Plant use of endophytic fungi in defense
Plant use of endophytic fungi in defense occurs when endophytic fungi, which live symbiotically with the majority of plants by entering their cells, are utilized as an indirect defense against herbivores. In exchange for carbohydrate energy resources, the fungus provides benefits to the plant which can include increased water or nutrient uptake and protection from phytophagous insects, birds or mammals. Once associated, the fungi alter nutrient content of the plant and enhance or begin production of secondary metabolites. The change in chemical composition acts to deter herbivory by insects, grazing by ungulates and/or oviposition by adult insects. Endophyte-mediated defense can also be effective against pathogens and non-herbivory damage.
This differs from other forms of indirect defense in that the fungi live within the plant cells and directly alter their physiology. In contrast, other biotic defenses such as predators or parasites of the herbivores consuming a plant are normally attracted by volatile organic compounds (known as semiochemicals) released following damage or by food rewards and shelter produced by the plant. These defenders vary in the time spent with the plant: from long enough to oviposit to remaining there for numerous generations, as in the ant-acacia mutualism. Endophytic fungi tend to live with the plant over its entire life.
- 1 Diversity of endophytic associations
- 2 Mechanisms of defense
- 3 Impacts on host plants
- 4 History of research
- 5 Importance to humans
- 6 See also
- 7 References
- 8 Further References
- 9 External links
Diversity of endophytic associations
The fungal endophytes are a diverse group of organisms forming associations almost ubiquitously throughout the plant kingdom. The endophytes which provide indirect defense against herbivores may have come from a number of origins, including mutualistic root endophyte associations and the evolution of entomopathogenic fungi into plant-associated endophytes. The endomycorrhiza, which live in plant roots, are made up of five groups: arbuscular, arbutoid, ericoid, monotropoid, and orchid mycorrhizae. The majority of species are from the phylum Glomeromycota with the ericoid species coming from the Ascomycota, while the arbutoid, monotropoid and orchid mycorrhizae are classified as Basidiomycota. The entomopathogenic view has gained support from observations of increased fungal growth in response to induced plant defenses and colonization of plant tissues.
Examples of host specialists are numerous – especially in temperate environments – with multiple specialist fungi frequently infecting one plant individual simultaneously. These specialists demonstrate high levels of specificity for their host species and may form physiologically adapted host-races on closely related congeners. Piriformospora indica is an interesting endophytic fungus of the order Sebacinales, the fungus is capable of colonising roots and forming symbiotic relationship with every possible plant on earth . P. indica has also been shown to increase both crop yield and plant defence of a variety of crops(barley, tomato, maize etc.) against root-pathogens. However, there are also many examples of generalist fungi which may occur on different hosts at different frequencies (e.g. Acremonium endophytes from five subgenera of Festuca) and as part of a variety of fungal assemblages. They may even spread to novel, introduced plant species. Endophytic mutualists associate with species representative of every growth form and life history strategy in the grasses and many other groups of plants. The effects of associating with multiple strains or species of fungus at once can vary, but in general, one type of fungus will be providing the majority of benefit to the plant.
Mechanisms of defense
Secondary metabolite production
Some chemical defenses once thought to be produced by the plant have since been shown to be synthesized by endophytic fungi. The chemical basis of insect resistance in endophyte-plant defense mutualisms has been most extensively studied in the perennial ryegrass and three major classes of secondary metabolites are found: indole diterpenes, ergot alkaloids and peramine. Related compounds are found across the range of endophytic fungal associations with plants. The terpenes and alkaloids are inducible defenses which act similarly to defensive compounds produced by plants and are highly toxic to a wide variety of phytophagous insects as well as mammalian herbivores. Peramine occurs widely in endophyte-associated grasses and may also act as a signal to invertebrate herbivores of the presence of more dangerous defensive chemicals. Terpenoids and ketones have been linked to protection from specialist and generalist herbivores (both insect and vertebrate) across the higher plants.
Generalist herbivores are more likely than specialists to be negatively affected by the defense chemicals that endophytes produce because they have, on average, less resistance to these specific, qualitative defenses. Among the chewing insects, infection by mycorrhizae can actually benefit specialist feeders even if it negatively affects generalists. The overall pattern of effects on insect herbivores seems to support this, with generalist mesophyll feeders experiencing negative effects of host infection, although phloem feeders appear to be affected little by fungal defenses.
Secondary metabolites may also affect the behaviour of natural enemies of herbivorous species in a multi-trophic defense/predation association. For instance, terpenoid production attracts natural enemies of herbivores to damaged plants. These enemies can reduce numbers of invertebrate herbivores substantially and may not be attracted in the absence of endophytic symbionts. Multi-trophic interactions can have cascading consequences for the entire plant community, with the potential to vary widely depending on the combination of fungal species infecting a given plant and the abiotic conditions.
Altered nutrient content
Due to the inherently nutrient-exchange based economy of the plant-endophyte association, it is not surprising that infection by fungi directly alters the chemical composition of plants, with corresponding impacts on their herbivores. Endophytes frequently increase apoplastic carbohydrate concentration, altering the C:N ratio of leaves and making them a less efficient source of protein. This effect can be compounded when the fungus also uses plant nitrogen to form N-based secondary metabolites such as alkaloids. For example, the thistle gall fly (Urophora cardui) experiences reduced performance on plants infected with endophytic fungi due to the decrease in N-content and ability to produce large quantities of high-quality gall tissue. Additionally, increased availability of limiting nutrients to plants improves overall performance and health, potentially increasing the ability of infected plants to defend themselves.
Impacts on host plants
Studies of fungal infection consistently reveal that plants with endophytes are less likely to suffer substantial damage, and herbivores feeding on infected plants are less productive. There are multiple modes through which endophytic fungi reduce insect herbivore damage, including avoidance (deterrence), reduced feeding, reduced development rate, reduced growth and/or population growth, reduced survival and reduced oviposition. Vertebrate herbivores such as birds, rabbits and deer show the same patterns of avoidance and reduced performance. Even below-ground herbivores such as nematodes and root-feeding insects are reduced by endophyte infection. The strongest evidence for anti-herbivore benefits of fungal endophytes come from studies of herbivore populations being extirpated when allowed to feed only on infected plants. Examples of local extinction have been documented in crickets, larval armyworms and flour beetles.
