Plant use of endophytic fungi in defense

{{Main|Endophyte}}

File:Ergot01.jpg spp. fungus growing on wheat spikes, a common endophyte of the grasses.]]

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.{{cite journal | last1 = Vega | first1 = F.E. | last2 = Posada | first2 = F. | last3 = Aime | first3 = M.C. | last4 = Pava-Ripoll | first4 = M. | last5 = Infante | first5 = F. | last6 = Rehner | first6 = S.A. | year = 2008 | title = Entomopathogenic fungal endophytes | url = https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=1390&context=usdaarsfacpub| journal = Biological Control | volume = 46 | issue = 1 | pages = 72–82 | doi = 10.1016/j.biocontrol.2008.01.008| bibcode = 2008BiolC..46...72V | s2cid = 53559011 }} 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.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}}. The entomopathogenic view has gained support from observations of increased fungal growth in response to induced plant defenses{{cite journal | last1 = Baverstock | first1 = J| last2 = Elliot | first2 = S.L. | last3 = Alderson | first3 = P.G. | last4 = Pell | first4 = J.K. | year = 2005 | title = Response of the entomopathogenic fungus Pandora neoaphidis to aphid-induced plant volatiles | journal = Journal of Invertebrate Pathology | volume = 89 | issue = 2| pages = 157–164 | doi = 10.1016/j.jip.2005.05.006 | pmid = 16005016| bibcode = 2005JInvP..89..157B}} and colonization of plant tissues.{{cite journal | last1 = Gómez-Vidal | first1 = S. | last2 = Salinas | first2 = J. | last3 = Tena | first3 = M. | last4 = Lopez-Llorca | first4 = L.V. | year = 2009 | title = Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi | journal = Electrophoresis | volume = 30 | issue = 17| pages = 2996–3005 | doi = 10.1002/elps.200900192 | pmid = 19676091 | s2cid = 27158428}}

Examples of host specialists are numerous – especially in temperate environments – with multiple specialist fungi frequently infecting one plant individual simultaneously.{{cite journal | last1 = Arnold | first1 = A.E. | last2 = Lutzoni | first2 = F. | year = 2007 | title = Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? | journal = Ecology | volume = 88 | issue = 3| pages = 541–549 | doi = 10.1890/05-1459 | pmid = 17503580 | bibcode = 2007Ecol...88..541A | s2cid = 23661161}}{{cite journal | last1 = Leuchtmann | first1 = A. | year = 1992 | title = Systematics, distribution and host specificity of grass endophytes | journal = Nat. Toxins | volume = 1 | issue = 3| pages = 150–162 | pmid = 1344916 | doi=10.1002/nt.2620010303}} These specialists demonstrate high levels of specificity for their host species and may form physiologically adapted host-races on closely related congeners.{{cite journal | last1 = Leuchtmann | first1 = A. | last2 = Clay | first2 = K. | year = 1990 | title = Isozyme variation in the Acremonium/Epichloe fungal endophyte complex | journal = Phytopathology | volume = 80 | issue = 10| pages = 1133–1139 | doi = 10.1094/Phyto-80-1133| bibcode = 1990PhPat..80.1133L }} 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.{{cite journal |last1=Varma |first1=Ajit |last2=Sahay |first2=Nirmal |last3=Bütehorn |first3=Britta |last4=Franken |first4=Philipp |title=Piriformospora indica, a Cultivable Plant-Growth-Promoting Root Endophyte |journal=Applied and Environmental Microbiology |date=June 1999 |volume=65 |issue=6 |pages=2741–2744 |doi=10.1128/AEM.65.6.2741-2744.1999 |pmid=10347070|pmc=91405|bibcode=1999ApEnM..65.2741V }}{{cite journal |last1=Waller |first1=Frank |last2=Achatz |first2=Beate |last3=Baltruschat |first3=Helmut |last4=Fodor |first4=József |last5=Becker |first5=Katja |last6=Fischer |first6=Marina |last7=Heier |first7=Tobias |last8=Hückelhoven |first8=Ralph |last9=Neumann |first9=Christina |last10=von Wettstein |first10=Diter |last11=Franken |first11=Philipp |last12=Kogel |first12=Karl-Heinz |title=The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield |journal=Proceedings of the National Academy of Sciences |date=20 September 2005 |volume=102 |issue=38 |pages=13386–13391 |doi=10.1073/pnas.0504423102 |pmid=16174735 |pmc=1224632 |bibcode=2005PNAS..10213386W |doi-access=free }} 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{{cite journal | last1 = Leuchtmann | first1 = A. | year = 1988 | title = Isozyme relationships of Acremonium endophytes from twelve Festuca species | journal = Mycol. Res. | volume = 98 | pages = 25–33 | doi=10.1016/s0953-7562(09)80331-6}}) and as part of a variety of fungal assemblages.{{cite journal | last1 = Kluger | first1 = C.G. | last2 = Dalling | first2 = J.W. | last3 = Gallery | first3 = R.E. | last4 = Sanchez | first4 = E. | last5 = Weeks-Galindo | first5 = C. | last6 = Arnold | first6 = A.E. | year = 2008 | title = Prevalent host-generalism among fungi associated with the seeds of four neotropical pioneer species | journal = Journal of Tropical Ecology | volume = 24 | issue = 3| pages = 332–351 | doi = 10.1017/s0266467408005026| s2cid = 5757188 }}{{cite journal | last1 = Leuchtmann | first1 = A. | last2 = Clay | first2 = K. | year = 1989 | title = Isozyme variation in the fungus Atkinsonella hypoxylon within and among populations of its host grasses | journal = Can. J. Bot. | volume = 67 | issue = 9| pages = 2600–2607 | doi = 10.1139/b89-336| bibcode = 1989CaJB...67.2600L }} They may even spread to novel, introduced plant species.{{cite journal | last1 = Rykard | first1 = D.M. | last2 = Bacon | first2 = C.W. | last3 = Luttrell | first3 = E.S. | year = 1985 | title = Host relations of Myriogenospora atramentosa and Balansia epichloe (Clavicipitaceae) | url = https://zenodo.org/record/1235927| journal = Phytopathology | volume = 75 | issue = 8| pages = 950–956 | doi = 10.1094/Phyto-75-950| bibcode = 1985PhPat..75..950R }} Endophytic mutualists associate with species representative of every growth form and life history strategy in the grasses and many other groups of plants.{{cite book |last1=Clay |first1=K |editor1-last=Hawksworth |editor1-first=David Leslie |editor2-last=Pirozynski |editor2-first=K. A. |title=Coevolution of fungi with plants and animals |date=1988 |publisher=Academic Press |location=London |isbn=9780125573658 |chapter=Claviciptaceous fungal endophytes of grasses: coevolution and the change from parasitism to mutualism}} 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.{{cite journal | last1 = Vicari | first1 = M. | last2 = Hatcher | first2 = P.E. | last3 = Ayres | first3 = P.G. | year = 2002 | title = Combined effect of foliar and mycorrhizal endophytes on an insect herbivore | journal = Ecology | volume = 83 | issue = 9| pages = 2452–2464 | doi = 10.1890/0012-9658(2002)083[2452:CEOFAM]2.0.CO;2 | issn = 0012-9658}}{{cite journal | last1 = Klironomos | first1 = J. | year = 2008 | title = Variation in plant response to native and exotic arbuscular mycorrhizal fungi | journal = Ecology | volume = 84 | issue = 9| pages = 2292–2301 | doi=10.1890/02-0413| s2cid = 85949792 }}

