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The Plant as a Host for Fungi: An Opinion

Introduction

The most readily and widely available source of organic carbon is the plant. However, while all plants photosynthesise or have access to photosynthates, plants are not a homogenous or uniform group of organisms. As well, plants have evolved a suite of defences against unwanted invaders. Thus, though very attractive to heterotrophic organisms, plants are a highly diverse kingdom, with different approaches to their interactions with fungi found within the kingdom.

In the first instance, plants have quite characteristic defences. The defences have been categorised as generalised, including tannins and lignin, and induced, including phytoalexins. Further, the nature of the defence appears to be related to the mineral nutrients available to the plant. Carbon-based defences are more common in poor soils while nitrogen-based defences are more frequently found in plants growing in rich soils. Members of the plant kingdom are heavily defended against loss.

Because of the presence of extensive and variable defence mechanisms, we might ask why plants become colonised by fungi at all. After all, the fungus removes organic carbon from the plant. It might be argued that this loss is tolerated by the plant because the plant grows in sunlight and therefore can afford to pass some of its photosynthate to the heterotrophic party. Others would argue that loss of organic carbon would only make sense if the plant benefited in some way from the association.

The plant has three quite clear types of association with fungi: endophytes of the leaves, stems and roots, mycorrhizal fungi of the roots, and plant pathogens sensu lato. Note that epiphytes are not considered as a separate group here.

Endophytes in Shoots

Vertically transmitted fungi such as Neotyphodium in grasses, and horizontally transmitted fungi such as Rhabdocline parkeri in Douglas fir clearly benefit thier host plant. LINK In general, the fungus has a complex interaction with the host. The fungus lives for some years within the leaf tissue and gains access to organic carbon of the host. Host defences apparently limit spread of the endophyte through the tissue. Plant responses are apparent and in some cases, the fungus is constrained to one or two cells until the tissue senesces.

The fungus benefits the host in both the examples above: insect herbivory is reduced in the presence of the endophyte. The fungi produce secondary metabolites which can  slow rates of metabolism of those insects that feed from the plant. Some further metabolites deter insects from landing and feeding. These are clearly mutually beneficial associations.

The benefits of other associations are less obvious. Some endophytic entomopathogens colonise susceptible insects as they feed or traverse the plant. Endophytes may also induce a localised or systemic plant response that is detected by the insect, leading to reduced loss of plant tissue. Under these circumstances, the colonised host plant gains a clear competitive advantage over uncolonised plants.

 

Neotyphodium
Leaf colonised by Neotyphodium.

The fungus gains access to an almost unlimited supply of organic carbon. The host provides a protected and predictable environment. In the case of Neotyphodium, the host also provides the mechanism for initiation of colonisation of the next plant generation. Quite clearly, the association is mutually advantageous in these cases.

A wide range of fungi can be isolated from within healthy plant tissues. The cost to the host in most of these cases (endophytes sensu lato) is unknown. Though just as readily isolated, less is known about endophytes of roots. In most cases, the benefit to the host is unknown. While benefit may be in the form of a reduction in herbivory, other hypotheses require careful examination. The endophyte may directly compete with potential pathogens, and other members of the general biota resulting in benefit to the plant. Indeed, the endophye may modify the environment in which the plant lives, resulting in benefit to the plant. Finally, the assumption that endophytes always benefit thier host cannot be sustained. In some circumstances, presence of the endophyte will have detrimental effects on the host plant.

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Mycorrhizal fungi in Roots

Mnay fungi can be seen in and isolated from healthy roots of healthy plants. A clear relationship of mutual benefit has been demonstrated in the case of mycorrhizal associations: much less in known about other fungi. LINK In mycorrhizas, the fungi colonise roots and access organic carbon from the host. The fungus has the potential to enhance access by the host plant to mineral nutrients, commonly phosphate and/or nitrogen from soil. In the case of orchids, the mycorrhizal fungus also ensures germination of orchid seed in the wild, supplying organic carbon to the plant.