Yet chemical defenses produced by fungal endophytes are not universally effective, and numerous insect herbivores are unaffected by a given compound at one or more life history stages; larval stages are often more susceptible to toxins than adults. Even endophytes which purportedly provide some defense benefit to their hosts such as the Neotyphidium partner of many grass species in the alpine tundra do not always lead to avoidance or ill-effects on herbivores due to spatial variation in levels of consumption.
Not all endophytic symbioses confer protection from herbivores – only some species associations act as defense mutualisms. The difference between a mutualistic endophyte and a pathogenic one can be indistinct and dependent on interactions with other species or environmental conditions. Some fungi which are pathogens in the absence of herbivores may become beneficial under high levels of insect damage, such as species which kill plant cells in order to make nutrients available for their own growth, thereby altering nutritional content of leaves and making them a less desirable foodstuff. Some endomycorrhizae may provide defense benefits but at the cost of lost reproductive potential by rendering grasses partially sterile with their own fungal reproductive structures taking precedence. This is not unusual among fungi, as non-endophytic plant pathogens have similar conditionally beneficial effects on defense. Some species of endophyte may be beneficial for the plants in other ways (e.g. nutrient and water uptake) but will provide less benefit as a plant receives more damage and not produce defensive chemicals in response. The effect of one fungus on the plant can be altered when multiple strains of fungi are infecting a given individual in combination.
Some endomycorrhizae may actually promote herbivore damage by making plants more susceptible to it. For example, some oak fungal endophytes are positively correlated with the levels of damage from leaf miners (Cameraria spp.), although negatively correlated with number of larvae present due to a reduction of oviposition on infected plants, which partially mitigates the higher damage rate. This continuum between mutualism and pathogenicity of endophytic fungi has major implications for plant fitness depending on the species of partners available in a given environment; mutualist status is conditional in a way similar to pollination and can shift from one to the other just as frequently.
Fitness and competitive ability
Fungal endophytes which provide defensive services to their host plants may exert selective pressures favouring association through enhanced fitness relative to uninfected hosts. The fungus Neotyphodium spp. infects grasses and increases fitness under conditions with high levels of interspecific competition. It does this through a combination of benefits including anti-herbivore defenses and growth promoting factors. The customary assumption that plant growth promotion is the main way fungal mutualists improve fitness under attack from herbivores is changing; alteration of plant chemical composition and induced resistance are now recognized as factors of great importance in improving competitive ability and fecundity. Plants undefended by chemical or physical means at certain points in their life histories have higher survival rates when infected with beneficial endophytic fungi. The general trend of plants infected with mutualistic fungi outperforming uninfected plants under moderate to high herbivory exerts selection for higher levels of fungal association as herbivory levels increase. Unsurprisingly, low to moderate levels of herbivore damage also increases the levels of infection by beneficial endophytic fungi.
In some cases the symbiosis between fungus and plant reaches a point of inseparability; fungal material is transmitted vertically from the maternal parent plant to seeds, forming a near-obligate mutualism. Because seeds are an important aspect of both fecundity and competitive ability for plants, high germination rates and seedling survival increase lifetime fitness. When fitness of plant and fungus become tightly intertwined, it is in the best interest of the endophyte to act in a manner beneficial to the plant, pushing it further toward the mutualism end of the continuum. Such effects of seed defense can also occur in dense stands of conspecifics through horizontal transmission of beneficial fungi. Mechanisms of microbial association defense, protecting the seeds rather than the already established plants, can have such drastic impacts on seed survival that they have been recognized to be an important aspect of the larger ‘seed defence theory’.
The range of associated plants and fungi may be altered as climate changes, and not necessarily in a synchronous fashion. Plants may lose or gain endophytes, with as yet unknown impacts on defense and fitness, although generalist species may provide indirect defense in new habitats more often than not. Above-ground and below-ground associations can be mutual drivers of diversity, so altering the interactions between plants and their fungi may also have drastic effects on the community at large, including herbivores. Changes in distribution may bring plants into competition with previously established local species, making the fungal community – and particularly the pathogenic role of fungus – important in determining outcomes of competition with non-native invasive species. As carbon dioxide levels rise, the amplified photosynthesis will increase the pool of carbohydrates available to endophytic partners, potentially altering the strength of associations. Infected C3 plants show greater relative growth rate under high CO2 conditions compared to uninfected plants, and it is possible that the fungi drive this pattern of increased carbohydrate production.
Levels of herbivory may also increase as temperature and carbon dioxide concentrations rise. However, should plants remain associated with their current symbiotic fungi, evidence suggests that the degree of defense afforded them should not be altered. Although the amount of damage caused by herbivores frequently increases under elevated levels of atmospheric CO2, the proportion of damage remains constant when host plants are infected by their fungal endophytes. The change in Carbon-Nitrogen ratio will also have important consequences for herbivores. As carbohydrate levels increase within plants, relative nitrogen content will fall, having the dual effects of reducing nutritional benefit per unit biomass and also lowering concentrations of nitrogen-based defenses such as alkaloids.
History of research
The effects of endophytic fungi on the chemical composition of plants have been known by humans for centuries in the form of poisoning and disease as well as medicinal uses. Especially noted were impacts on agricultural products and livestock. Recognition and study of the mutualism did not begin in earnest until the 1980s when early studies on the impacts of alkaloids on animal herbivory confirmed their importance as agents of deterrence. Biologists began to characterize the diversity of endophytic mutualists through primitive techniques such as isozyme analysis and measuring the effects of infection on herbivores. Basic descriptive accounts of these previously neglected species of fungus became a major goal for mycologists, and a lot of research focus shifted to associates of the grass family (Poaceae) in particular, because of the large number of species which represent economically important commodities to humans.
