13.17 The effects of mycorrhizas and their commercial applications, and the impact of environmental and climate changes
So far we have described some detail about each specific type of mycorrhiza. We now want to bring these strands together and discuss the mycorrhizal symbiosis in general.
The major advantage that a mycorrhizal association confers to both plant and fungus is a supply of nutrients enhanced beyond that which would normally be available. It is usually a bidirectional movement of nutrients: carbon source (as carbohydrate) from plant to fungus, and soil nutrients, especially nitrogen and phosphorus, from fungus to plant. This is the essential quality of a mycorrhiza, and is presumably the foundation for the mutualistic association because it results in the synergy that the two organisms involved can perform better when together than they can perform when apart. There are exceptions.
From what we have already described about monotropoid mycorrhizas and all orchidaceous mycorrhizas at the juvenile stages of the plant, it is not at all clear that the fungus actually benefits from the association. That is, these associations are much closer to being better described as parasitism of the fungus by the plant. Remembering that the Orchidaceae is the most diverse family of flowering plants, it is clear that there is a very large number of this particular exception. The monotropoid relationship is more complicated as monotropoid mycorrhizas are often ectomycorrhizal with surrounding trees, and carbohydrates from that alternate source sustain both the fungus and the associated Monotropa.
As a rule, mycorrhizal infection enhances plant growth by increasing nutrient uptake by:
- increasing the surface area of the absorbing organ within the soil (it becomes the mycelium rather than the root hairs);
- mobilising nutrients from sources which are not available to the plant because they need to be digested or made soluble by enzymes produced by the fungus;
- scavenging what nutrients are present by excreting chelating compounds and/or producing transporters with very high affinities.
Nutrients are obtained by hyphae, which extend from the roots, sometimes organised into strands, exploring and exploiting a much larger volume of soil than the host roots themselves could possibly exploit. Following uptake by the hyphae, nutrients are translocated back to the host root with high efficiency (see the sections on The endomembrane systems and Hyphal fusions and mycelial interconnections in Chapter 5, and The flow of nutrients: transport and translocation in Chapter 10; CLICK on the section titles to view the pages now). When the nutrients have been returned to the weft of hyphae that usually surrounds mycorrhizal roots, or the hyphal sheath of ectomycorrhizas, both of which can act as storage sites for nutrients that can be supplied to the plant as and when required.
In return for receiving extra nutrients, mycorrhizal host plants supply the fungus with between 10% and 20% of the photosynthates they produce, which go to the formation, maintenance and functioning of the mycorrhizal fungi and their associated structures (Jakobsen & Rosendahl, 1990). This is an investment in the fungus, not a tax on the plant: the more carbohydrate supplied to the fungus, the greater its ability to win soil nutrients for the benefit of the plant.
With regard to the transfer of carbon from plant to fungus, carbohydrate leaves the plant as sucrose, is hydrolysed to glucose and fructose, most often by an invertase of plant origin, then carbohydrates entering the fungi appear in the hyphae as trehalose, and in some strains as mannitol. When carbohydrates are transferred from fungus to plant, as in orchid and monotropoid mycorrhizas, the reverse occurs, with trehalose and mannitol being converted to sucrose.
In arbuscular mycorrhizas nutrient exchange occurs through the arbuscules and in ericoid (and other endotrophic) mycorrhizas through the hyphal coils; both of these structures are intracellular interfaces as far as the plant cell is concerned. In contrast, the interface between plant and fungi in ectomycorrhizas takes place through the Hartig net, which is extracellular to the plant cell.
Direct uptake of nutrients by plant roots can often result in zones of nutrient deficiency around the root system. Subsequent absorption of nutrients is then limited entirely by the rate at which nutrients can move through the soil. Hyphae can grow past these depletion zones and by so doing enhance the absorption of nutrients by the root. Nourishing a mycorrhizal fungus so that it continues extending its hyphae is a more economical way of sustaining contact with nutrients than by continually extending roots.