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.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.{{cite journal | last1 = Rowan | first1 = D.D. | last2 = Hunt | first2 = M.B. | last3 = Gaynor | first3 = D.L. | year = 1986 | title = Peramine, a novel insect feeding deterrent from ryegrass infected with the endophyte Acremonium loliae | journal = J. Chem. Soc. Chem. Commun. | volume = 1986 | issue = 12| pages = 935–936 | doi=10.1039/c39860000935}} 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.{{cite journal | last1 = Zhang | first1 = D.X. | last2 = Nagabhyru | first2 = P. | last3 = Schardl | first3 = C.L. | year = 2009 | title = Regulation of a Chemical Defense against Herbivory Produced by Symbiotic Fungi in Grass Plants | journal = Plant Physiology | volume = 150 | issue = 2| pages = 1072–1082 | doi = 10.1104/pp.109.138222 | pmid = 19403726 | pmc = 2689992}}{{cite journal | last1 = Clay | first1 = K. | last2 = Cheplick | first2 = G.P. | year = 1989 | title = Effect of ergot alkaloids from fungal endophyt-infected grasses on fall armyworm (Spodoptera frugiperda) | journal = J. Chem. Ecol. | volume = 15 | issue = 1| pages = 169–182 | doi = 10.1007/BF02027781 | pmid = 24271434 | bibcode = 1989JCEco..15..169C | s2cid = 22517484}}{{cite journal | last1 = Patterson | first1 = C.G. | last2 = Potter | first2 = D.A. | last3 = Fannin | first3 = F.F. | year = 1991 | title = Feeding deterrency of alkaloids from endophyte-infected grasses to Japanese beetle grubs | journal = Entomologia Experimentalis et Applicata | volume = 61 | issue = 3| pages = 285–289 | doi = 10.1111/j.1570-7458.1991.tb01561.x | bibcode = 1991EEApp..61..285P | s2cid = 85793589}}{{cite book |last1=Prestidge |first1=R.A. |last2=Ball |first2=O.J.-P |editor1-last=Gange |editor1-first=A. C. |editor2-last=Brown |editor2-first=Valerie K. |title=Multitrophic interactions in terrestrial systems: the 36th Symposium of the British Ecological Society, Royal Holloway College, University of London, 1995 |date=1997 |publisher=Blackwell Science |location=Oxford |isbn=9780865427679 |pages=171–192 |chapter=A catch 22: The utilization of endophytic fungi for pest management }} 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.{{cite journal | last1 = Rowan | first1 = D.D. | last2 = Dymock | first2 = J.J. | last3 = Brimble | first3 = M.A. | year = 1990 | title = Effect of fungal metabolite peramine and analogs on feeding and development of Argentine stem weevil (Listronotus bonariensis) | journal = J. Chem. Ecol. | volume = 16 | issue = 5| pages = 1683–1695 | doi = 10.1007/BF01014100 | pmid = 24263837 | bibcode = 1990JCEco..16.1683R | s2cid = 24714381}} Terpenoids and ketones have been linked to protection from specialist and generalist herbivores (both insect and vertebrate) across the higher plants.{{cite journal | last1 = Akiyama | first1 = K. | last2 = Hayashi | first2 = H. | year = 2001 | title = Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots | journal = Biosci. Biotechnol. Biochem. | volume = 66 | issue = 4| pages = 762–769 | doi=10.1271/bbb.66.762 | pmid=12036048| s2cid = 36336157| doi-access = free }}{{cite journal | last1 = Rapparini | first1 = F. | last2 = Llusia | first2 = J. | last3 = Penuelas | first3 = J. | year = 2008 | title = Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L | journal = Plant Biol. | volume = 10 | issue = 1| pages = 108–122 | doi = 10.1055/s-2007-964963 | pmid = 18211551 | bibcode = 2008PlBio..10..108R | citeseerx = 10.1.1.712.2028| s2cid = 260251297}}

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.{{cite book |last1=Smith |first1=S. E. |last2=Read |first2=David J. |title=Mycorrhizal symbiosis |date=2008 |publisher=Academic Press |location=London |isbn=978-0-12-370526-6 |edition=3rd}} Among the chewing insects, infection by mycorrhizae can actually benefit specialist feeders even if it negatively affects generalists.{{cite journal | last1 = Koricheva | first1 = J. | last2 = Gange | first2 = A.C. | last3 = Jones | first3 = T. | year = 2009 | title = Effects of mycorrhizal fungi on insect herbivores: a meta-analysis | journal = Ecology | volume = 90 | issue = 8| pages = 2088–2097 | doi = 10.1890/08-1555.1 | pmid = 19739371 | bibcode = 2009Ecol...90.2088K | s2cid = 6518292}} 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.{{cite journal | last1 = Gehring | first1 = C. | last2 = Bennett | first2 = A. | year = 2009 | title = Mycorrhizal fungal-plant-insect interactions: the importance of a community approach | journal = Environ. Entomol. | volume = 38 | issue = 1| pages = 93–102 | doi = 10.1603/022.038.0111 | pmid = 19791601 | doi-access = free}}

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.{{cite journal | last1 = Langenheim | first1 = J.H. | year = 1994 | title = Higher-plant terpenoids – a phytocentric view of their ecological roles | journal = J. Chem. Ecol. | volume = 20 | issue = 6| pages = 1223–1280 | doi = 10.1007/BF02059809 | pmid = 24242340 | s2cid = 25360410}} These enemies can reduce numbers of invertebrate herbivores substantially and may not be attracted in the absence of endophytic symbionts.{{cite journal | last1 = Kagata | first1 = H. | last2 = Ohgushi | first2 = T. | year = 2006 | title = Bottom-up trophic cascades and material transfer in terrestrial food webs | journal = Ecol. Res. | volume = 21 | issue = 1 | pages = 26–34 | doi = 10.1007/s11284-005-0124-z | bibcode = 2006EcoR...21...26K | s2cid = 39501055}} 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.{{cite journal | last1 = Pineda | first1 = A. | last2 = Zheng | first2 = S.J. | last3 = van Loon | first3 = J.J.A. | last4 = Pieterse | first4 = C.M.J. | last5 = Dicke | first5 = M. | year = 2010 | title = Helping plants to deal with insects: the role of beneficial soil-borne microbes | journal = Trends in Plant Science | volume = 15 | issue = 9| pages = 507–514 | doi = 10.1016/j.tplants.2010.05.007 | pmid = 20542720| bibcode = 2010TPS....15..507P | hdl = 1874/387958 | s2cid = 18883590 | hdl-access = free }}{{cite journal | last1 = Gange | first1 = A.C. | last2 = Brown | first2 = V.K. | last3 = Aplin | first3 = D.M. | year = 2003 | title = Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids | journal = Ecol. Lett. | volume = 6 | issue = 12| pages = 1051–1055 | doi = 10.1046/j.1461-0248.2003.00540.x| bibcode = 2003EcolL...6.1051G }}{{cite journal | last1 = Valenzuela-Soto | first1 = J.H. | last2 = Estrada-Hernandez | first2 = M.G. | last3 = Ibarra-Laclette | first3 = E. | last4 = Delano-Frier | first4 = J.P. | year = 2010 | title = Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development | journal = Planta | volume = 231 | issue = 2| pages = 397–410 | doi = 10.1007/s00425-009-1061-9 | pmid = 20041333 | bibcode = 2010Plant.231..397V | s2cid = 1693336}}