Recent advances and future directions
In addition to continuing descriptive studies of the effects of infection by defense mutualist endophytes, there has been a sharp increase in the number of studies which delve further into the ecology of plant-fungus associations and especially their multi-trophic impacts. The processes by which endophytic fungi alter plant physiology and volatile chemical levels are virtually unknown, and limited current results show a lack of consistency under differing environmental conditions, especially differing levels of herbivory. Studies comparing the relative impacts of mutualistic endophytes on inducible defenses and tolerance show a central function of infection in determining both responses to herbivore damage. On the whole, molecular mechanisms behind endophyte-mediated plant defense has been an increasing focus of research over the past ten years.
Since the beginning of the biotechnology revolution, much research has been also focused on using genetically modified endophytes to improve plant yields and defensive properties. The genetic basis of response to herbivory is being explored in tall fescue, where it appears the production of jasmonic acid may play a role in downregulation of the host plant’s chemical defense pathways when a fungal endophyte is present. In some cases, fungi that are closely associated with their hosts have transferred genes for secondary metabolite production to the host genome, which could help to explain multiple origins of chemical defenses within the phylogeny of various groups of plants. This represents an important line of inquiry to pursue, especially in regards to understanding the chemical pathways that can be utilized in biotechnological applications.
Importance to humans
Agriculture and livestock
The secondary chemicals produced by endophytic fungi when associated with their host plants can be very harmful to mammals including livestock and humans, causing more than 600 million dollars in losses due to dead livestock every year. For example, the ergot alkaloids produced by Claviceps spp. have been dangerous contaminants of rye crops for centuries. When not lethal, defense chemicals produced by fungal endophytes may lead to lower productivity in cows and other livestock feeding on infected forage. Reduced nutritional quality of infected plant tissue also lowers the performance of farm animals, compounding the effect of reduced feed uptake when provided with infected plant matter. Reduced frequency of pregnancy and birth has also been reported in cattle and horses fed with infected forage. Consequently, the dairy and meat-production industries must endure substantial economic losses.
Fungal resistance to herbivores represents an environmentally sustainable alternative to pesticides that has experienced reasonable success in agricultural applications. The organic farming industry has embraced mycorrhizal symbionts as one tool for improving yields and protecting plants from damage. Infected crops of soybean, ribwort plantain, cabbage, banana, coffee bean plant and tomato all show markedly lower rates of herbivore damage compared to uninfected plants. Endophytic fungi show great promise as a means of indirect biocontrol in large-scale agricultural applications. The potential for biotechnology to improve crop populations through inoculation with modified fungal strains could reduce toxicity to livestock and improve yields of human-consumed foods. The endophyte, either with detrimental genes removed or beneficial new genes added, is used as a surrogate host to transform the crops genetically. An endophyte of ryegrass has been genetically transformed in this way and used successfully to deter herbivores.
Understanding how to mediate top-down effects on crop populations caused by the enemies of herbivores as well as bottom-up effects of chemical composition in infected plants has important consequences for the management of agricultural industries. The selection of endophytes for agricultural use must be careful and consideration must be paid to the specific impacts of infection on all species of pest and predators or parasites, which may vary on a geographic scale. The union of ecological and molecular techniques to increase yield without sacrificing the health of the local or global environment is a growing area of research.
Many secondary metabolites from endophyte-plant interactions have also been isolated and used in raw or derived forms to produce a variety of drugs treating many conditions. The toxic properties of ergot alkaloids also make them useful in the treatment of headaches and throughout the process of giving birth by inducing contractions and stemming hemorrhages. Drugs used to treat Parkinson's Disease have been created from isolates of ergot toxins, although health risks may accompany their use. Ergotamine has also been used to synthesize lysergic acid diethylamide because of its chemical similarity to lysergic acid. The generally chemically-based defense properties of endophytic fungi make them a perfect group of organisms to search for new antibiotic compounds within, as other fungi have in the past yielded such useful drugs as penicillin and streptomycin and plants use their antibiotic qualities as a defense against pathogens.
- Plant defense against herbivory
- Arbuscular mycorrhiza
- Interspecies communication
- Chemical ecology
- Strauss, S.Y. & Zangerl, A.R. (2003). Plant-insect interactions in terrestrial ecosystems. In: Plant-animal interactions: an evolutionary approach (Herrera, C.M. & Pellmyr, O., Eds.). Malden: Blackwell Publishing. pp. 77-106. ISBN 978-0-632-05267-7
- Wang, B.; Qiu, Y.L. (2006). "Phylogenetic distribution and evolution of mycorrhizae in land plants". Mycorrhiza. 16 (5): 299–363. doi:10.1007/s00572-005-0033-6. PMID 16845554.
- Lekberg, Y.; Koide, R. T. (2005). "Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A metaanalysis of studies published between 1988 and 2003". New Phytol. 168 (1): 189–204. doi:10.1111/j.1469-8137.2005.01490.x. PMID 16159333.
- Dighton, J. (2003). Fungi in Ecosystem Processes. New York: Marcel Dekker. ISBN 978-0-8247-4244-7
- Clay, K. (1990). "Fungal endophytes of grasses". Annu. Rev. Ecol. Syst. 21: 275–297. doi:10.1146/annurev.es.21.110190.001423.
- Arnold, A.E.; Mejia, L.C.; Kyllo, D.; Rojas, E.I.; Maynard, Z.; Robbins, N.; Herre, E.A. (2003). "Fungal endophytes limit pathogen damage in a tropical tree". Proc. Natl. Acad. Sci. U.S.A. 100 (26): 15649–15654. doi:10.1073/pnas.2533483100. PMC . PMID 14671327.
- Thaler J (1999). "Jasmonate-inducible plant defences cause increased parasitism of herbivores". Nature. 399 (6737): 686–688. doi:10.1038/21420.
- Janzen, D. H. (1966). "Coevolution of mutualism between ants and acacias in Central America". Evolution. 20 (3): 249–275. doi:10.2307/2406628.
