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Transmission electron microscope image of a cross section though a soybean (Glycine max.Essex) root nodule (endophyte. The bacteria, Bradyrhyzobium japonicum, infects the roots and establishes a nitrogen fixing symbiosis. This high magnification image shows part of a cell with single bacteriods (bacterium-like cell or modified bacterial cell) within their symbiosomes. In his image, you can also see endoplasmic reticulum, dictysome and cell wall.

An endophyte is an endosymbiont, often a bacterium or fungus, that lives within a plant for at least part of its life cycle without causing apparent disease. Endophytes are ubiquitous and have been found in all species of plants studied to date; however, most of the endophyte/plant relationships are not well understood. Some endophytes may enhance host growth, nutrient acquisition and improve the plant's ability to tolerate abiotic stresses, such as drought, and decrease biotic stresses by enhancing plant resistance to insects, pathogens and herbivores.

History

Endophytes were first described by the German botanist Johann Heinrich Friedrich Link in 1809. They were thought to be plant parasitic fungi and they were later termed as "microzymas" by the French scientist Béchamp. There was a belief that plants were healthy under sterile conditions and it was not until 1887 that Victor Galippe discovered bacteria normally occurring inside plant tissues.^[1]

Transmission

Endophytes may be transmitted either vertically (directly from parent to offspring) or horizontally (among individuals).^[2] Vertically transmitted fungal endophytes are typically considered clonal and transmit via fungal hyphae penetrating the embryo within the host’s seeds, while reproduction of the fungi through asexual conidia or sexual spores leads to horizontal transmission, where endophytes may spread between plants in a population or community.^[3]

Symbiosis

Most endophyte-plant relationships are still not well understood.^[4] Endophytes and plants often engage in mutualism, with endophytes primarily aiding in the health and survival of the host plant with issues such as pathogens and disease, water stress, heat stress, nutrient availability and poor soil quality, salinity, and herbivory.^[5] In exchange the endophyte receives carbon for energy from the plant host. Plant-microbe interactions are not strictly mutualistic, endophytic fungi can potentially become pathogens or saprotrophs. Endophytes may become active and reproduce under specific environmental conditions or when their host plants are stressed or begin to senesce, thereby limiting the amount of carbon provided to the endophyte.^[6][7]

Endophytes may benefit host plants by preventing other pathogenic or parasitic organisms from colonizing them. Endophytes can extensively colonize plant tissues and competitively exclude other potential pathogens.^[8][9] Some fungal and bacterial endophytes have proven to increase plant growth and improve overall plant hardiness.^[10]

Studies have shown that endophytic fungi grow in a very intimate interaction with their host plant cells. Fungal hyphae have been seen growing either flattened or wedged against plant cells. This growth pattern indicates that fungal hyphae are substantially attached to the plant host's cell wall, but do not invade plant cells.^[11] Endophytic fungal hyphae appear to grow at the same rate as their host leaves, within the intercellular spaces of the plant tisssue.^[12]

The presence of certain fungal endophytes in host meristems, leaves and reproductive structures has been shown to dramatically enhance the survival of their hosts. This enhanced survivability is largely attributed to endophytic production of secondary metabolites which protect against herbivory as well as increased uptake of nutrients.^[11] Studies have also shown that during experimental circumstances endophytes contribute significantly to plant growth and fitness under light-limited conditions, and plants appear to have increased reliance on their endophytic symbiont under these conditions.^[13]

There is evidence that plants and endophytes engage in communication with each other that can aid symbiosis. For example, plant chemical signals have been shown to activate gene expression in endophytes. One example of this plant-endosymbiont interaction occurs between dicotyledon plants, Convolvulaceae and clavicipitaceous fungi. When the fungus is in the plant it synthesizes ergoline alkaloids at a higher rate, compared to when it is grown apart from the plant. This supports the hypothesis that plant signaling is required in order to induce expression of endophytic secondary metabolites.^[14]