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.{{cite book |last1=Richardson |first1=M.D. |editor1-last=Bacon |editor1-first=Charles W. |editor2-last=White |editor2-first=James F. |title=Microbial endophytes |date=2000 |publisher=M. Dekker |location=New York |isbn=0-8247-8831-1 |pages=323 |chapter=Alkaloids of endophyte-infected grasses: defense chemicals or biological anomalies?}} 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.{{cite journal | last1 = Gange | first1 = A.C. | last2 = Nice | first2 = H.E. | year = 1997 | title = Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization | journal = New Phytologist | volume = 137 | issue = 2| pages = 335–343 | doi = 10.1046/j.1469-8137.1997.00813.x| pmid = 33863184 | doi-access = free | bibcode = 1997NewPh.137..335G }} Additionally, increased availability of limiting nutrients to plants improves overall performance and health, potentially increasing the ability of infected plants to defend themselves.{{cite journal | last1 = Gosling | first1 = P. | last2 = Hodge | first2 = A. | last3 = Goodlass | first3 = G. | last4 = Bending | first4 = G.D. | year = 2006 | title = Arbuscular mycorrhizal fungi and organic farming | journal = Agric. Ecosyst. Environ. | volume = 113 | issue = 1–4| pages = 17–35 | doi = 10.1016/j.agee.2005.09.009| bibcode = 2006AgEE..113...17G }}

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.{{cite journal | last1 = Latch | first1 = G.C.M. | year = 1993 | title = Physiological interactions of endophytic fungi and their hosts. Biotic stress tolerance imparted to grasses by endophytes | journal = Agric. Ecosyst. Environ. | volume = 44 | issue = 1–4| pages = 143–156 | doi = 10.1016/0167-8809(93)90043-O| bibcode = 1993AgEE...44..143L }}{{cite journal | last1 = Schmidt | first1 = S.P. | last2 = Osborn | first2 = T.G. | year = 1993 | title = Effects of endophyte-infected tall fescue on animal performance | journal = Agric. Ecosyst. Environ. | volume = 44 | issue = 1–4| pages = 233–262 | doi = 10.1016/0167-8809(93)90049-U| bibcode = 1993AgEE...44..233S }} 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.{{cite book |last1=Currie |first1=Amanda F. |last2=Wearn |first2=James |last3=Hodgson |first3=Su |last4=Wendt |first4=Hilary |last5=Broughton |first5=Sue |last6=Jin |first6=Liang |chapter=Foliar Fungal Endophytes in Herbaceous Plants: A Marriage of Convenience? |editor1-last=Verma |editor1-first=Vijay C. |editor2-last=Gange |editor2-first=Alan C. |title=Advances in Endophytic Research |date=2014 |pages=61–81 |doi=10.1007/978-81-322-1575-2_3|isbn=978-81-322-1574-5 }} Vertebrate herbivores such as birds,{{cite journal | last1 = Madej | first1 = C.W. | last2 = Clay | first2 = K. | year = 1991 | title = Avian seed preference and weight loss experiments: the role of fungal endophyte-infected tall fescue seeds | journal = Oecologia | volume = 88 | issue = 2| pages = 296–302 | doi = 10.1007/BF00320825 | pmid = 28312146 | s2cid = 25432064}} rabbitsSadler, K. (1980). Of rabbits and habitat, a long term look. Missouri Conservationist March: 4-7. and deer{{cite journal | last1 = Mackintosh | first1 = C.G. | last2 = Orr | first2 = M.B. | last3 = Gallagher | first3 = R.T. | last4 = Harvey | first4 = I.C. | year = 1982 | title = Ryegrass staggers in Canadian wapiti deer | journal = N. Z. Vet. J. | volume = 36 | issue = 7| pages = 106–107 | doi = 10.1080/00480169.1982.34899 | pmid = 16030885}} 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.{{cite journal | last1 = West | first1 = C.P. | last2 = Izekor | first2 = E. | last3 = Oosterhuis | first3 = D.M. | last4 = Robbins | first4 = R.T. | year = 1988 | title = The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue | journal = Plant Soil | volume = 112 | issue = 1 | pages = 3–6 | doi = 10.1007/BF02181745 | bibcode = 1988PlSoi.112....3W | s2cid = 33069313}}{{cite book |last1=Clay |first1=K. |editor1-last=Jones |editor1-first=Clive G. |editor2-last=Barbosa |editor2-first=Pedro |editor3-last=Krischik |editor3-first=Vera A. |title=Microbial mediation of plant-herbivore interactions |date=1991 |publisher=Wiley |location=New York |isbn=978-0-471-61324-4 |pages=199–226 |chapter=Fungal endophytes, grasses, and herbivores}}{{cite journal | last1 = Newsham | first1 = K.K. | last2 = Fitter | first2 = A.H. | last3 = Watkinson | first3 = A.R. | year = 1995 | title = Arbuscular mycorrhizae protect an annual grass from root pathogenic fungi in the field | journal = Journal of Ecology | volume = 83 | issue = 6| pages = 991–1000 | doi = 10.2307/2261180 | jstor = 2261180 | bibcode = 1995JEcol..83..991N | s2cid = 35674502}}{{cite journal | last1 = Gange | first1 = A.C. | year = 2000 | title = Arbuscular mycorrhizal fungi, Collembola and plant growth | journal = Trends in Ecology and Evolution | volume = 15 | issue = 9| pages = 369–372 | doi = 10.1016/S0169-5347(00)01940-6 | pmid = 10931669| bibcode = 2000TEcoE..15..369G }} 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,{{cite journal | last1 = Ahmad | first1 = S. | last2 = Govindarajan | first2 = S. | last3 = Funk | first3 = C.R. | last4 = Johnson-Cicalese | first4 = J.M. | year = 1985 | title = Fatality of house crickets on perennial ryegrass infected with fungal endophyte | journal =Entomologia Experimentalis et Applicata | volume = 39 | issue = 2| pages = 183–190 | doi = 10.1111/j.1570-7458.1985.tb03561.x | bibcode = 1985EEApp..39..183A | s2cid = 85139290}} larval armyworms and flour beetles.{{cite journal | last1 = Cheplick | first1 = G.P. | last2 = Clay | first2 = K. | year = 1988 | title = Acquired chemical defenses of grasses: the role of fungal endophytes | journal = Oikos | volume = 52 | issue = 3| pages = 309–318 | doi = 10.2307/3565204 | jstor = 3565204| bibcode = 1988Oikos..52..309C }}