- Vega, F.E.; Posada, F.; Aime, M.C.; Pava-Ripoll, M.; Infante, F.; Rehner, S.A. (2008). "Entomopathogenic fungal endophytes". Biological Control. 46: 72–82. doi:10.1016/j.biocontrol.2008.01.008.
- Peterson, R.L.; Massicotte, H.B. & Melville, L.H. (2004). Mycorrhizas: anatomy and cell biology. National Research Council Research Press. ISBN 978-0-660-19087-7.
- Baverstock, J; Elliot, S.L.; Alderson, P.G.; Pell, J.K. (2005). "Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles". Journal of Invertebrate Pathology. 89 (2): 157–164. doi:10.1016/j.jip.2005.05.006. PMID 16005016.
- Gómez-Vidal, S.; Salinas, J.; Tena, M.; Lopez-Llorca, L.V. (2009). "Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi". Electrophoresis. 30 (17): 2996–3005. doi:10.1002/elps.200900192. PMID 19676091.
- Arnold, A.E.; Lutzoni, F. (2007). "Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots?". Ecology. 88 (3): 541–549. doi:10.1890/05-1459. PMID 17503580.
- Leuchtmann, A. (1992). "Systematics, distribution and host specificity of grass endophytes". Nat. Toxins. 1 (3): 150–162. doi:10.1002/nt.2620010303. PMID 1344916.
- Leuchtmann, A.; Clay, K. (1990). "Isozyme variation in the Acremonium/Epichloe fungal endophyte complex". Phytopathology. 80 (10): 1133–1139. doi:10.1094/Phyto-80-1133.
- Varma, Ajit; Verma S., Sudha, Nirmal S., Bütehorn B., Franken P. (23 December 1998). "Piriformospora indica, a Cultivable Plant-Growth-Promoting Root Endophyte". Applied and Environmental Microbiology. 65 (6): 2741–2744. PMC . PMID 10347070. Cite uses deprecated parameter
- Kogel, Karl-Heinz; Frank Waller,*† Beate Achatz,*†‡Baltruschat H., Fodor J., Becker K., Fischer M., Heier T., Hückelhoven R., Neumann C.,Wettstein D. V.,Franken P. (20 September 2005). "The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield". Proc. Natl. Acad. Sci. U.S.A. 102 (38): 13386–13391. doi:10.1073/pnas.0504423102. PMC . PMID 16174735. Cite uses deprecated parameter
- Leuchtmann, A. (1988). "Isozyme relationships of Acremonium endophytes from twelve Festuca species". Mycol. Res. 98: 25–33. doi:10.1016/s0953-7562(09)80331-6.
- Kluger, C.G.; Dalling, J.W.; Gallery, R.E.; Sanchez, E.; Weeks-Galindo, C.; Arnold, A.E. (2008). "Prevalent host-generalism among fungi associated with the seeds of four neotropical pioneer species". Journal of Tropical Ecology. 24: 332–351. doi:10.1017/s0266467408005026.
- Leuchtmann, A.; Clay, K. (1989). "Isozyme variation in the fungus Atkinsonella hypoxylon within and among populations of its host grasses". Can. J. Bot. 67 (9): 2600–2607. doi:10.1139/b89-336.
- Rykard, D.M.; Bacon, C.W.; Luttrell, E.S. (1985). "Host relations of Myriogenospora atramentosa and Balansia epichloe (Clavicipitaceae)". Phytopathology. 75 (8): 950–956. doi:10.1094/Phyto-75-950.
- Clay, K. (1988). Claviciptaceous fungal endophytes of grasses: coevolution and the change from parasitism to mutualism. In: Coevolution of Fungi with Plants and Animals (Hawksworth, D. & Pirozynski, K., eds.). London: Academic Press.
- Vicari, M.; Hatcher, P.E.; Ayres, P.G. (2002). "Combined effect of foliar and mycorrhizal endophytes on an insect herbivore". Ecology. 83 (9): 2452–2464. doi:10.1890/0012-9658(2002)083[2452:CEOFAM]2.0.CO;2. ISSN 0012-9658.
- Klironomos, J. (2008). "Variation in plant response to native and exotic arbuscular mycorrhizal fungi". Ecology. 84 (9): 2292–2301. doi:10.1890/02-0413.
- Betina, V. (1984). Indole derived tremorgenic toxins. In: Mycotoxins Production, Isolation, Separation and Purification (Betina, V., ed.). Developments in Food Science, Vol. 8. New York: Elsivier.
- Rutschmann, J. & Stadler, P.A. (1978). Chemical background. In: Ergot Alkaloids and Related Compounds (Berde, B. & Schild, H.O., eds.) Berlin: Springer-Verlag.
- Rowan, D.D.; Hunt, M.B.; Gaynor, D.L. (1986). "Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae". J. Chem. Soc. Chem. Commun. 1986: 935–936. doi:10.1039/c39860000935.
- Zhang, D.X.; Nagabhyru, P.; Schardl, C.L. (2009). "Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants". Plant Physiology. 150 (2): 1072–1082. doi:10.1104/pp.109.138222. PMC . PMID 19403726.
- Popay, A.J.; Prestidge, R.A.; Rowan, D.D. & Dymock, J.J. (1990). The role of Acremonia lolli mycotoxins in insect resistance of perennial ryegrass (Lolium perenne). In: Proc. 1st Int. Symp. Acremonium/Grass interactions (Quisenberry, S.S. & Joost, R.E., eds.) Baton Rouge: Louisiana Agriculture Experiment Station.
- Clay, K.; Cheplick, G.P. (1989). "Effect of ergot alkaloids from fungal endophyt-infected grasses on fall armyworm (Spodoptera frugiperda)". J. Chem. Ecol. 15: 169–182. doi:10.1007/BF02027781.
- Patterson, C.G.; Potter, D.A.; Fannin, F.F. (1991). "Feeding deterrency of alkaloids from endophyte-infected grasses to Japanese beetle grubs". Entomol. Exp. Appl. 61 (3): 285–289. doi:10.1111/j.1570-7458.1991.tb01561.x.