While many fungi can be isolated from leaves, fewer seem to be present in the living part of the root. Many saprotrophic fungi exist outside the exodermis in young roots, and outside the endodermis once cortical cells have senesced. These fungi do not overcome host barriers, they are living in dead or dieing tissue, and so are not equivalent to endophytes in leaves. The number of fungi inside the living tissue of the root is highly variable. Water and nutrient stress to the host plant and absence of mycorrhizal fungi appear to be associated with increased colonisation, though this hypothesis requires testing. Some 10% of the culturable fungi are pathogens. Around half of the others may leave the plant unaffected or actually increase growth of the seedling.

Dark septate endophyte are a taxonomically diverse group of melanised, slow growing fungi. A few isolates increase plant growth in experimental conditions. The mechanism of enhanced plant growth remains uncertain.

Direct and indirect interactions between endophyte and plant are possible. Increased mineral uptake and drought tolerance might be hypothesised, analagous to the effect of mycorrhizal fungi. Presence of endophytes might induce a host response that reduces colonisation by root pathogens. For example, the presence of competitors of pathogens has been documented. Binucleate Rhizoctonia appears to competitively reduce colonisation of pathogenic Rhizoctonia solani. Similarly, pathogenic and saprotrophic species of Fusarium interact. Indeed, the biocontrol fungus Trichoderma, is most effective when it has colonised the cortex of the root of the host plant. Finally, the fungus may modify the soil environment in which the plant functions. This area of research is wide open.

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Pathogens

Interestingly, most potential plant pathogens do not penetrate the barriers of the host plant. We see pathogens in plants, but only a few of the enormous array known to cause disease that can be isolated from the surrounding soil. LINK In a few cases, the fungus may penetrate the host tissue, only to have it collapse around the penetration tube. Plant penetration is the exception, rather than the rule. Evolution of pathogen/plant interactions appears to have led to a situation where the plant is not seriously disadvantaged in natural ecosystems.

However, in cropping systems the interaction can be devastating. When the pathogenic fungus initiates infection, it spreads rapidly. This is because the crop is a genetically uniform target (monoculture), growing in uniform environments, at the same rate. Once established in plants in cropping soil, pathogens are positively selected LINK. The pathogen has the genetic constitution to avoid recognition by the host, and the physiology to parasitise the entire crop. Some of the most spectacular crop losses have been where a single crop has been almost wiped out by a single genotype of a pathogen. While these incidents have historical importance, they also contain lessons for plant breeders and growers. The ramifications include appropriate targets for plant genetic manipulations, attitudes to sources and use of genetic diversity, reliance on single genotypes, and loss of organic carbon from and microbial diversity in arable soil LINK

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Colonisation

In all these cases, the interaction between fungus and plant has involved a series of steps between plant and fungus (see below). When the spore lands on the plant surface, it releases a chemical message which may be recognised by the plant. The spore attachs to the surface, germinates, and the emergent germ tube then forms an appressorium. A fine penetration peg grows through the plant surface, either directly through the epidermis, or via a natural (stomata in the leaf) opening. The hypha then ramifies through the plant tissue.

Initial energy for colonisation comes from the spore, perhaps with a small contribution from plant exudates on the surface. This leads to the collapse of the spore and the appressorium. Plant carbohydrates become increasingly important as the tissue is penetrated.

Presumably, those fungi that are recognised as pathogens will induce an immediate (hypersensitive) response from the plant that results in no subsequent colonisation. The details of pathogenesis are now understood. The details of interaction between mutualistic symbionts are still being clarified, though appear to be similar. It is clear that colonisation is an active process which involves a series of steps enabling colonisation and yet controlling  spread. Specific fungi interact with each plant species. A small number of generalists also establish colonies in a range of plants. Presumably, the process of recognition and colonisation is under tight genetic control, and may be as complex as the immune system in mammals.

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Conclusion

Much of the study of fungal colonisation of plants has concentrated on plant pathogens. However, a diversity of fungi interact with plants. Some of the fungi may cause disease, but many apparently lack detriment, and a few clearly benefit the host. The approach we take with fungi in plants needs to be modified by the knowledge that fungi may benefit the plant in ways we have yet to understand. The results of these studies have the potential to reorganise the way we think about fungi, though they may also confirm the pathology- based thinking extant today.

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