Diversity

Endophytic species are very diverse; only a small minority of existing endophytes have been characterized.^[15][16] Many endophytes are in the phylums Basidiomycota and Ascomycota. Endophytic fungi may be from Hypocreales and Xylariales of the Sordariomycetes (Pyrenomycetes) class or from the class of Loculoascomycetes.^[17] One group of fungal endophytes are the arbuscular mycorrhizal fungi involving biotrophic Glomeromycota associated with various plant species.^[18] As often with other organisms associated with plants such as mycorrhizal fungus, endophytes gain carbon from their association with the plant host. Bacterial endophytes are polyphyletic, belonging to broad range of taxa, including α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria, Firmicutes, Actinobacteria.^[19]

One or more endophytic organisms are found in nearly every land plant.^[20] It is suggested that areas of high plant diversity such as Tropical rainforests may also contain the highest diversity of endophytic organisms that possess novel and diverse chemical metabolites.^[21] It has been estimated that there could be approximately 1 million endophytic fungi that exist in the world.^[21]

Classification

Endophytes include a wide variety of microorganisms including fungi, bacteria and viruses. There are currently two different means of classifying endophytes.

Systemic and non-systemic

The first method divides endophytes into two categories: systemic (true) and nonsystemic (transient). These categories are based on the endophyte's genetics, biology and mechanism of transmission from host to host.^[22] Systemic endophytes are defined as organisms that live within plant tissues for the entirety of its life cycle and participate in a symbiotic relationship without causing disease or harm to the plant at any point. Additionally systemic endophytes concentrations and diversity do not change in a host with changing environmental conditions.^[22] Non-systemic or transient endophytes on the other hand vary in number and diversity within their plant hosts under changing environmental conditions. Non-systemic endophytes have also been shown to become pathogenic to their host plants under stressful or resource limited growing conditions.^[22]

Clavicipitaceous and non-clavicipitaceous

The second method divides fungal endophytes into four groups based on taxonomy and six other criteria: host range, host tissues colonized, in planta colonization, in planta biodiversity, mode of transmission and fitness benefits.^[23] These four groups are divided into clavicipitaceous endophytes (Class 1) and non-clavicipitaceous endophytes (Class 2, 3, and 4).

Class 1 endophytes are all phylogenetically related and proliferate within cool and warm season grasses. They typically colonize plant shoots where they form a systemic intercellular infection. Class 1 endophytes are mainly transmitted from host to host by vertical transmission, in which maternal plants pass fungi on to their offspring through seeds. Class 1 endophytes can further be divided into Types I, II and III. Among these three types of clavicipitaceous endophytes are different interactions with their plant hosts. These interaction range from pathogenic to symbiotic and symptomatic to asymptomatic. Type III clavicipitaceous endophytes grow within their plant host without manifesting symptoms of disease or harming their host. Class 1 endophytes typically confer benefits on their plant host such as improving plant biomass, increasing drought tolerance and increasing the production of chemicals that are toxic and unappetizing to animals, thereby decreasing herbivory. These benefits can vary depending on the host and environmental conditions.^[23]

Non-clavicipitaceous endophytes represent a polyphyletic group of organisms. Non-clavicipitaceous endophytes are typically Ascomycota fungi. The ecological roles of these fungi are diverse and still poorly understood. These endophyte plant interactions are widespread and have been found in nearly all land plants and ecosystems.^[23] Many non-clavicipitaceous endophytes have the ability to switch between endophytic behavior and free-living lifestyles. Non-clavicipitaceous endophytes are divided into class 2, 3 and 4. Class 2 endophytes can grow in plant tissues both above and below ground. This class of non-clavicipitaceous endophytes has been the most extensively researched and has been shown to enhance fitness benefits of their plant host as a result of habitat-specific stresses such as pH, temperature and salinity.^[23] Class 3 endophytes are restricted to growth in below ground plant tissues and form in localized areas of plant tissue. Class 4 endophytes are also restricted to plant tissues below ground but can colonize much more of the plant tissue. These classes of non-clavicipitaceous endophytes have not been as extensively studied to date.^[23]