The rate at which nutrients move through the soil depends on their chemistry and can be crucial to their availability to plant roots. Phosphorus, in the form of phosphate (PO4-), has very low mobility in soil, because the phosphates of the most common divalent metals are insoluble, and this tends to be the limiting nutrient in most ecosystems. In contrast, ammonium (NH4+) is about ten times more mobile than phosphate, but is also required and absorbed in ten times greater quantity. Ammonium is an acid (ammonia, NH3, is a gas) and is in greatest abundance in acidic soils, such as those of forests and heathland; otherwise in most soils nitrate (NO3-) is the main immediately-available source of nitrogen for the root.
What the fungal component of the mycorrhizal association adds to these considerations is a change in the meaning of the word ' available'. When a horticulturalist talks about ‘available nitrogen and phosphorus’ they are talking about soluble salts in the soil water. If the salt is not soluble, it is not available; if the element is not in simple mineral salt form, it is not available. The fungus doesn’t speak this restrictive language.
The fungi produce organic compounds such as citrate and oxalate (Plassard & Fransson, 2009), which help in the desorption of adsorbed phosphate or the dissolution of poorly soluble phosphates; they also excrete extracellular acid phosphatases which release phosphate from organic complexes (phosphoglucans, phospholipids and nucleic acids) in the soil. In addition, fungi store and translocate phosphorus in the form of polyphosphates in the hyphae, which maintains a low inorganic phosphate (low Pi) concentration in the hypha and enhances uptake of any external phosphate that can be found.
Add to these considerations the large volume of soil explored per unit surface area of all those narrow hyphae, and the meaning of the phrase ‘available phosphorus’ to the mycorrhizal root is expanded enormously, and, in general, the large growth increases in the plant consequential on mycorrhizal infection are due to increases in phosphate absorption. In arbuscular mycorrhizal plants up to 80% of the plant phosphorus comes to it through the hyphal network. The beneficial effects of mycorrhizas with regard to phosphorus uptake are lost if the concentration of phosphorus in the soil increases. Both arbuscular and ectomycorrhizal infections decrease in high phosphorus soils. Ultimately, the mycorrhizal association can be abandoned in such soils.
Similar considerations apply to the nutrient nitrogen. Plants roots may be limited to mineral sources (NH4+ and NO3-) and most plants will preferentially take up ammonium over nitrate, largely because nitrate-nitrogen must be reduced before it can be used in metabolism and this is an energy-demanding process. This preference is also expressed by fungi, indeed many fungi are not able to utilise nitrate at all. Fungi are particularly efficient at assimilating ammonium through high affinity transporters, but their main contribution is their ability to use organic nitrogen sources, through the production of proteinases and peptidases. This allows them to access nitrogen sources that are not available to non-mycorrhizal plant roots. As with phosphorus; if mineral nitrogen becomes available to the plant from other sources (by application of chemical fertilisers like NH4NO3, for example) the value of the mycorrhizal association to the plant is diminished and mycorrhizal infections tend to decrease.
Mycorrhizas offer other benefits to their plant partner, though. Metal ions such as potassium (see Fig. 14), calcium, copper, zinc and iron are all assimilated more quickly and in greater amounts by mycorrhizal plants, again through the ability of the fungal hyphae to release, absorb and translocate minerals quickly and efficiently. The ectomycorrhizal fungal sheath also provides a number of advantages over naked (that is, non-mycorrhizal) plant roots. The sheath hyphae can accumulate and immobilise heavy metals, so when growing in soils with high concentrations of heavy metals, like zinc, cadmium and arsenic, the metals are unable to reach the plant tissues and the host plant remains undamaged (Hartnett & Wilson, 2002).
Other benefits of mycorrhizal associations. Mycorrhizal fungi can also benefit their plant partners by increasing tolerance to other adverse conditions. Probably most crucial, and controversial, is that all fungi can grow at water potentials lower than those that plants can tolerate. This means that fungi remain metabolically active and scavenging for water and nutrients in conditions where non-mycorrhizal plants would wilt, cease to grow and eventually die. Mycorrhizal plants can therefore continue to grow in conditions of high water stress because the extended mycelial zone of their mycorrhizal fungi enables them to tap reserves of water from deeper in the soil and from greater distance from the host plant. This operates in all ecosystems but is especially obvious in desert ecosystems. Many of the most common desert plants, including cacti, are heavily mycorrhizal, showing that mycorrhizas make a particularly important contribution to the water relations of their host plants even in those extreme ecosystems where soils have poor water retention.