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;{{cite journal | last1 = Lewis | first1 = G.C. | last2 = Clements | first2 = R.O. | year = 1986 | title = A survey of ryegrass endophyte (Acremonium loliae) in the U.K. and its apparent ineffectuality on a seedling pest | journal = J. Agric. Sci. | volume = 107 | issue = 3| pages = 633–638 | doi=10.1017/s002185960006980x| s2cid = 86253358 }} larval stages are often more susceptible to toxins than adults.{{cite journal | last1 = Hardy | first1 = T.N. | last2 = Clay | first2 = K. | last3 = Hammond | first3 = A.M. Jr | year = 1986 | title = Leaf age and related factors affecting endophyte-mediated resistance to fall armyworm (Lepidoptera: Noctuidae) in tall fescue | journal = Environ. Entomol. | volume = 15 | issue = 5| pages = 1083–1089 | doi = 10.1093/ee/15.5.1083}}{{cite journal | last1 = Kindler | first1 = S.D. | last2 = Breen | first2 = J.P. | last3 = Springer | first3 = T.L. | year = 1991 | title = Reproduction and damage by Russian wheat aphid (Homoptera:Aphididae) as influenced by fungal endophytes and cool-season turfgrasses | journal = J. Econ. Entomol. | volume = 84 | issue = 2| pages = 685–692 | doi=10.1093/jee/84.2.685}} 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.{{cite journal | last1 = Koh | first1 = S. | last2 = Hik | first2 = D.S. | year = 2007 | title = Herbivory mediates grass-endophyte relationships | journal = Ecology | volume = 88 | issue = 11| pages = 2752–2757 | doi = 10.1890/06-1958.1 | pmid = 18051643 | bibcode = 2007Ecol...88.2752K | s2cid = 6522331}}

Not all endophytic symbioses confer protection from herbivores – only some species associations act as defense mutualisms.{{cite journal | last1 = Tibbets | first1 = T.M. | last2 = Faeth | first2 = S.H. | year = 1999 | title = Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants? | journal = Oecologia | volume = 118 | issue = 3| pages = 297–305 | doi = 10.1007/s004420050730 | pmid = 28307273 | bibcode = 1999Oecol.118..297T | s2cid = 5933308}} The difference between a mutualistic endophyte and a pathogenic one can be indistinct and dependent on interactions with other species or environmental conditions. Some endophytic fungi can counteract the negative impacts of pathogenic fungi in some plants such as Siberian ryegrass (Elymus sibiricus) by increasing seed germination, coleoptile and radicle length, and seedling weight.{{Cite journal |last1=Li |first1=Xiu-Zhang |last2=Song |first2=Mei-Ling |last3=Yao |first3=Xiang |last4=Chai |first4=Qing |last5=Simpson |first5=Wayne R. |last6=Li |first6=Chun-Jie |last7=Nan |first7=Zhi-Biao |date=2017-12-15 |title=The Effect of Seed-Borne Fungi and Epichloë Endophyte on Seed Germination and Biomass of Elymus sibiricus |journal=Frontiers in Microbiology |volume=8 |page=2488 |doi=10.3389/fmicb.2017.02488 |pmid=29375493 |pmc=5770693 |issn=1664-302X|doi-access=free }} 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.{{cite journal | last1 = Clay | first1 = K. | last2 = Cheplick | first2 = G.P. | last3 = Marks | first3 = S. | year = 1989 | title = Impact of the fungus Balansia henningsiana on Panicum agrostoides: frequency of infection, plant growth and reproduction, and resistance to pests | journal = Oecologia | volume = 80 | issue = 3| pages = 374–380 | doi = 10.1007/BF00379039 | pmid = 28312065 | bibcode = 1989Oecol..80..374C | s2cid = 24441887}} This is not unusual among fungi, as non-endophytic plant pathogens have similar conditionally beneficial effects on defense.{{cite journal | last1 = Kruess | first1 = A. | year = 2002 | title = Indirect interaction between a fungal plant pathogen and a herbivorous beetle of the weed Cirsum aravense | journal = Oecologia | volume = 130 | issue = 4| pages = 563–569 | doi = 10.1007/s00442-001-0829-9 | pmid = 28547258 | bibcode = 2002Oecol.130..563K | s2cid = 21123232| url = https://resolver.sub.uni-goettingen.de/purl?gro-2/44330 }} 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.{{cite journal | last1 = Gehring | first1 = C.A. | last2 = Whitham | first2 = T.G. | year = 1994 | title = Interactions between aboveground herbivores and the mycorrhizal mutualists of plants | journal = Trends in Ecology & Evolution | volume = 9 | issue = 7| pages = 251–255 | doi = 10.1016/0169-5347(94)90290-9 | pmid = 21236843| bibcode = 1994TEcoE...9..251G }}{{cite journal | last1 = Fitter | first1 = A.H. | last2 = Garbaye | first2 = J. | year = 1994 | title = Interactions between mycorrhizal fungi and other soil organisms | doi = 10.1007/BF00000101 | journal = Plant and Soil | volume = 159 | issue = 1| pages = 123–132 | bibcode = 1994PlSoi.159..123F | s2cid = 29782421 }} The effect of one fungus on the plant can be altered when multiple strains of fungi are infecting a given individual in combination.{{cite journal | last1 = Gange | first1 = A.C. | last2 = Brown | first2 = V.K. | last3 = Aplin | first3 = D.M. | year = 2005 | title = Ecological specificity of arbuscular mycorrhizae: evidence from foliar- and seed-feeding insects | journal = Ecology | volume = 86 | issue = 3| pages = 603–611 | doi = 10.1890/04-0967}}

