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Endophytes

Introduction

A wide diversity of fungi are isolated from healthy tissues of most terrestrial and aquatic plants, and red and brown algae. Fungi are present in most plant parts. The leaves appear to house a greater diversity of fungi than the roots. The fungi may be either endophytes or latent pathogens. Endophytes are contained within the plant without disease. Plant tissues remain entire and functional. However, some endophytes may also be isolated from the surface of leaves, indicating an unclear separation between endo- and epiphytic life form.

Endophytic Fungi

Endophytes colonise plant tissue and remain within the tissue, except that fruiting structures may emerge through the surface of the plant tissue. Leaves may be colonised by a variety of fungi within a few weeks of leaf emergence. The colonies remain asymptomatic and some in perennial plant parts may have a very long life.

Endophytic fungi are found in all divisions of fungi so have presumably evolved the association independently on many occasions. The most common endophytes are anamorphic members of the Ascomycota, and some are closely related to fungi known to cause disease in plant or animal (especially insect). Phylogenetic evidence is used to suggest that some endophytes have evolved from pathogens and for others, vice versa. The mechanisms of host recognition and development of colonisation may also be common among closely related endophytic and pathogenic fungi.

A wide range of plants have now been examined for endophytes, and endophytes have been found in nearly all of them. An enormous number of different fungi can be isolated from plants growing in their native habitat. Most of the fungi are uncommon and narrowly distributed, taxonomically and geographically. However a few fungi are widely distributed with the host, suggesting a long standing, close and mutually beneficial interaction. Some fungi are found in many different terrestrial hosts, especially endophytes of crop plants. While most information has been gathered from terrestrial ecosystems, fungi are found in algae and seagrasses. Just as we know less about marine ecosystems, our understanding of the biology of marine endophytes is extremely limited and will not be discussed further.

Aerial dispersal either in the wind or on vectors is probably a common mechanism for fungal dispersal. Endophytic fungi colonise various parts of the plant. Many of the fungi sporulate in culture indicating the potential to release spores in the air. Indeed, sporulation is seen after senescence of plant tissues. However, few cases of dispersal have been documented in the wild and the various mechanisms remain unexplored.

Apart from Neothyphodium and some related species, endophytes are transmitted horizontally. That is, each plant is colonised by fungal propagules that arrive from the environment. The source of natural transmission has been determined in only a few cases. Most aerial endophytes will be vectored in the air and colonise plant tissue directly. Endophytes of roots will initiate colonies by hyphal extension from existing resources in soil. Other mechanisms are likely. Propagules of some endophytes have been found in the body of insect pests of the host. Intriguingly, at least four entomopathogens (Lecanicillium, Beauvaria, Metarhizium and Isaria) have been documented as endophytic fungi, and some grow systemically in the plant. Thus insects may disperse some fungi from host to host, and insect feeding may enhance initiation of colonisation.

Nutrients are cycled between the host and fungus. The endophytic fungus gains a protected and long-lived environment in which nutrients are readily available. Thus the benefits for fungi establishing endophytic associations are clear. The benefits for the plant are becoming clearer. They include:

Increased shoot and/or root growth, enhanced systemic resistance to plant pathogens or insect pests, improved plant response to abiotic stress such as heat and salt, enhanced uptake of minerals possibly following solubilisation, enhanced nitrogen use efficiency, and rate of recovery by physiologically impaired seeds.

Plants may benefit from the presence of endophytes in many ways. Potential plant benefits have been examined in several quite different cases. The parallels with Neotyphodium are clear in only a few cases. Rhabdocline parkeri produces a compound called rugulosin that reduces needle attack by borers. Metabolites produced by Phomopsis sp in cotton appear to deter larvae of Helicoverpa from feeding on leaves. These examples indicate the potential for further similar examples. Thier importance to the host will be determined by the toxicity of the compounds, distribution of the fungi in the plant and the size of the colonising unit in the plant.

Evidence of direct interactions bewteen insects and endophytic fungi is uncommon. Aphids feeding on leaves of cotton colonised by the entomopathogen Lecanicillium lecanii may become colonised when conditions permit. Presence of Lecanicillium lecanii in cotton leaves reduces feeding by aphids and slows the rate of reproduction. The effect is probably due to induction of host responses.

Endophytes may upregulate host responses to pathogens and pests. Biocontrol species of Trichoderma modify host responses to pathogens. Chaetomium globosum increases host resistance to rust and tan spot pathogens in wheat. Direct interactions between Trichoderma and plant pathogens have been documented, they appear to be unlikely with the endophyte Chaetomium. That is, subsequent attack by a plant pathogen invoked a much faster response from the plant and less disease developed as a consequnce: the plant had been "primed".

Increased plant growth may be a benefit arising from the presence of endophytes. However, enhanced growth of roots may be a benefit in that the plant is healthier, or it may indicate reduction in colonisation by arbuscular mycorrhizal fungi. If the latter, then mineral nutrition may be reduced and the plant less healthy. Critical examination of the mechanisms underlying growth data is warranted. The environment surrounding plants is complex and simple laboratory based experiments, especially using Arabidopsis may provide only part of the information needed to understand the role of fungi living in the plants.

The loss of plant resources to the fungus, and the potential of some fungi to grow rapidly in culture, indicates that the host regulates development of colonies. Each plant has a range of physical, chemical, constitutive and induced controls over the spread of fungi within tissues. The reaction of the plant to endophytes suggests that the interaction is one of confinement by the plant. Colonisation by endophytes ranges from single cells (Rhabdocline parkeri) to patchy distribution through leaves, stems and roots (Chaetomium globosum). An enormous diversity of phenolic and other deterrent plant compounds are associated with the presence of endophytic fungi, in fact more than are associated with potent pathogens in the same host. The picture is not the same for each interaction. An immediate upregulation of plant SA and JA pathways may be followed by down regulation of one or both. Most commonly, presence of endophytes upregulates or primes plant responses to pathogens. While some argue that endophye/plant interactions are an example of balanced antagonism, it is more likely that the interaction between fungus and plant involves an exquisitely balanced series of genetic and molecular triggers resulting in the endophyte being contained within the plant.