What is controversial about this is that plant physiologists argue that the cross-sectional area of fungal hyphae connected to a root is typically too small for them to make a significant contribution to water flux in the plant, so water transport by the mycorrhiza may be significant only in delaying wilting at times of extreme water deficit. This line of argument seems to ignore the fact that fungal hyphae are highly adapted to translocating large quantities of all sorts of nutrients extremely rapidly over long distances; it’s their way of life. Add to this consideration the sheer quantity of extraradical mycelium that might be supporting a plant (see Fig. 12B) and we think there is little doubt about the potential value of the mycorrhizal fungal contribution to the water relations of their host plant.
Earlier we mentioned that mycorrhizas protect the plant against root pathogens. Ectomycorrhizas are particularly effective and have several strategies to combat pathogen attack:
- excretion of antifungal and antibiotic substances, 80% of Trichloma spp. produce antibiotics and Boletus and Clitocybe produce antifungal substances;
- stimulation of the growth of other microorganisms, which themselves limit pathogens;
- stimulation of the plant to produce antibiotics under the control of the mycorrhizal fungus;
- structural protection of the root by the thick fungal sheath; the mechanical barrier gives effective protection because plant pathogens need to access plant tissue to infect it, they cannot usually infect fungal tissue.
Arbuscular mycorrhizas also increase plant resistance to pathogen attack, in particular to root infecting fungi, such as Fusarium oxysporum, and Oomycota like Phytophthora parasitica. Because most root pathogenic fungi infect roots more rapidly than do arbuscular mycorrhizal fungi, simultaneous infection often leads to the mycorrhiza being out-competed. However, if the mycorrhizal association is already established, pathogenic infection is much reduced.
For example, one study showed that arbuscular mycorrhizal tomato plants challenged with Fusarium showed only 9% necrotic roots compared to 32% in non-mycorrhizal plants (Werner, 1992). Similarly, arbuscular mycorrhizal infection has been shown to reduce the effects of pathogens and even pests, such as root pathogenic nematodes. Little is known about the mechanism(s) involved in this case, but the plant response to mycorrhizal infection, perhaps altered cell wall chemistry or the production of phytoalexins, may cause a general improvement to pathogen and pest resistance (Newsham, Fitter & Watkinson, 1995).
It’s not just plants that benefit from all those mycorrhizal hyphae. We have discussed elsewhere that many small animals (microarthropods in particular) depend on fungal mycelium for food (see Fungi in food webs section in Chapter 11; CLICK HERE to view the page). We have also stated above that mycorrhizal fungi consume about 20% of their host plant’s photosynthetically fixed carbon.
Put the last two sentences together and you will see that mycorrhizal hyphae are an important route for the redistribution of plant-derived carbohydrate into the soil animals: atmospheric carbon dioxide to photosynthetic carbohydrate in the plant, sucrose to hexose sugar in the apoplastic space, hexose to trehalose in the mycorrhiza synthesised into fungal tissue, which is finally eaten, digested and transformed into the bodies of the small animals that make up the soil biota.
Structure and change of natural communities. By benefiting individual plants in the ways outlined above mycorrhizas inevitably affect the ecology of plant communities. In general, both ectomycorrhizas and arbuscular mycorrhizas show very low host specificity, which allows a single fungus to infect several plants in one area, and also several different fungi to infect a single plant. This allows mycorrhizas to establish a network that may link many different plants of many different species within a single habitat. This is the ‘woodwide web’; a network that allows carbohydrates, amino acids and mineral nutrients, and chemical signals, flow between plants through their shared fungi.
The woodwide web can allow seedlings to be supported by their parent plant while establishing themselves. Receiving nutrients through the mycelial network can also allow plants and seedlings to thrive in less favourable conditions, such as in local shade, suffering water stress, inadequate soil, etc., the disadvantaged plants having their nutrition supplemented by resources from neighbouring plants growing in more ideal conditions. A consequence of the contribution that mycorrhizas make to plant growth is that plant reproduction increases and offspring survival is improved, which can increase population size and influence population density and species distributions within the community (Koide & Dickie, 2002).
