonly cultivated (McCoy 2018). Despite this, they shouldn’t be neglected by horticulturalists when considering the valuable role mycelium plays in the soil, especially due to the extensive network they form within the soil and leaf litter. This network, known as the ectomycorrhizal extramatrical mycelium, has been shown to conduct nutrients throughout the soil system. For example, succession in ecosystems from Paper Birch trees to Douglas Fir trees has been shown to be facilitated by the movement of carbon between the trees by the ectomycorrhizal network (Simard et al 1997). This symbiotic relationship has extended as far as predation, with the ectomycorrhizal fungus Laccaria bicolor having been shown to lure and kill springtails, a source of nitrogen which is consumed by the fungi but also transferred to the plant. Some plant species such as the Easter White Pine have been shown to derive up to a quarter of their nitrogen from this source (Klironomos and Hart 2001).

Figure 4 – Ectomycorrhizal fungi use both mantles (left) and Hartig nets (right) to envelope the cortical cells of roots, especially the root tips (Atrebe 2013).

How do mycorrhizae benefit plants?

Mycorrhizae are prolific and even vital in many ecosystems, but what benefits do they actually provide to plants? The main component of the mutualism between fungi and plants is in their sugar-water-mineral exchange. The fungi derive from the plant a relatively constant source of important carbohydrates like glucose and sucrose, to which the fungi would otherwise have much more limited access in the soil environment (Harrison 2005). The fungi also have a very high surface/area to volume ratio given the minute size of their hyphae and the branching extent of their mycelium. This gives them an increased absorptive capacity, which benefits the plants with which they associate (Selosse et al 2006). Perhaps most importantly, mycorrhizal fungi are also able to take up chemically or even physically immobilised nutrients and make them available to the plant. This includes both macronutrients such as phosphate irons, and micronutrients such as iron. An example of this is in clay soils or highly alkaline soils, in which mycorrhizae can use ion exchange, organic acids, chelation or other methods to access nutrients (Li 2006). These benefits extend as far as allowing plants to colonise barren soil, with plants without mycorrhizae often being outperformed by those with mycorrhizae (Richardson 2000). This can be seen even at the ecosystem level, with the absence of mycorrhizae resulting in slower colonisation of degraded landscapes and slower plant growth during ecological succession (Jeffries 2003).

This increased accessibility of nutrients also applies to organic matter such as plant secondary growth (such as wood and bark). The mycorrhizal fungi, like most fungi, are saprophytes or primary decomposers, and some can break down lignin, cellulose and other organic compounds to provide both themselves and their host with nutrients. In some environments such as humic or ‘dystrophic’ forests, where phosphate is less available to plants’ roots, the plants are able to bypass the depleted soil and instead draw nitrogen from the leaf litter, with the saprophytic mycorrhizal fungi breaking down the leaves (Hogan 2011). An example of this is the Inga Tree, which is now being used in a technique called Inga alley cropping (see Figure 5). The technique, suggested as a sustainable alternative to slash and burn cultivation, involves the planting of Inga alleys amongst agricultural crops, due to both their leguminous nature and their ability to recycle phosphorous from organic matter into the soil and prevent phosphate run-off (Guinness 2004). Another example of mycorrhizae allowing plants to inhabit nutrient-poor sites is the Lodgepole Pine, which has formed a symbiosis with both Suillus tomentosus (a fungus) and nitrogen fixing bacteria in specialised structures known as tuberculate ectomycorrhizae (Paul et al 2007).

Figure 5 – Inga alley cropping can be seen in the image above. It is being proposed as an alternative to slash and burn cultivation. Aside from other benefits the inga tree provides, the symbiosis of this tree with mycorrhizal fungi and nitrogen fixing bacteria means the tree provides both phosphorous and nitrogen to neighbouring agricultural plants (Hand 2014).