- Prestidge, R.A. & Ball, O.J.-P. (1997). A catch 22: the utilization of endophytic fungi for pest management. In: Multitrophic Interactions in Terrestrial Systems (Gange, A.C. & Brown, V.K., eds.). Oxford: Blackwell Scientific. pp. 171-192. ISBN 978-0-521-83995-2
- Rowan, D.D.; Dymock, J.J.; Brimble, M.A. (1990). "Effect of fungal metabolite peramine and analogs on feeding and development of Argentine stem weevil (Listronotus bonariensis)". J. Chem. Ecol. 16 (5): 1683–1695. doi:10.1007/BF01014100.
- Akiyama, K.; Hayashi, H. (2001). "Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots". Biosci. Biotech. Biochem. 66: 762–769. doi:10.1271/bbb.66.762.
- Rapparini, F.; Llusia, J.; Penuelas, J. (2008). "Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L". Plant Biol. 10 (1): 108–122. doi:10.1055/s-2007-964963. PMID 18211551.
- Smith, S.E. & Read, D.J. (2008). Mycorrhizal symbiosis. (3rd ed.) London: Academic Press. ISBN 978-0-12-370526-6
- Koricheva, J.; Gange, A.C.; Jones, T. (2009). "Effects of mycorrhizal fungi on insect herbivores: a meta-analysis". Ecology. 90 (8): 2088–2097. doi:10.1890/08-1555.1. PMID 19739371.
- Gehring, C.; Bennett, A. (2009). "Mycorrhizal fungal-plant-insect interactions: the importance of a community approach". Environ. Entomol. 38 (1): 93–102. doi:10.1603/022.038.0111. PMID 19791601.
- Langenheim, J.H. (1994). "Higher-plant terpenoids – a phytocentric view of their ecological roles". J. Chem. Ecol. 20 (6): 1223–1280. doi:10.1007/BF02059809.
- Kagata, H.; Ohgushi, T. (2006). "Bottom-up trophic cascades and material transfer in terrestrial food webs". Ecol. Res. 21: 26–34. doi:10.1007/s11284-005-0124-z.
- Pineda, A.; Zheng, S.J.; van Loon, J.J.A.; Pieterse, C.M.J.; Dicke, M. (2010). "Helping plants to deal with insects: the role of beneficial soil-borne microbes". Trends in Plant Science. 15 (9): 507–514. doi:10.1016/j.tplants.2010.05.007. PMID 20542720.
- Gange, A.C.; Brown, V.K.; Aplin, D.M. (2003). "Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids". Ecol. Lett. 6 (12): 1051–1055. doi:10.1046/j.1461-0248.2003.00540.x.
- Valenzuela-Soto, J.H.; Estrada-Hernandez, M.G.; Ibarra-Laclette, E.; Delano-Frier, J.P. (2010). "Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development". Planta. 231 (2): 397–410. doi:10.1007/s00425-009-1061-9. PMID 20041333.
- Richardson, M.D. (2000). Alkaloids of endophyte-infected grasses: defense chemicals or biological anomalies? In: Microbial Endophytes (Bacon, C.W.; White, J.F., eds.). New York: Marcel Dekker. pp. 323-340. ISBN 0-8247-8831-1
- Gange, A.C.; Nice, H.E. (1997). "Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization". New Phytologist. 137 (2): 335–343. doi:10.1046/j.1469-8137.1997.00813.x.
- Gosling, P.; Hodge, A.; Goodlass, G.; Bending, G.D. (2006). "Arbuscular mycorrhizal fungi and organic farming". Agric. Ecosyst. Environ. 113: 17–35. doi:10.1016/j.agee.2005.09.009.
- Latch, G.C.M. (1993). "Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes". Agric. Ecosyt. Environ. 44: 143–156. doi:10.1016/0167-8809(93)90043-O.
- Schmidt, S.P.; Osborn, T.G. (1993). "Effects of endophyte-infected tall fescue on animal performance". Agric. Ecosyt. Environ. 44: 233–262. doi:10.1016/0167-8809(93)90049-U.
- Latch, G.C.M.; Christensen, M.J.; Gaynor, D.L. (1985). "Aphid detection of endophytic infection in tall fescue". N.Z. J. Agric. Res. 28: 129–132. doi:10.1080/00288233.1985.10427006.
- Knoch, T.R.; Faeth, S.H. & Arnott, D.S. (1993). Fungal endophytes: plant mutualists via seed predation and germination. Bull. Ecol. Soc. Am. 74(Abstr.): 313.
- Lacey, L.A.; Neven, L.G. (2006). "The potential of the fungus, Muscodor albus, as a microbial control agent of potato tuber moth (Lepidoptera: Gelechiidae) in stored potatoes". J. Invertebr. Pathol. 91 (3): 195–198. doi:10.1016/j.jip.2006.01.002. PMID 16494898.
- Madej, C.W.; Clay, K. (1991). "Avian seed preference and weight loss experiments: the role of fungal endophyte-infected tall fescue seeds". Oecologia. 88 (2): 296–302. doi:10.1007/BF00320825.
- Sadler, K. (1980). Of rabbits and habitat, a long term look. Missouri Conservationist March: 4-7.
- Mackintosh, C.G.; Orr, M.B.; Gallagher, R.T.; Harvey, I.C. (1982). "Ryegrass staggers in Canadian wapiti deer". N.Z. Vet. J. 36: 106–107.
- West, C.P.; Izekor, E.; Oosterhuis, D.M.; Robbins, R.T. (1988). "The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue". Plant Soil. 112: 3–6. doi:10.1007/BF02181745.
- Clay, K. (1991). Fungal endophytes, grasses, and herbivores. In: Microbial mediation of plant-herbivore interactions (Barbosa, P.; Krischik, V.A. & Jones, C.G., eds.) New York: John Wiley and Sons. pp. 199-226. ISBN 978-0-471-61324-4
- Newsham, K.K.; Fitter, A.H.; Watkinson, A.R. (1995). "Arbuscular mycorrhizae protect an annual grass from root pathogenic fungi in the field". Journal of Ecology. 83 (6): 991–1000. doi:10.2307/2261180.