Many of the fungal fruit bodies with which we are most familiar belong to mycorrhizal fungi and it is common knowledge that they are seasonal and follow successional changes alongside the associated changes in the vegetation. There is a considerable research literature about changes in species composition of the communities characterising a range of habitats (Frankland, 1998). Successions of ectomycorrhizal agarics have been described during the development of temperate forests, particularly those of Betula, Pinus and Picea.
The pattern and succession of mycorrhizal development varies during the life of a tree. Some fungi are successful primary colonisers (called early-stage fungi), whilst other fungi dominate as the tree ages and reaches maturity (late stage fungi). However, some fungi will infect regardless of plant age, and seedlings germinating in a mature forest are usually colonised by the dominant late stage fungi. Early stage fungi have more of a role where their plant partner is a pioneer colonist and there are few other soil fungi present. These early stage fungi act like ruderal or r-selected species (populations that experience rapid growth and rapid reproduction), and those of the late stage are unable to survive in soil not already inhabited by other mycelia and are k-selected organisms (k-selected species tend to be very competitive, with stable populations having low reproductive rates).
So, as far as forest fungi are concerned, species diversity tends to increase until canopy closure (which takes about 27 years in northern temperate forests), but declines when tree litter accumulated and a greater proportion of the nitrogen was in organic form. Laccaria proxima is an example of agarics that are not highly selective of their host trees, and that reproduce prolifically, producing relatively small fruit bodies lacking mycelial strands or cords, and occurring under young, first-generation trees. More host-selective species, for example Amanita muscaria, with larger, more persistent fruit bodies, which are often served by mycelial strands and cords (implying greater dependence on nutrients supplied by the host tree) typified the later stage.
A word of warning is necessary here, because evidence based on the presence of fruit bodies above ground can be misleading unless it is accompanied by information about the mycelia associated with the tree roots. Some common species of mycorrhiza fruit rarely if at all. This is one reason why so much attention is currently given to analysis of molecular sequences from the environment to characterise fungal diversity, using PCR-(polymerase chain reaction)-based and nucleic acid hybridisation-based techniques (Mitchell & Zuccaro, 2006; Anderson & Parkin, 2007). The picture that emerges when ectomycorrhizas on pine roots are studied as mycelia using these molecular techniques is slightly different from that resulting from study of fruit bodies. Mycelia indicate that species diversity increases for up to 41 years before it stabilises (Frankland, 1998).
The distinction between early and late types of fungi is important commercially as it aids the forester, for example, to choose between mycorrhizal inoculants for forest nurseries and for regeneration of trees following deforestation. The early stage fungi can be used as inoculants to stimulate new forest growth, whereas the late stage fungi are not suited to this.
The impact of climate change. Changes in the seasonal pattern of fruiting in the UK have been detected from field records of fruit body finds made over the last 60 years (Gange et al., 2007). The outcome of the analysis of these data shows how our common fungi are reacting to climate change, which has caused fungal fruiting patterns in the UK to alter dramatically over this time period. The changes in fungal fruiting mirror changes in British temperatures recorded since 1975. In temperate climates, the majority of larger fungi are expected to fruit in autumn, following mycelial activity in spring and summer. In general the date of first fruiting is now significantly earlier in the year, and the last date of fruiting is now significantly later in the year than they were 60 years ago, resulting in an extended fruiting season. The increase is dramatic: in the 1950s the average fruiting period of the 315 species in the data set was 33.2 days, but this has more than doubled to 74.8 days in the first decade of the 21st century (Gange et al., 2007).
Fruiting of species that are mycorrhizal with both deciduous and coniferous trees is delayed in deciduous, but not in coniferous forests, indicating important physiological differences in climate responses between these ecosystems. Significant numbers of species that previously only fruited in autumn now also fruit in spring, indicating increased mycelial activity and decay rates in ecosystems in response to changes in spring and summer temperature and rainfall. Such analyses show that relatively simple field observations of fungi can detect climate change, and that fungal responses are sufficiently sensitive to react to the climate change that has already occurred by adapting their pattern of development.