Aside from increasing plants’ access to nutrients and water, mycorrhizal fungi also provide other benefits to their hosts, including increased resistance to pathogens, toxicity and environmental stresses. Some mycorrhizae can excrete enzymes that are toxic to soil borne organisms and pathogens, such as nematodes (Azcon-Aguilar 1997). Even just the formation of the mycorrhizal association itself appears to improve a plant’s defences, with the establishment of the association resulting in a modulation of the plant’s defences that systematically activates or ‘primes’ the plant for responses against pathogens (Jung 2012). More generally, mycorrhizae help control plant pathogens through: anatomical and morphological changes to the rhizosphere; changing the microbial population of the rhizosphere; and eliciting plant defence mechanisms (Azcon-Aguilar 1997). Plant protection, especially against instincts, can also take place through plants utilising the mycorrhizal network to send and receive warning signals (Babikova et al 2013 and Johnson et al 2015). Aside from protecting against biological threats, mycorrhizal fungi also aid their hosts through increased resilience against environmental stresses, including: situations of drought (Lehto 1992 and Nikolaou 2003); high salinity (Porcel 2012); and toxicity, especially heavy metals in contaminated soils or highly acidic soils (Tam 1995), putatively achieved through the binding of toxins to non-vital components of the mycelial network, thereby preventing its uptake by critical components of the mycorrhizae (Richardson 2000).

These benefits are summarised by McCoy (2016) who believes that mycorrhizae can: increase nutrient use efficiency by plants, thereby decreasing application needs and run off; improve soil structure and stability through the production of glomalin; supress pathogens; improve root growth and survival; increase efficiency of water use; and, perhaps more controversially, alter phytochemical attributes of a plant and increase flowering or nutritional value. Although these purported wonders of mycorrhizae for garden health must be taken with a grain of salt, the literature described above does substantiate most of these claims.

How to establish or preserve mycorrhizae

How can we take advantage of the benefits mycorrhizal fungi have to offer? As was stated earlier, arbuscular mycorrhizal fungi can be easily cultivated. The Rodale Institute (2010) has developed an introductory method for gardeners/farmers to achieve this, which begins with introducing commercial arbuscular mycorrhizal fungus spores to a host plant crop (see Figure 6). An association will then form with the host plant over the course of approximately four months, after which the plant is killed (via cutting the stem/trunk) and watering is stopped, forcing the fungus to produce spores. Approximately a fortnight later the roots of the plant crop can be harvested for use as inoculum or for later use. Although an initial inoculum is required, the process greatly amplifies the amount of inoculum available at the end. The Rodale Institute (2010) has conducted trials showing that inoculating crops can increase the yields of many crops, including tomatoes, potatoes, sweet potatoes, strawberries, leeks and capsicums.

Figure 6 – The Rodale Institute (2003) has produced mycorrhizal inoculum using bahiagrass, seen above. This grass was selected because it is killed by first frost of autumn/winter, allowing the harvest of the inoculum and preventing the grass from becoming invasive.

According to Dr. David Douds, a microbiologist who has conducted comprehensive trials in association with the Rodale Institute, there are also some key strategies that can be undertaken to conserve and promote mycorrhizae in farms or gardens, whether this be instead of or in addition to inoculation. He cautions against frequent or heavy tilling and soil applied fungicides, along with the overuse of chemical fertilizers, especially those rich in phosphorous (which can circumvent or weaken the mycorrhizal association). However, he has found that even phosphorous rich soils exhibit mycorrhizae or can benefit from mycorrhizae because of the range of other benefits they provide such as enhanced disease resistance, improved soil aggregation and better water usage (Rodale Institute 2003).

Dr Douds instead recommends using light tilling, weeding and mulching and especially encourages the use of over-winter cover crops or even a weedy fallow which allow mycorrhizae to persist throughout winter and increase their viability or survivability when they come out of dormancy during warm spells in early spring or late fall. Given this advice, mycorrhizal fungi appear to give the biggest benefit in low-input farms or gardens where they allow crops to more efficiently utilise inputs. Finally, he recommends careful consideration of crop rotations, with some crops not benefiting from the presence of mycorrhizal fungi or even depressing the levels of mycorrhizal fungi after these crops are grown, including plants which do not form mycorrhizal associations such as the Brassicaceae (broccoli, cabbage, turnips etc.), Chenopodiaceae (beets and spinach) and Polygonaceae (buckwheat)(Rodale Institute 2003).