- Gange, A.C. (2000). "Arbuscular mycorrhizal fungi, Collembola and plant growth". Trends in Ecology and Evolution. 15 (9): 369–372. doi:10.1016/S0169-5347(00)01940-6. PMID 10931669.
- Ahmad, S.; Govindarajan, S.; Funk, C.R.; Johnson-Cicalese, J.M. (1985). "Fatality of house crickets on perennial ryegrass infected with fungal endophyte". Entomol. Exp. Appl. 39 (2): 183–190. doi:10.1111/j.1570-7458.1985.tb03561.x.
- Cheplick, G.P.; Clay, K. (1988). "Acquired chemical defenses of grasses: the role of fungal endophytes". Oikos. 52 (3): 309–318. doi:10.2307/3565204.
- Lewis, G.C.; Clements, R.O. (1986). "A survey of ryegrass endophyte (Acremonium loliae) in the U.K. and its apparent ineffectuality on a seedling pest. J. Agric". Sci. 107: 633–638. doi:10.1017/s002185960006980x.
- Hardy, T.N.; Clay, K.; Hammond, A.M. Jr (1986). "Leaf age and related factors affecting endophyte-mediated resistance to fall armyworm (Lepidoptera: Noctuidae) in tall fescue". Environ. Entomol. 15: 1083–1089.
- Kindler, S.D.; Breen, J.P.; Springer, T.L. (1991). "Reproduction and damage by Russian wheat aphid (Homoptera:Aphididae) as influenced by fungal endophytes and cool-season turfgrasses". J. Econ. Entomol. 84: 685–692.
- Koh, S.; Hik, D.S. (2007). "Herbivory mediates grass-endophyte relationships". Ecology. 88 (11): 2752–2757. doi:10.1890/06-1958.1. PMID 18051643.
- Tibbets, T.M.; Faeth, S.H. (1999). "Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants?". Oecologia. 118 (3): 297–305. doi:10.1007/s004420050730.
- Clay, K.; Cheplick, G.P.; Marks, S. (1989). "Impact of the fungus Balansia henningsiana on Panicum agrostoides: frequency of infection, plant growth and reproduction, and resistance to pests". Oecologia. 80 (3): 374–380. doi:10.1007/BF00379039.
- Kruess, A. (2002). "Indirect interaction between a fungal plant pathogen and a herbivorous beetle of the weed Cirsum aravense". Oecologia. 130 (4): 563–569. doi:10.1007/s00442-001-0829-9.
- Gehring, C.A.; Whitham, T.G. (1994). "Interactions between aboveground herbivores and the mycorrhizal mutualists of plants". Trends in Ecology & Evolution. 9 (7): 251–255. doi:10.1016/0169-5347(94)90290-9.
- Fitter, A.H.; Garbaye, J. (1994). "Interactions between mycorrhizal fungi and other soil organisms". Plant and Soil. 159 (1): 123–132. doi:10.1007/BF00000101.
- Gange, A.C.; Brown, V.K.; Aplin, D.M. (2005). "Ecological specificity of arbuscular mycorrhizae: evidence from foliar- and seed-feeding insects". Ecology. 86 (3): 603–611. doi:10.1890/04-0967.
- Mueller, R.C.; Sthultz, C.M.; Martinez, T.; Gehring, C.A.; Whitham, T.G. (2005). "The relationship between stem-galling wasps and mycorrhizal colonization of Quercus turbinella". Can. J. Bot. 83 (10): 1349–1353. doi:10.1139/b05-105.
- Faeth, S.H.; Hammon, K.E. (1997a). "Fungal endophytes in oak trees: I. Long-term patterns of abundance and association with leafminers". Ecology. 78 (3): 810–819. doi:10.1890/0012-9658(1997)078[0810:FEIOTL]2.0.CO;2. ISSN 0012-9658.
- Faeth, S.H.; Hammon, K.E. (1997b). "Fungal endophytes in oak trees: II. Experimental analyses of interactions with leafminers". Ecology. 78 (3): 820–827. doi:10.1890/0012-9658(1997)078[0820:FEIOTE]2.0.CO;2. ISSN 0012-9658.
- Thomson, J.D. (2003). "When is it mutualism? (An American Society of Naturalists presidential address)". The American Naturalist. 162: S1–S9. doi:10.1086/378683.
- Arnold, A.E.; Miadlikowskam, J.; Higgins, K.L.; Sarvate, S.D.; Gugger, P.; Way, A.; Hofstetter, V.; Kauff, F.; Lutzoni, F.; et al. (2009). "A phylogenetic estimation of trophic transition networks for ascomycetors fungi: are lichens cradles of symbiotic fungal diversification?". Systematic Biology. 58 (3): 283–297. doi:10.1093/sysbio/syp001. PMID 20525584.
- Arnold, A.E.; Lamit, L.J.; Gehring, C.A.; Bidartondo, M.I.; Callahan, H. (2010). "Interwoven branches of the plant and fungal trees of life". New Phytologist. 185 (4): 874–878. doi:10.1111/j.1469-8137.2010.03185.x. PMID 20356341.
- Lane, G.A.; Christenses, M.J. & Miles, C.O. (2000). Coevolution of fungal endophytes with grasses: the significance of secondary metabolites. In: Microbial Endophytes (Bacon, C.W.; White, J.F., eds.). New York: Marcel Dekker. pp. 341-388. ISBN 0-8247-8831-1
- Bezemer, T.M.; van Dam, N.M. (2005). "Linking aboveground and belowground interactions via induced plant defenses". Trends Ecol. Evol. 20 (11): 617–624. doi:10.1016/j.tree.2005.08.006. PMID 16701445.