The fruiting trends seem to be responses to temperature and rainfall in July and August. In years when July and August temperatures were high and rainfall low, fruiting was delayed. Trends among mycorrhizal species are different from nonmycorrhizal saprotrophic fungi in the same habitats, suggesting that mycorrhizal species respond to cues from their host trees more than environmental factors (Gange et al., 2007).
Overall, the impact of climate change on UK fungi seems to be that the mycelium of many species has now become active in late winter and early spring as well as late summer and autumn (well into November, probably). This has major implications for ecosystem functioning, as it indicates increased decomposition rates and altered competition between fungi over this much longer interval of mycelial activity in the year. The fact that mycelial activity is changing and increasing rapidly means that decay processes and symbiotic associations will also change, leading to profound alterations in grassland and forest dynamics and food webs (Gange et al., 2007; Moore et al., 2008).
Global environmental change, especially increased atmospheric CO2 concentration and consequential increases in temperatures, will affect most ecosystems. We need to know more about the effects of these changes on mycorrhizal systems because, as we have outlined above, mycorrhizal fungi have a major impact on the structure of plant communities and already account for a substantial proportion of their host’s photosynthetic capacity (Söderström, 2002; Staddon, Heinemeyer & Fitter, 2002).
Commercial applications of mycorrhizas. Given that mycorrhizas are nearly always beneficial to plant growth and health, their potential value in agriculture and horticulture could be immense. Studies have shown that several crops respond well to inoculation with arbuscular mycorrhizal fungi: growth rates of maize, wheat and barley increased by two, three and four times, respectively, when inoculated with arbuscular mycorrhizas. Onions inoculated with arbuscular mycorrhizas showed a six times greater growth than non-mycorrhizal controls. Despite this potential, however, deliberate inoculation of crops with mycorrhizas is rarely done and mycorrhizas are introduced intentionally in only a few industries.
Forestry is one of the industries to recognise and exploit the role of mycorrhizas in plant growth. The majority of commercial timber comes from trees forming ectomycorrhizal associations and amounts to more than three billion m3 felled annually, worth something like £400 billion. New plantations benefit considerably from ectomycorrhizal inoculation, especially if the land has not previously grown ectomycorrhizal trees. Similarly, non-indigenous species of tree (so-called exotics) nearly always grow unsatisfactorily unless suitable mycorrhizal fungi are introduced with them. However, once an exotic has been established, others of its species are easier to cultivate as the mycorrhizas are already established in the soil.
Several smaller industries regularly use mycorrhizal infection. Germination of orchid seeds requires mycorrhizal inoculation unless the seedlings are supplied with the necessary nutrients in artificial culture. However, non-mycorrhizal seedlings tend to be more susceptible to fungal disease when mature, and the industry generally accepts that the key to producing healthy, mature plants is to inoculate seedlings with mycorrhizas.
As mentioned above, mycorrhizal plants can tolerate higher levels of heavy metals in soils than those without mycorrhizas, so mycorrhizas can contribute to reclamation programmes for ex-industrial land. Large areas of waste land created by mining and other heavy industrial operations are often polluted by metals such as aluminium, iron, nickel, lead, zinc or cadmium. The metallic pollutants may also affect soil pH and the mobility of essential nutrients such as nitrogen, phosphorus and potassium.
Restoration can involve major earth moving operations such as reshaping and regrading of slopes, and large scale toxic waste removal, with the result that the topsoil is largely artificial and is often pH-corrected and dosed with chemical fertilisers. Despite these efforts, up to 90% of plants may fail to establish and if recolonisation is discouraged bare soil remains unstable and subject to erosion.
A common reason for failure to recolonise is the absence of mycorrhizas, which can prevent heavy metal poisoning and help seeds to germinate successfully. By accumulating and immobilising heavy metals the mycorrhizal fungus acts a natural clean-up mechanism for soils. As we have seen above, mycorrhizas initiate the cycling of nutrients in the new soil, taking up immobile nutrients that would otherwise be unavailable to plants and compensating for the deficiencies in nitrogen and phosphorus that often afflict mining soils and industrial wasteland. Once a mycelial network has been established, soil structure and stability improves and the land is well on the way to restoration.
Updated December 17, 2016