Some endomycorrhizae may actually promote herbivore damage by making plants more susceptible to it.{{cite journal | last1 = Mueller | first1 = R.C. | last2 = Sthultz | first2 = C.M. | last3 = Martinez | first3 = T. | last4 = Gehring | first4 = C.A. | last5 = Whitham | first5 = T.G. | year = 2005 | title = The relationship between stem-galling wasps and mycorrhizal colonization of Quercus turbinella | journal = Can. J. Bot. | volume = 83 | issue = 10| pages = 1349–1353 | doi = 10.1139/b05-105| bibcode = 2005Botan..83.1349M }} 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.{{cite journal | last1 = Faeth | first1 = S.H. | last2 = Hammon | first2 = K.E. | year = 1997a | title = Fungal endophytes in oak trees: I. Long-term patterns of abundance and association with leafminers | journal = Ecology | volume = 78 | issue = 3| pages = 810–819 | doi = 10.1890/0012-9658(1997)078[0810:FEIOTL]2.0.CO;2 | issn = 0012-9658}}{{cite journal | last1 = Faeth | first1 = S.H. | last2 = Hammon | first2 = K.E. | year = 1997b | title = Fungal endophytes in oak trees: II. Experimental analyses of interactions with leafminers | journal = Ecology | volume = 78 | issue = 3| pages = 820–827 | doi = 10.1890/0012-9658(1997)078[0820:FEIOTE]2.0.CO;2 | issn = 0012-9658}} 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.{{cite journal | last1 = Thomson | first1 = J.D. | year = 2003 | title = When is it mutualism? (An American Society of Naturalists presidential address) | journal = The American Naturalist | volume = 162 | issue = 4 Suppl| pages = S1–S9 | doi=10.1086/378683| pmid = 14583853| s2cid = 34146093 }}{{cite journal | last1 = Arnold | first1 = A.E. | last2 = Miadlikowskam | first2 = J. | last3 = Higgins | first3 = K.L. | last4 = Sarvate | first4 = S.D. | last5 = Gugger | first5 = P. | last6 = Way | first6 = A. | last7 = Hofstetter | first7 = V. | last8 = Kauff | first8 = F. | last9 = Lutzoni | first9 = F.| year = 2009 | title = A phylogenetic estimation of trophic transition networks for ascomycetors fungi: are lichens cradles of symbiotic fungal diversification? | journal = Systematic Biology | volume = 58 | issue = 3| pages = 283–297 | doi = 10.1093/sysbio/syp001 | pmid = 20525584 | s2cid = 4835456 |display-authors=etal| doi-access = free }}

Fungal endophytes which provide defensive services to their host plants may exert selective pressures favouring association through enhanced fitness relative to uninfected hosts.{{cite journal | last1 = Arnold | first1 = A.E. | last2 = Lamit | first2 = L.J. | last3 = Gehring | first3 = C.A. | last4 = Bidartondo | first4 = M.I. | last5 = Callahan | first5 = H. | year = 2010 | title = Interwoven branches of the plant and fungal trees of life | journal = New Phytologist | volume = 185 | issue = 4| pages = 874–878 | doi = 10.1111/j.1469-8137.2010.03185.x | pmid = 20356341| doi-access = free | bibcode = 2010NewPh.185..874A }} The fungus Neotyphodium spp. infects grasses and increases fitness under conditions with high levels of interspecific competition.{{cite book |last1=Lane |first1=Geoffrey A. |title=Microbial endophytes |last2=Christensen |first2=Michael J. |last3=Miles |first3=Christopher O. |date=2000 |publisher=M. Dekker |isbn=0-8247-8831-1 |editor1-last=Bacon |editor1-first=Charles W. |location=New York |pages=341–388 |chapter=Coevolution of fungal endophytes with grasses: the significance of secondary metabolites |editor2-last=White |editor2-first=James F.}} 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.{{cite journal | last1 = Bezemer | first1 = T.M. | last2 = van Dam | first2 = N.M. | year = 2005 | title = Linking aboveground and belowground interactions via induced plant defenses | journal = Trends Ecol. Evol. | volume = 20 | issue = 11| pages = 617–624 | doi = 10.1016/j.tree.2005.08.006 | pmid = 16701445 | hdl = 2066/90875 | s2cid = 32217638 | hdl-access = free}} Plants undefended by chemical or physical means at certain points in their life histories have higher survival rates when infected with beneficial endophytic fungi.{{cite journal | last1 = U'Ren | first1 = J.M. | last2 = Dalling | first2 = J.W. | last3 = Gallery | first3 = R.E. | last4 = Maddison | first4 = D.R. | last5 = Davis | first5 = E.C. | last6 = Gibson | first6 = C.M. | last7 = Arnold | first7 = A.E. | year = 2009 | title = Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analyzing fungal environmental samples | journal = Mycological Research | volume = 113 | issue = Pt 4| pages = 432–449 | doi = 10.1016/j.mycres.2008.11.015 | pmid = 19103288}} 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.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}} Unsurprisingly, low to moderate levels of herbivore damage also increases the levels of infection by beneficial endophytic fungi.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}}

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.{{cite journal | last1 = Wilson | first1 = D. | year = 1993 | title = Fungal endophytes: out of sight but should not be out of mind | journal = Oikos | volume = 68 | issue = 2| pages = 379–384 | doi = 10.2307/3544856 | jstor = 3544856| bibcode = 1993Oikos..68..379W }}{{cite journal | last1 = Funk | first1 = C.R. | last2 = Halisky | first2 = P.M. | last3 = Johnson | first3 = M.C. | last4 = Siegel | first4 = M.R. | last5 = Stewart | first5 = A.V. | last6 = Ahmad | first6 = S. | last7 = Hurley | first7 = R.H. | last8 = Harvey | first8 = I.C. | year = 1983 | title = An endophytic fungus and resistance to sod webworms: association in Lolium perenne | journal = Biotechnology | volume = 1 | issue = 2| pages = 189–191 | doi = 10.1038/nbt0483-189 | s2cid = 34172988}} Having a mutualistic relationship with endophytic fungi can promote seed production and seed germination rates in some plant species, such as perennial ryegrass (Lolium perenne) and tall fescue (Festuca arundinacea).{{Cite journal |last=Clay |first=K. |date=1987 |title=Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea |url=http://dx.doi.org/10.1007/bf00385251 |journal=Oecologia |volume=73 |issue=3 |pages=358–362 |doi=10.1007/bf00385251 |pmid=28311516 |bibcode=1987Oecol..73..358C |s2cid=22650421 |issn=0029-8549|url-access=subscription }} The fungi can also benefit the growth of the seedlings as it can enhance seedling growth rate, tiller number and height, and overall biomass. 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.{{cite journal | last1 = Gallery | first1 = R.E. | last2 = Dalling | first2 = J.W. | last3 = Arnold | first3 = A.E. | year = 2007 | title = Diversity, host affinity and distribution of seed-infecting fungi: a case-study with neotropical Cecropia | journal = Ecology | volume = 88 | issue = 3| pages = 582–588 | doi = 10.1890/05-1207 | pmid = 17503585 | s2cid = 18922308}} 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'.{{cite journal | last1 = Dalling | first1 = J.W. | last2 = Davis | first2 = A.S. | last3 = Schutte | first3 = B.J. | last4 = Arnold | first4 = A.E. | year = 2011 | title = Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community | journal = Journal of Ecology | volume = 99 | issue = 1| pages = 89–95 | doi = 10.1111/j.1365-2745.2010.01739.x| bibcode = 2011JEcol..99...89D | s2cid = 18903196 | doi-access = free }}