Impact of urban soils on mycorrhizae

Given that mycorrhizal associations tend to flourish the most in less modified settings such as low input farms or gardens, is it possible for mycorrhizae to flourish in the urban environment, which tends to be more homogenous, disturbed and contaminated? Dietrich et al (2016) found that urbanisation does indeed alter the physiochemical environment in such a way to that microbial ecosystems tend to converge. They found that ectomycorrhizae decreased in biodiversity and abundance in both turf and ruderal land-uses, as part of a clear trend in the widespread suppression of ectomycorrhizal fungi by human management practices such as physical disruption of the soil, nutrient enrichment and other plant management strategies. This convergence is also a deforestation response, with the removal of tree hosts denying mycorrhizal fungi access to the photosynthates they depend on. This convergence was noted especially in temperate and boreal ecosystems, but this may be due more to these regions having initially more diverse mycorrhizal populations, with decreases in that greater population being more noticeable.

Similar investigations by Tyburska et al (2013) found similar convergence taking place even at low disturbance levels, and with higher rates of disturbance resulting in the further reduction of mycorrhizal fungi to limited ‘Urban ectomycorrhizal fungus groups’ (Karpati et al 2011) and with some fungi being limited to specific sites (Gebhardt et al 2007). Karpati et al (2011) also found that the ectomycorrhizal fungi associated with late ecological succession stage plants were missing in disturbed sites. Bainard et al (2011) argue that urban sites tend to favour vesicular and arbuscular mycorrhizae and that these associations are becoming of greater importance than ectomycorrhizal fungi in urban areas. Another factor that affects mycorrhizal populations is the introduction of non-native species into the urban environment. Although non-native trees can utilize both native ectomycorrhizal communities (Tedersoo et al 2007) and endomycorrhizal communities (Cousins et al 2003), non-native stands of trees nevertheless exhibit lower fungal diversity (Cousins et al 2003).

According to Dietrich et al (2016), key strategies for combatting this convergence include preserving patches of remnant ecosystem and planting native flora to support native mycorrhizal fungus assemblages. Another strategy for promoting mycorrhizal fungus populations (in the context of afforestation) is the inoculation or artificial introduction of mycorrhizal fungi into plantings (Szabo et al 2016), which will help plants overcome urban stresses and mitigate the impact of low levels of naturally occurring fungal inoculum in disturbed soils (Bainard et al 2011). Rao et al (2006) determined that these inocula are more effective when conducted in situ, rather than in a nursery environment. According to Schaefer (2011) this fungal repopulation can also take a more natural form, with the planting of close natural stands serving as a source of fungal propagules that can be dispersed by wind or other vectors to different sites (Stabler et al 2001).

Conclusion – Mycorrhizae: plant panacea or placebo?

Although this report has presented many of the benefits of fostering mycorrhizal fungi in urban spaces, Kleczewski et al (2016) remind us that the inoculation of urban plants with mycorrhizal fungi should not be viewed as a miraculous panacea, but instead just one tool to be considered along with others. In terms of the food-grower or home gardener, the focus of the mycorrhizal scientific literature on tree species and natural ecologies, rather than on crop species, makes adamant assertions about their usefulness difficult. Indeed, the nature of most modern crop production, both industrially and at the garden scale, demonstrates that mycorrhizae are indeed largely dispensable in this context, albeit at the expense of microbially healthy soil. However, the work of researchers such as David Douds of the Rodale Institute demonstrates that mycorrhizae can be integrated into crop production to great benefit, especially when the method of production is one that is seeking to prioritise the efficient use of water and nutrients, a goal that both lowers the cost of inputs and mitigates the impacts of nutrient runoff and water depletion on the environment. Of course, this approach does have its setbacks, as the minimal tilling and minimal fungicide use prescribed by Douds to foster mycorrhizae necessitates more careful crop planning and maintenance and potentially more labour. The world of urban farming, however, is often characterised by a higher availability of labour, decreased access to agricultural machines or spaces that can accommodate them, and, most importantly, an increased interest in sustainability. Urban food production therefore represents a valuable opportunity to both evaluate and re-emphasise the role beneficial symbioses such as mycorrhizae play in the health of our soil, and in turn, the production of our food.



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