- U'Ren, J.M.; Dalling, J.W.; Gallery, R.E.; Maddison, D.R.; Davis, E.C.; Gibson, C.M.; Arnold, A.E. (2009). "Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analyzing fungal environmental samples". Mycological Research. 113 (Pt 4): 432–449. doi:10.1016/j.mycres.2008.11.015. PMID 19103288.
- Clay, K. (1997). Fungal endophytes, herbivores and the structure of grassland communities. In: Multitrophic Interactions in Terrestrial Systems (Gange, A.C. & Brown, V.K., eds.). Oxford: Blackwell Scientific. pp. 151-169. ISBN 978-0-521-83995-2
- Gange, A.C. (2007). Insect–mycorrhizal interactions: patterns, processes and consequences. In Ecological Communities: Plant Mediation in Indirect Interaction Webs (Ohgushi, T.; Craig, T.P. & Price, P.W., eds.), pp. 124–143. Cambridge, UK: Cambridge University Press. ISBN 978-0-521-85039-1
- Wilson, D. (1993). "Fungal endophytes: out of sight but should not be out of mind". Oikos. 68 (2): 379–384. doi:10.2307/3544856.
- Funk, C.R.; Halisky, P.M.; Johnson, M.C.; Siegel, M.R.; Stewart, A.V.; Ahmad, S.; Hurley, R.H.; Harvey, I.C. (1983). "An endophytic fungus and resistance to sod webworms: association in Lolium perenne". Biotechnology. 1 (2): 189–191. doi:10.1038/nbt0483-189.
- Gallery, R.E.; Dalling, J.W.; Arnold, A.E. (2007). "Diversity, host affinity and distribution of seed-infecting fungi: a case-study with neotropical Cecropia". Ecology. 88: 582–588. doi:10.1890/05-1207.
- Dalling, J.W.; Davis, A.S.; Schutte, B.J.; Arnold, A.E. (2011). "Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community". Journal of Ecology. 99 (1): 89–95. doi:10.1111/j.1365-2745.2010.01739.x.
- Van WH, der Putten W (2003). "Plant defense belowground and spatiotemporal processes in natural vegetation". Ecology. 84 (9): 2269–2280. doi:10.1890/02-0284.
- Wardle, D.A.; Bardgett, R.D.; Klironomos, J.N.; Setala, H.; Van, WH; der Putten, W.H.; Wall, D.H. (2004). "Ecological linkages between aboveground and belowground biota". Science. 304 (5677): 1629–1633. doi:10.1126/science.1094875. PMID 15192218.
- Molinari, N.; Knight, C. (2010). "Correlated evolution of defensive and nutritional traits in native and non-native plants". Bot. J. Linn. Soc. 163 (1): 1–13. doi:10.1111/j.1095-8339.2010.01050.x.
- Dighton, J.; Jansen, A.E. (1991). "Atomospheric pollutants and ectomycorrhizas: more questions than answers?". Environ. Pollut. 73 (3–4): 179–204. doi:10.1016/0269-7491(91)90049-3. PMID 15092077.
- Marks, S.; Clay, K. (1990). "Effects of CO2 enrichment, nutrient addition and fungal endophyte-infection on the growth of two grasses". Oecologia. 84: 207–214. doi:10.1007/BF00318273.
- Currano, E.D.; Wilf, P.; Wing, S.L.; Labandeira, C.C.; Lovelock, E.; Royer, D. (2008). "Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum". Proceedings of the National Academy of Sciences of the United States of America. 105 (6): 1960–1964. doi:10.1073/pnas.0708646105. PMC . PMID 18268338.
- Marks, S.; Lincoln, D.E. (1996). "Antiherbivore defense mutualism under elevated carbon dioxide levels: a fungal endophyte and grass". Environ. Entomol. 25 (3): 618–623.
- Clay, K. (1994). The potential role of endophytes in ecosystems. In: Biotechnology of endophytic fungi of grasses. Boca Raton: CRC Press. pp. 73-86. ISBN 978-0-8493-6276-7
- Bailey, V. (1903). "Sleepy grass and its effect on horses". Science. 17 (427): 392–393. doi:10.1126/science.17.427.392. PMID 17735119.
- Nobindro, U. (1934). "Grass poisoning among cattle and goats in Assam". Indian Vet. J. 10: 235–236.
- Siegel, M.R.; Latch, G.C.M.; Johnson, M.C. (1985). "Acremonium fungal endophytes of tall fescue and perennial ryegrass: significance and control". Plant Dis. 69 (2): 179–183.
- Clay, K. (1988). "Fungal endophytes of grasses – a defensive mutualism between plants and fungi". Ecology. 69 (1): 10–16. doi:10.2307/1943155.
- Hartley, S.E.; Gange, A.C. (2009). "Impacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualism in a Multitrophic Context". Annu. Rev. Entomol. 54: 323–342. doi:10.1146/annurev.ento.54.110807.090614.
- Fontana, A.; Reichelt, M.; Hempel, S.; Gershenzon, J.; Unsicker, S.B. (2009). "The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L". J. Chem. Ecol. 35 (7): 833–843. doi:10.1007/s10886-009-9654-0. PMC . PMID 19568812.
- Bultman, T.L.; Bell, G.; Martin, W.D. (2004). "A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass". Ecology. 85 (3): 679–685. doi:10.1890/03-0073.
- Pieterse, C.M.J.; Dicke, M. (2007). "Plant interactions with microbes and insects: from molecular mechanisms to ecology". Trends Plant Sci. 12 (12): 564–569. doi:10.1016/j.tplants.2007.09.004. PMID 17997347.
- Zheng, S.J.; Dicke, M. (2008). "Ecological genomics of plant-insect interactions: from gene to community". Plant Physiol. 146 (3): 812–817. doi:10.1104/pp.107.111542. PMC . PMID 18316634.
- Simmons, L.; Bultman, T.L.; Sullivan, T.J. (2008). "Effects of Methyl Jasmonate and an Endophytic Fungus on Plant Resistance to Insect Herbivores". J. Chem. Ecol. 34 (12): 1511–1517. doi:10.1007/s10886-008-9551-y. PMID 18925382.