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.{{cite journal | last1 = Van | first1 = Wim H.| last2 = der Putten | first2 = W.H. |name-list-style=vanc | year = 2003 | title = Plant defense belowground and spatiotemporal processes in natural vegetation | url = https://pure.knaw.nl/ws/files/476516/VanderPutten_3157.pdf| journal = Ecology | volume = 84 | issue = 9| pages = 2269–2280 | doi = 10.1890/02-0284 | bibcode = 2003Ecol...84.2269V| hdl = 20.500.11755/8ca02f26-57c5-4774-a00e-fd0ddddff9f6| hdl-access = free }} 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.{{cite journal | last1 = Wardle | first1 = D.A. | last2 = Bardgett | first2 = R.D. | last3 = Klironomos | first3 = J.N. | last4 = Setala | first4 = H. | last5 = Van | first5 = WH| last6 = der Putten | first6 = W.H. | last7 = Wall | first7 = D.H. | year = 2004 | title = Ecological linkages between aboveground and belowground biota | journal = Science | volume = 304 | issue = 5677| pages = 1629–1633 | doi = 10.1126/science.1094875 | pmid = 15192218 | bibcode = 2004Sci...304.1629W | s2cid = 36949807}} 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.{{cite journal | last1 = Molinari | first1 = N. | last2 = Knight | first2 = C. | year = 2010 | title = Correlated evolution of defensive and nutritional traits in native and non-native plants | journal = Bot. J. Linn. Soc. | volume = 163 | issue = 1| pages = 1–13 | doi = 10.1111/j.1095-8339.2010.01050.x | doi-access = free}} As carbon dioxide levels rise, the amplified photosynthesis will increase the pool of carbohydrates available to endophytic partners, potentially altering the strength of associations.{{cite journal | last1 = Dighton | first1 = J. | last2 = Jansen | first2 = A.E. | year = 1991 | title = Atmospheric pollutants and ectomycorrhizas: more questions than answers? | journal = Environ. Pollut. | volume = 73 | issue = 3–4| pages = 179–204 | doi = 10.1016/0269-7491(91)90049-3 | pmid = 15092077| bibcode = 1991EPoll..73..179D }} 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.{{cite journal | last1 = Marks | first1 = S. | last2 = Clay | first2 = K. | year = 1990 | title = Effects of {{CO2}} enrichment, nutrient addition and fungal endophyte-infection on the growth of two grasses | journal = Oecologia | volume = 84 | issue = 2| pages = 207–214 |doi=10.1007/BF00318273| pmid = 28312754 | bibcode = 1990Oecol..84..207M | s2cid = 7201542}}

Levels of herbivory may also increase as temperature and carbon dioxide concentrations rise.{{cite journal | last1 = Currano | first1 = E.D. | last2 = Wilf | first2 = P. | last3 = Wing | first3 = S.L. | last4 = Labandeira | first4 = C.C. | last5 = Lovelock | first5 = E. | last6 = Royer | first6 = D. | year = 2008 | title = Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum | journal = Proceedings of the National Academy of Sciences of the United States of America| volume = 105 | issue = 6| pages = 1960–1964 | doi = 10.1073/pnas.0708646105 | pmid = 18268338 | pmc = 2538865 | bibcode = 2008PNAS..105.1960C| doi-access = free }} 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.{{cite journal | last1 = Marks | first1 = S. | last2 = Lincoln | first2 = D.E. | year = 1996 | title = Antiherbivore defense mutualism under elevated carbon dioxide levels: a fungal endophyte and grass | journal = Environ. Entomol. | volume = 25 | issue = 3| pages = 618–623 | doi = 10.1093/ee/25.3.618| doi-access = free }} 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.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}}

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.{{cite journal | last1 = Bailey | first1 = V. | year = 1903 | title = Sleepy grass and its effect on horses | url = https://zenodo.org/record/1447874| journal = Science | volume = 17 | issue = 427| pages = 392–393 | doi = 10.1126/science.17.427.392 | pmid = 17735119 | bibcode = 1903Sci....17..392B}}{{cite journal | last1 = Nobindro | first1 = U. | year = 1934 | title = Grass poisoning among cattle and goats in Assam | journal = Indian Vet. J. | volume = 10 | pages = 235–236}} 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.{{cite journal | last1 = Siegel | first1 = M.R. | last2 = Latch | first2 = G.C.M. | last3 = Johnson | first3 = M.C. | year = 1985 | title = Acremonium fungal endophytes of tall fescue and perennial ryegrass: significance and control | journal = Plant Dis. | volume = 69 | issue = 2| pages = 179–183}}{{cite journal | last1 = Clay | first1 = K. | year = 1988 | title = Fungal endophytes of grasses – a defensive mutualism between plants and fungi | journal = Ecology | volume = 69 | issue = 1| pages = 10–16 | doi = 10.2307/1943155 | jstor = 1943155| bibcode = 1988Ecol...69...10C }}

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.{{cite journal | last1 = Hartley | first1 = S.E. | last2 = Gange | first2 = A.C. | year = 2009 | title = Impacts of Plant Symbiotic Fungi on Insect Herbivores: Mutualism in a Multitrophic Context | journal = Annu. Rev. Entomol. | volume = 54 | pages = 323–342 | doi = 10.1146/annurev.ento.54.110807.090614 | pmid = 19067635}} 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.{{cite journal | last1 = Fontana | first1 = A. | last2 = Reichelt | first2 = M. | last3 = Hempel | first3 = S. | last4 = Gershenzon | first4 = J. | last5 = Unsicker | first5 = S.B. | year = 2009 | title = The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L | journal = J. Chem. Ecol. | volume = 35 | issue = 7| pages = 833–843 | doi = 10.1007/s10886-009-9654-0 | pmid = 19568812 | pmc = 2712616| bibcode = 2009JCEco..35..833F }} 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.{{cite journal | last1 = Bultman | first1 = T.L. | last2 = Bell | first2 = G. | last3 = Martin | first3 = W.D. | year = 2004 | title = A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass | journal = Ecology | volume = 85 | issue = 3| pages = 679–685 | doi = 10.1890/03-0073| bibcode = 2004Ecol...85..679B }} On the whole, molecular mechanisms behind endophyte-mediated plant defense has been an increasing focus of research over the past ten years.{{cite journal | last1 = Pieterse | first1 = C.M.J. | last2 = Dicke | first2 = M. | year = 2007 | title = Plant interactions with microbes and insects: from molecular mechanisms to ecology | journal = Trends Plant Sci. | volume = 12 | issue = 12| pages = 564–569 | doi = 10.1016/j.tplants.2007.09.004 | pmid = 17997347 | bibcode = 2007TPS....12..564P | hdl = 1874/27851 | hdl-access = free}}{{cite journal | last1 = Zheng | first1 = S.J. | last2 = Dicke | first2 = M. | year = 2008 | title = Ecological genomics of plant-insect interactions: from gene to community | journal = Plant Physiol | volume = 146 | issue = 3| pages = 812–817 | doi = 10.1104/pp.107.111542 | pmid = 18316634 | pmc = 2259077}}