Applications

Endophytes are an increasingly important area of research in many fields because of their chemical diversity and their ability to produce many novel secondary metabolites that can be utilized for fuel, medicine, restoration and agriculture. It is their chemical diversity that sparks profound interest in these organisms.^[24]

Biofuel

The main quality selected for use in biofuel is high productivity. Through the above benefits use of endophytes can potentially increase productivity and allow production to occur on land otherwise unsuitable.^[25]Inoculating plants with certain endophytes may provide increased disease or parasite resistance^[26] while others may possess metabolic processes that convert cellulose and other carbon sources into "myco-diesel" hydrocarbons and hydrocarbon derivatives.^[27] Common species used in biofuel in the US are Zea mays (corn), Salix species (poplars and willows), and sugarcane species.

Many endophytic fungi have been found that associate with algae. One of the endophytic fungi was found in Ecuador and appears to be closely related to Nigrograna mackinnonii. This fungus produces a variety of volatile organic compounds including terpenes and odd chain polyenes. The polyenes isolated from the fungus have properties that are sought in gasoline-surrogate biofuels.^[28]

Environmental remediation

In restoration ecology, endophytes can assist native species in outcompeting non-native invasive species and, colonizing barren land in secondary ecological succession, and restoring ecosystems degraded by pollutants. As with in biofuel production, in phytoremediation high productivity species are often used. Plants are able to contain, store, potentially break down, and stimulate microorganisms in the soil to break down certain pollutants.^[29] With phytoremediation the main challenge is the growth of plants in soil contaminated with organic pollutants and inorganic pollutants such as heavy metals. In this endophytes assist plants in converting pollutants into less biologically harmful forms such as breaking down TCE of PAHs in their metabolic pathways, and assist plants in tolerating higher levels of soil contamination with pollutants such as toluene.^[29]

The roots of plant communities to varying degrees help hold soil together by creating a network of roots that trap soil within. This in turn helps prevent soil erosion, stabilizes slopes and prevent landslides, helps prevent desertification in vulnerable areas, and controls pollution into waterways by acting as part of riparian buffers.^[30]

The endophyte Pestalotiopsis microspora isolated from stems of plants from the Ecuadorian Rainforest by Yale Researchers, was shown in laboratory experiments to be able to digest Polyurethane plastic as the fungus's sole carbon source. While other fungi have demonstrated the ability to remediate polyurethane plastic, the two isolates in this experiment were able to grow on this plastic in the absence of light or oxygen.^[31]

Drug discovery

Endophytes can produce a wide variety of compounds that might be useful as lead compounds in drug discovery.^[32][33] Certain fungal endophyte secondary metabolites have anti-fungal, anti-microbial, anti-viral, anti-oxidant, and anti-cancer properties; examples of this include taxol, torreyanic acid, exopolysaccharides, and solamargine.^[34] Manipulations of a plant's endosymbiots can also affect plant development, growth and ultimately the quality and quantity of compounds harvested from the plant.^[6]

It has been shown in studies the endophytic fungi are able to produce important secondary metabolites that were thought to only be manufactured by plants. The production of these metabolites in plants could either be produced solely by endophytes or have been transferred to or from the host plant genome.^[35]

Endophytes produce many secondary metabolites. Over the years there has been increasing importance placed on the discovery of endophytes natural products, also referred to as bioprospecting. Many of these novel compounds produced by endophytes have been shown to have important medical applications such as antimicrobial, antiparasitic, cytotoxic, neuroprotective, antioxidant, insulin mimetic and immunosuppresant properties.^[35]

A well known example of the discovery of chemicals derived from endophytic fungi is from the fungus Taxomyces andreanae isolated from the pacific yew Taxus brevifolia. T. andreanae produces Paclitaxel also known as Taxol. This drug is important for the treatment of cancer. Other endophytes since have been discovered that also produce paclitaxel in other host species, but to date there has been no successful industrial source of paclitaxel created.^[35]