Endophytes appear to have direct and induced effects on plant responses to biotic agents. The interaction with abiotic agents remains less clear. The presence of an endophyte may enhance plant mineral nutrition. The mechanisms used by endophytic and mycorrhizal fungi seem to be quite different. For instance, the biocontrol fungus Trichoderma harzianum T22 increased the efficiency of use of fertiliser N in corn, resulting in increased plant growth. Not all strains of the fungus modify nitrogen use efficiency, and the mechanism is unclear. Indeed, some strains of Trichoderma and many other soil fungi can solubilise P in soil, but not all can alter plant P uptake; others increase plant growth but do not solubilise P. Modifying the mineral nutrition of plants appears to involve a variety of mechanisms.

Our understanding of the response of plants colonised by endophytes to temperature, salinity and water availability is uneven. For instance, Trichoderma improved germination of maize seed and enhanced subsequent growth in field soils, possibly via influence on the osmotic potential in the seed and enhancement of root growth to depth. In contrast, colonisation of the grass Dichanthelium lanuginosum by the fungus Curvularia protuberata resulted in the grass tolerating temperatures up to 65C. This tolerance was only possible because of the presence of a double stranded RNA virus in the fungus. Similar data documenting improved stress tolerance associated with endophytic fungi will need to consider more complex interactions than plant and fungus.

The broader, ecological function of endophytic associations is still being debated. Many fungi that are associated with the initial stages of litter decomposition are found in healthy tissue of the same plants. LINK Thus they are involved in the initial stages of resource recycling. Endophytes are also associated with aquatic activities. Many aquatic fungi have an endophytic stage in their life cycle. LINK An enormous diversity of endophytes are found and endophytes are probably associated with a wide variety of host functions.

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Latent Pathogens

Latent infection of plants by pathogens is the state where a host is infected by a potential pathogen and the signs of infection are absent. Latent infection is eventually followed the expression of macroscopic disease. Disease may be induced by time, changes to the host physiology due to the activity of the fungus, or changes in the environment that increase the stress on the plant. For instance, a decline in available light, or water, or increased herbivory may trigger development of signs of disease. In some cases, the signs of disease do not appear until the host tissue has reached maturity or senescence. The causes of disease are possibly due to significant removal of host resources, response to toxins released as secondary metabolites by the fungus, or alteration of host metabolic pathways which reduce host growth rates. At the very least, pathogens reduce the growth of the infected host. LINK

The period of latency has been defined as the time between initiation of infection to the expression of macroscopic signs. Thus the length of the latency period may be days or years. Latent infections are important for the damage they cause directly. They may also weaken the host plant, predisposing it to infection by other pathogens and pests. Further, infection in one plant is likely to spread to adjacent plants as happens with many pathogens of crops. Because the host lacks obvious signs, the presence of latent pathogens is likely to go undetected and their effect ascribed to other causes.

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Epiphytes

Fungi that exist on the surfaces of plants are called epiphytes. While some fungi are adapted to the plant surface, the community also includes propagules of air-borne species, fungi that would not otherwise be considered epiphytes. Some fungi on the leaf surface may also have an endophytic connection. The interaction of epiphytes with their host is largely unknown. The surface of the plant, especially the leaf is a challenging environment. Though plants express metabolites through the cuticle, the surface is dry, waxy and affectedby UV radiation.

Epiphytic fungi may differ markedly from endophytes. Epiphytes have many obvious characteristics that enable continuation through the inclement conditions of the leaf surface. In brief, epiphytes are likely to be coloured (melanised), and thus able to resist UV radiation. Some epiphytes can digest lipidic substrates, and thus may utilise the waxy layer covering the leaf. Finally the yeast form has a relatively short life cycle enabling epiphytes to multiply during the short periods of appropriate environment.

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Conclusion

Endophytes include fungi that have one or more of a variety of interactions with their host plant: some fungi are widespread and found on many different plant species; others are highly specific to single hosts in single environments. Further, a diverse array of interactions between plant and fungus have been found. Given that a huge array of fungi may be isolated from any one host, it seems plausible that endophytes will have one or more of a wide array of functions, most of which are unknown at present.

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References

Marquez LM, Redman RS, Rodriguez RJ and Roossinck MJ 2007 A virus in a fungus in a plant: three way symbiosis required for thermal tolerance. Science 315, 513-515.

Shoresh M, Harman GE and Mastouri F (2010) Induced resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology 48: 21 - 43.

van Bael et al. (2005) eds Dighton J, White JF & Oudemans P. The Fungal Community. Taylor & Francis.

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Is Alternaria a Latent Pathogen of Cotton?

Cotton in Australia is commonly colonised by Alternaria alternata and A. macrosporum. The fungi are among the first that can be isolated from emergent seedlings. The fungi can be readily isolated from leaf tissue for the rest of the growing season, and spores can be washed from the leaf surface. The leaf tissue may be heavily colonised. The fungi rarely cause serious disease. However, when concentration of K in the leaf tissue falls below adequate levels, a purple leaf spot develops which contains Alternaria. Purple leaf spot can be induced under experimental conditions of K deficiency, by inoculating otherwise healthy leaves with Alternaria. Other factors are also usually associated with development of the disease and causation is apparently multifactorial.

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