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.{{cite journal | last1 = Simmons | first1 = L. | last2 = Bultman | first2 = T.L. | last3 = Sullivan | first3 = T.J. | year = 2008 | title = Effects of Methyl Jasmonate and an Endophytic Fungus on Plant Resistance to Insect Herbivores | journal = J. Chem. Ecol. | volume = 34 | issue = 12| pages = 1511–1517 | doi = 10.1007/s10886-008-9551-y | pmid = 18925382 | bibcode = 2008JCEco..34.1511S | s2cid = 7083646}} 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.{{cite journal | last1 = Wink | first1 = M. | year = 2008 | title = Plant secondary metabolism: Diversity, function and its evolution | journal = Natural Product Communications | volume = 3 | issue = 8| pages = 1205–1216 | doi = 10.1177/1934578X0800300801 | doi-access = free}}{{cite journal | last1 = Lambais | first1 = M.R. | year = 2001 | title = In silico differential display of defense-related expressed sequence tags from sugarcane tissues infected with diazotrophic endophytes | journal = Genetics and Molecular Biology | volume = 24 | issue = 1| pages = 103–111 | doi = 10.1590/S1415-47572001000100015 | doi-access = free}} This represents an important line of inquiry to pursue, especially in regards to understanding the chemical pathways that can be utilized in biotechnological applications.

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.{{cite journal | last1 = Hoveland | first1 = C.S. | year = 1993 | title = Importance and economic significance of the Acremonium endophytes to performance of animals and grass plant | journal = Agric. Ecosyst. Environ. | volume = 44 | issue = 1| pages = 3–12 | doi = 10.1016/0167-8809(93)90036-O| bibcode = 1993AgEE...44....3H }} 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.{{cite journal | last1 = Jarvis | first1 = B.B. | last2 = Wells | first2 = K.M. | last3 = Lee | first3 = Y.W. | last4 = Bean | first4 = G.A. | last5 = Kommendahl | first5 = T. | last6 = Barros | first6 = C.S. L. | last7 = Barros | first7 = S.S. | year = 1987 | title = Macrocyclic triocothecene mycotoxins in Brazilian species of Baccharis | journal = Phytopathology | volume = 12 | pages = 111–128}} 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.{{cite journal | last1 = Steudemann | first1 = J.A. | last2 = Hoveland | first2 = C.S. | year = 1988 | title = Fescue endophyte: history and impact on animal agricultural | journal = Journal of Production Agriculture| volume = 1 | pages = 39–44 | doi = 10.2134/jpa1988.0039}} Reduced frequency of pregnancy and birth has also been reported in cattle and horses fed with infected forage. Endophytic fungi can even cause severe toxicity in grazing livestock, which is often referred to as fescue toxicosis.{{Cite journal |last1=Belesky |first1=David P. |last2=Bacon |first2=Charles W. |date=August 2009 |title=Tall fescue and associated mutualistic toxic fungal endophytes in agroecosystems |url=http://www.tandfonline.com/doi/full/10.1080/15569540903082143 |journal=Toxin Reviews |language=en |volume=28 |issue=2–3 |pages=102–117 |doi=10.1080/15569540903082143 |s2cid=85900080 |issn=1556-9543|url-access=subscription }} Cattle that graze on tall fescue (Festuca arundinacea) develop symptoms such as fescue foot, fat necrosis and summer slump, which is a general malady of fescue toxicosis. Fungi, plants and herbivore population sizes can have a cyclical predator-prey pattern. Infection rates of endophytic fungi in plants tend to increase with rise in grazing pressure.{{Cite journal |last1=Bazely |first1=Dawn R. |last2=Vicari |first2=Mark |last3=Emmerich |first3=Samantha |last4=Filip |first4=Lynda |last5=Lin |first5=David |last6=Inman |first6=Alastair |date=August 1997 |title=Interactions between Herbivores and Endophyte-Infected Festuca rubra from the Scottish Islands of St. Kilda, Benbecula and Rum |url=http://dx.doi.org/10.2307/2405276 |journal=The Journal of Applied Ecology |volume=34 |issue=4 |pages=847 |doi=10.2307/2405276 |jstor=2405276 |bibcode=1997JApEc..34..847B |issn=0021-8901|url-access=subscription }} If endophytic fungi becomes highly prevalent in grazer food sources, it can even lead to population crashes in grazing animals. 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.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. The organic farming industry has embraced mycorrhizal symbionts as one tool for improving yields and protecting plants from damage.{{cite journal | last1 = Shrivastava | first1 = G. | last2 = Rogers | first2 = M. | last3 = Wszelaki | first3 = A. | last4 = Panthee | first4 = D.R. | last5 = Chen | first5 = F. | year = 2010 | title = Plant Volatiles-based Insect Pest Management in Organic Farming | journal = Critical Reviews in Plant Sciences | volume = 29 | issue = 2| pages = 123–133 | doi=10.1080/07352681003617483| bibcode = 2010CRvPS..29..123S | s2cid = 84573807}} Infected crops of soybean,{{cite journal | last1 = Rabin | first1 = L.B. | last2 = Pacovsky | first2 = R.S. | year = 1985 | title = Reduced larva growth of two Lepidoptera (Noctuidae) on excised leaves of soybean infected with amycorrhizal fungus | journal = J. Econ. Entomol. | volume = 78 | issue = 6| pages = 1358–1363 | doi=10.1093/jee/78.6.1358}} ribwort plantain,{{cite journal | last1 = Gange | first1 = A.C. | last2 = West | first2 = H.M. | year = 1994 | title = Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L | journal = New Phytol | volume = 128 | issue = 1 | pages = 79–87 | doi = 10.1111/j.1469-8137.1994.tb03989.x| pmid = 33874534 | doi-access = free | bibcode = 1994NewPh.128...79G }} cabbage, banana,{{cite journal | last1 = Akello | first1 = J. | last2 = Dubois | first2 = T. | last3 = Coyne | first3 = D. | last4 = Kyamanywa | first4 = S. | year = 2008 | title = Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage | journal = Crop Protection | volume = 27 | issue = 11| pages = 1437–1441 | doi = 10.1016/j.cropro.2008.07.003| bibcode = 2008CrPro..27.1437A }} coffee bean plant and tomato{{cite journal | last1 = Jallow | first1 = M.F.A. | last2 = Dugassa-Gobena | first2 = D. | last3 = Vidal | first3 = S. | year = 2004 | title = Indirect interaction between and unspecialized endophytic fungus and a polyphagous moth | journal = Basic and Applied Ecology | volume = 5 | issue = 2| pages = 183–191 | doi = 10.1078/1439-1791-00224| bibcode = 2004BApEc...5..183J | url = https://resolver.sub.uni-goettingen.de/purl?gro-2/49040 }} 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.{{cite book |last1=Dent |first1=David |title=Insect pest management |date=2000 |publisher=CABI Pub |location=Wallingford, Oxon, UK; New York, NY, USA |isbn=0-85199-340-0 |edition=2nd}} 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.{{cite journal | last1 = Murray | first1 = F.R. | last2 = Latch | first2 = G.M.C. | last3 = Scott | first3 = D.B. | year = 1992 | title = Surrogate transformation of perennial ryegrass, Lolium perenne, using genetically modified Acremonium endophyte | journal = Mol. Gen. Genet. | volume = 233 | issue = 1–2| pages = 1–9 | doi = 10.1007/BF00587554 | pmid = 1603053 | s2cid = 12900163}}

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.{{cite journal | last1 = Shennan | first1 = C. | year = 2008 | title = Biotic interactions, ecological knowledge and agriculture | journal = Phil. Trans. R. Soc. B | volume = 363 | issue = 1492| pages = 717–739 | doi = 10.1098/rstb.2007.2180 | pmid = 17761466 | pmc = 2610106}} 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.