- Wink, M. (2008). "Plant secondary metabolism: Diversity, function and its evolution". Natural Product Communications. 3 (8): 1205–1216.
- Lambais, M.R. (2001). "In silico differential display of defense-related expressed sequence tags from sugarcane tissues infected with diazotrophic endophytes". Genetics and Molecular Biology. 24 (1): 103–111. doi:10.1590/S1415-47572001000100015.
- Shrivastava, G.; Rogers, M.; Wszelaki, A.; Panthee, D.R.; Chen, F. (2010). "Plant Volatiles-based Insect Pest Management in Organic Farming". Plant Sciences. 29 (2): 123–133. doi:10.1080/07352681003617483.
- Hoveland, C.S. (1993). "Importance and economic significance of the Acremonium endophytes to performance of animals and grass plant". Agric. Ecosyst. & Environ. 44 (1): 3–12. doi:10.1016/0167-8809(93)90036-O.
- Jarvis, B.B.; Wells, K.M.; Lee, Y.W.; Bean, G.A.; Kommendahl, T.; Barros, C.S. L.; Barros, S.S. (1987). "Macrocyclic triocothecene mycotoxins in Brazilian species of Baccharis". Phytopathology. 12: 111–128.
- Steudemann, J.A.; Hoveland, C.S. (1988). "Fescue endophyte: history and impact on animal agricultural". J. Product Agric. 1: 39–44.
- West, C.P. & Gwinn, K.D. (1993). Role of Acremonium in drought, pest and disease tolerance of grasses. In: Proc. 2nd Int. Symp. Acremonium/grass interactions: plenary papers. (Hume, D.E.; Latch, G.C.M. & Easton, H.S., eds.) Palmerston North, NZ: AgResearch, Grasslanda Research Centre.
- Rabin, L.B.; Pacovsky, R.S. (1985). "Reduced larva growth of two Lepidoptera (Noctuidae) on excised leaves of soybean infected with amycorrhizal fungus". J. Econ. Entom. 78: 1358–1363.
- Gange, A.C.; West, H.M. (1994). "Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L". New Phytol. 128: 79–87. doi:10.1111/j.1469-8137.1994.tb03989.x.
- Akello, J.; Dubois, T.; Coyne, D.; Kyamanywa, S. (2008). "Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage". Crop Protection. 27 (11): 1437–1441. doi:10.1016/j.cropro.2008.07.003.
- Jallow, M.F.A.; Dugassa-Gobena, D.; Vidal, S. (2004). "Indirect interaction between and unspecialized endophytic fungus and a polyphagous moth". Basic and Applied Ecology. 5 (2): 183–191. doi:10.1078/1439-1791-00224.
- Dent, D. (1991) Insect pest management. Wallingford, UK: CAB International. ISBN 0-85199-340-0
- Murray, F.R.; Latch, G.M.C.; Scott, D.B. (1992). "Surrogate transformation of perennial ryegrass, Lolium perenne, using genetically modified Acremonium endophyte". Mol. Gen, Genet. 233: 1–9. doi:10.1007/BF00587554.
- Shennan, C. (2008). "Biotic interactions, ecological knowledge and agriculture". Phil. Trans. R. Soc. B. 363 (1492): 717–739. doi:10.1098/rstb.2007.2180. PMC . PMID 17761466.
- Black, M.H. & Halmer, P. (2006). The encyclopedia of seeds: science, technology and uses. Wallingford, UK: CABI. pp. 226. ISBN 978-0-85199-723-0.
- Schade, R.; Andersohn, F.; Suissa, S.; Haverkamp, W.; Garbe, E. (2007). "Dopamine agonists and the risk of cardiac-valve regurgitation". New England Journal of Medicine. 356 (1): 29–38. doi:10.1056/NEJMoa062222. PMID 17202453.
- Correia, T.; Grammel, N.; Ortel, I.; Keller, U.; Tudzynski, P. (2001). "Molecular cloning and analysis of the ergopeptine assembly system in the ergot fungus Claviceps purpurea". Chem Biol. 10 (12): 1281–1292. doi:10.1016/j.chembiol.2003.11.013. PMID 14700635.
- Gray, W.D. (1959). The Relation of Fungi to Human Affairs. New York: Henry Holt and Company, Inc.
- Dighton, J. (2003). Fungi in Ecosystem Processes. New York: M. Dekker. ISBN 978-0-8247-4244-7.
- Smith, S.E. & Read, D.J. (2008). Mycorrhizal symbiosis (3rd ed.). London: Academic Press. ISBN 978-0-12-370526-6.
- Redlin, S.C. & Carris, L.M. (1996). Endophytic fungi in grasses and woody plants: Systematics, ecology, and evolution. St. Paul, Minn: APS Press. ISBN 978-0-89054-213-2.
- Cheplick, G.P. & Faeth, S.H. (2009). Ecology and evolution of the grass-endophyte symbiosis. Oxford: Oxford University Press. ISBN 978-0-19-530808-2.
- Bacon, C.W. & White, J.F. (1994). Biotechnology of endophytic fungi of grasses. Boca Raton: CRC Press. ISBN 978-0-8493-6276-7.
- Bacon, C.W. & White, J.F. (editors) (2000). Microbial Endophytes. New York: Marcel Dekker. ISBN 0-8247-8831-1.
- White, J.F. & Torres, M.S. (2009). Defensive mutualism in microbial symbiosis. Boca Raton: CRC Press. ISBN 978-1-4200-6931-0.
- Heijden, M.G.A. & Sanders, I.R. (2002). Mycorrhizal ecology. Berlin: Springer. ISBN 978-3-540-42407-9.
- Mycorrhizal Associations: The Web Resource - Comprehensive illustrations and lists of mycorrhizal and nonmycorrhizal plants and fungi
- International Mycorrhiza Society
- Mycorrhizal Literature Exchange - Database of abstracts, reviews, books, theses and dissertations hosted by the University of Tennessee
- Plant Defense Systems and Medicinal Botany - Explanations of plant defensive chemicals and their use by humans