Many endophytes have been discovered with various anti-tumor properties. Endophytic fungi produce many secondary compounds such as alkaloids, triterpenes and steroids which have been shown to have anti tumor effects. The alkaloid beauvericin has been isolated from the fungus Fusarium oxysporum and has shown cytotoxicity against the tumor cells PC3, PANC-1, and A549.^[36][37] Three triterpenes were found in the endophyte Xylarialean sp., all three of these compounds displayed mild cytotoxic effects on tumor cells.^[37]

Some of the antimicrobial compounds produced by endophytic fungi are of interest in their effectiveness against pathogens which have developed resistances to antibiotics. Several isolates from the ascomycota Pestalotiopsis sp have been shown to have a broad range of antimicrobial effects,^[21] even against methicillin-resistant Staphylococcus aureus.^[38] Isolates from the marine fungus Nigrospora sp. have proved to be more effective in treating multi drug-resistant tuberculosis than current treatments.^[39]

A endophytic fungus from the species pseudomassaria has been found in the rainforest of the Democratic Republic of the Congo. This fungus yields a fungal metabolite that shows potential as an antidiabetic medicine, also known as an insulin mimetic. This compound acts like insulin and has been shown to significantly lower blood glucose levels in mouse model experiments.^[20]

Agriculture

Among the many promising applications of endophytic microbes are those intended to increase agricultural use of endophytes to produce crops that grow faster and are more resistant and hardier than crops lacking endophytes.^[40]Epichloë endophytes are being widely used commercially in turf grasses to enhance the performance of the turf and its resistance to biotic and abiotic stresses.^[41]Piriformospora indica is an interesting endophytic fungus of the order Sebacinales, the fungus is capable of colonising roots and forming symbiotic relationship with many plants.^[42]

Endophytes appear to enhance the growth of their plant host symbionts. Endophytes also provide their hosts with an increased resilience to both abiotic and biotic stressors such as drought, poor soils and herbivory. The increased growth and resilience is likely causes by the endophytes ability to improve plant nutrition or secondary metabolite production, as in the case of Phoma eupatorii's inhibition of the phytopathogen Phytophthora infestans.^[43] Endophytes accomplish this by increasing the uptake of valuable land limited nutrients from the soil such as phosphorus and making other plant nutrients available to plants such as rock phosphate and atmospheric nitrogen which are normally trapped informs that are inaccessible to plants.^[24]

Many endophytes protect plants from herbivory from both insects and animals by producing secondary metabolites that are either unappetizing or toxic to the herbivore. Increasingly there has been great importance placed on endophytes that protect valuable crops from invasive insects. One example of an endophyte-plant-insect interaction is located in the New Zealand grasslands, where endophytes, known as AR1 and AR37 are utilized to protect valuable ryegrass from the Argentine stem weevil but remain palatable to another important food source, livestock.^[44]

There are several endophytes that have been discovered that exhibit insecticidal properties. One such endophyte comes from the Nodulisporium sp. which was first harvested from the plant Bontia daphnoides. Indole diterpenes, known as nodulisporic acids, have been harvested from this endophyte which have effective insecticidal properties against the blowfly larvae.^[20]

There are many obstacles to successfully implementing the use of endophytes in agriculture. Despite the many known benefits that endophytes may confer to their plant hosts, conventional agricultural practices continue to take priority. Current agriculture relies heavily on fungicides and high levels of chemical fertilizers. The use of fungicides has a negative effect on endophytic fungi and fertilizers reduce a plant's dependence on its endophytic symbiont.^[44] Despite this, the interest and use of bio-insecticides and using endophytes to aid in plant growth is increasing as organic and sustainable agriculture is considered more important. As humans become more aware of the damage that synthetic insecticides cause to the environment and beneficial insects such as bees and butterflies biological insecticides may become more important to the agricultural industry.^[20]

See also

• Biofertilizer


• List of endophytes


• Plant use of endophytic fungi in defense


• Arbuscular mycorrhiza


• Mycorrhiza


• Rhizobia

References