File:Ergotamine3.png, a mycotoxin produced by Claviceps spp. which infects rye and related grasses, causing poisoning of livestock and humans]]

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.{{cite book |editor1-last=Black |editor1-first=Michael |editor2-last=Bewley |editor2-first=J. Derek |editor3-last=Halmer |editor3-first=Peter |title=The encyclopedia of seeds: Science, technology and uses |date=2006 |publisher=CABI |location=Wallingford |isbn=978-0-85199-723-0 |page=226}} Drugs used to treat Parkinson's disease have been created from isolates of ergot toxins, although health risks may accompany their use.{{cite journal | last1 = Schade | first1 = R. | last2 = Andersohn | first2 = F. | last3 = Suissa | first3 = S. | last4 = Haverkamp | first4 = W. | last5 = Garbe | first5 = E. | year = 2007 | title = Dopamine agonists and the risk of cardiac-valve regurgitation | journal = New England Journal of Medicine | volume = 356 | issue = 1| pages = 29–38 | doi = 10.1056/NEJMoa062222 | pmid = 17202453| doi-access = free }} Ergotamine has also been used to synthesize lysergic acid diethylamide because of its chemical similarity to lysergic acid.{{cite journal | last1 = Correia | first1 = T. | last2 = Grammel | first2 = N. | last3 = Ortel | first3 = I. | last4 = Keller | first4 = U. | last5 = Tudzynski | first5 = P. | year = 2001 | title = Molecular cloning and analysis of the ergopeptine assembly system in the ergot fungus Claviceps purpurea | journal = Chem. Biol. | volume = 10 | issue = 12| pages = 1281–1292 | doi = 10.1016/j.chembiol.2003.11.013 | pmid = 14700635 | doi-access = free}} 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.Gray, W.D. (1959). The Relation of Fungi to Human Affairs. New York: Henry Holt and Company, Inc.

• Arbuscular mycorrhiza
• Chemical ecology
• Endophytes
• Glomeromycota
• Interspecies communication
• Mutualism
• Mycorrhizae
• Plant defense against herbivory

{{Reflist|2}}

• {{Cite book|author1=Redlin, S.C. |author2=Carris, L.M. |name-list-style=amp |year=1996 |title=Endophytic fungi in grasses and woody plants: Systematics, ecology, and evolution|location=St. Paul, Minn |publisher=APS Press |isbn=978-0-89054-213-2}}
• {{Cite book|author1=Cheplick, G.P. |author2=Faeth, S.H. |name-list-style=amp |year=2009 |title=Ecology and evolution of the grass-endophyte symbiosis |url=https://books.google.com/books?id=wkfuA5D2UNQC&pg=PP1 |location=Oxford |publisher=Oxford University Press|isbn=978-0-19-530808-2}}
• {{Cite book|author1=Bacon, C.W. |author2=White, J.F. |name-list-style=amp |year=1994 |title=Biotechnology of endophytic fungi of grasses |location=Boca Raton |publisher=CRC Press |isbn=978-0-8493-6276-7}}
• {{Cite book|author1=White, J.F. |author2=Torres, M.S. |name-list-style=amp |year=2009 |title=Defensive mutualism in microbial symbiosis |location=Boca Raton |publisher=CRC Press |isbn=978-1-4200-6931-0}}
• {{Cite book|author1=Heijden, M.G.A. |author2=Sanders, I.R. |name-list-style=amp |year=2002 |title=Mycorrhizal ecology |location=Berlin |publisher=Springer |isbn= 978-3-540-42407-9}}
• Belesky, D. P., & Bacon, C. W. (2009) Tall fescue and associated mutualistic toxic fungal endophytes in agroecosystems. Toxin Reviews. 28(2-3): 102-117 doi:10.1080/15569540903082143
• Bazely, D. R., Vicari, M., Emmerich, S., Filip, L., Lin, D., & Inman, A. (1997). Interactions between herbivores and Endophyte-Infected Festuca rubra from the Scottish Islands of St. Kilda, Benbecula and Rum. British Ecological Society. 34(4):847–860 https://doi.org/10.2307%2F2405276
• Ahlholm, J. U., M. Helander, S. Lehtimaki, P. Wali, & K. Saikkonen. (2002). Vertically transmitted fungal endophytes: different responses of host parasite systems to environmental conditions. OIKOS 99:173183. https://doi.org/10.1034%2Fj.1600-0706.2002.990118.x
• Clay, K. (1987). Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia (Berline). 73: 358–362 https://doi.org/10.1007%2Fbf00385251
• Li, X., Song, M., Yao, X., Chai, Q., Simpson, W. R., Li, C., & Nan, Z. (2017) The Effect of Seed-Borne Fungi and Epichloë Endophyte on Seed Germination and Biomass of Elymus sibiricus. Frontiers in Microbiology 8: 2488 https://doi.org/10.3389%2Ffmicb.2017.02488

• [http://mycorrhizas.info/index.html Mycorrhizal Associations: The Web Resource] – Comprehensive illustrations and lists of mycorrhizal and nonmycorrhizal plants and fungi
• [http://www.mycorrhizas.org/ International Mycorrhiza Society]
• [https://web.archive.org/web/20080509170441/http://mycorrhiza.ag.utk.edu/ Mycorrhizal Literature Exchange] – Database of abstracts, reviews, books, theses and dissertations hosted by the University of Tennessee
• [http://www2.mcdaniel.edu/Biology/botf99/herbnew/aintro.htm Plant Defense Systems and Medicinal Botany] {{Webarchive|url=https://web.archive.org/web/20070105193927/http://www2.mcdaniel.edu/Biology/botf99/herbnew/aintro.htm |date=2007-01-05 }} – Explanations of plant defensive chemicals and their use by humans

Category:Herbivory

Category:Plant roots

Category:Soil biology

Category:Symbiosis

Category:Mycology

Category:Plant physiology

Category:Biological pest control

Category:Sustainable agriculture