Abstract
Due to increasingly limited water resources, diminishing farmland acreage, and potentially negative effects of climate change, an urgent need exists to improve agricultural productivity to feed the ever-growing population. Plants interact with microorganisms at all trophic levels, adapting growth, developmental, and defense responses within a complicated network of community members. Endophytic fungi have been widely reported for their ability to aid in the defense of their host plants. Currently, many reports focus on the application of endophytic fungi with the capability to produce valuable bioactive molecules, while others focus on endophytic fungi as biocontrol agents. Plant responses upon endophytic fungi colonization are also good for the immune system of the plant. In this paper, the possible mechanisms between endophytic fungi and their hosts were reviewed. During long-term evolution, plants have acquired numerous beneficial strategies in response to endophytic fungi colonization. The interaction of endophytic fungi with plants modulates the relationship between plants and both biotic and abiotic stresses. It has previously been reported that this endophytic relationship confers additional defensive mechanisms on the modulation of the plant immune system, as the result of the manipulation of direct antimicrobial metabolites such as alkaloids to indirect phytohormones, jasmonic acid, or salicylic acid. Furthermore, plants have evolved to cope with combinations of stresses and experiments are required to address specific questions related to these multiple stresses. This review summarizes our current understanding of the intrinsic mechanism to better utilize these benefits for plant growth and disease resistance. It contributes new ideas to increase plant fitness and crop productivity.
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References
Abeer H, Abd Allah EF, Alqarawi AA, Al-Huqail AA, Stephan W, Dilfuza E (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardiiunder salt stress. Front Microbiol 7:1089. https://doi.org/10.3389/fmicb.2016.01089
Adame-Alvarez RM, Mendiola-Soto J, Heil M (2014) Order of arrival shifts endophyte-pathogen interactions in bean from resistance induction to disease facilitation. FEMS Microbiol Lett 355(2):100–107. https://doi.org/10.1111/1574-6968.12454
Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, Weigel D, Kemen EM (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14(1):e1002352. https://doi.org/10.1371/journal.pbio.1002352
Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77(1):36–44. https://doi.org/10.1016/j.sajb.2010.05.003
Ana G, Joana F, Marta SS, Andreia F (2016) Linking jasmonic acid to grapevine resistance against the biotrophic oomycete Plasmopara viticola. Front Plant Sci 7:565. https://doi.org/10.3389/fpls.2016.00565
Azooz MM, Youssef AM, Ahmad P (2011) Evaluation of salicylic acid (SA) application on growth, osmotic solutes and antioxidant enzyme activities on broad bean seedlings grown under diluted seawater. Int J Plant Physiol Biochem 3(14):253–264. https://doi.org/10.5897/IJPPB11.052
Bacon CW, White JF (2016) Functions, mechanisms and regulation of endophytic and epiphytic microbial communities of plants. Symbiosis 68(1-3):87–98. https://doi.org/10.1007/s13199-015-0350-2
Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol 34(5):576–581
Bai Y, Kissoudis C, Yan Z, Visser RGF, van der Linden G (2017) Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. Plant J 93(4):781–793. https://doi.org/10.1111/tpj.13800
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I (2008) Salt tolerance of barley induced by the root endophyte Piriformospora Indica is associated with a strong increase in antioxidants. New Phytol 180(2):501–510. https://doi.org/10.1111/j.1469-8137.2008.02583.x
Bano A, Ullah F, Nosheen A (2012) Role of abscisic acid and drought stress on the activities of antioxidant enzymes in wheat. Plant Soil Environ 58(4):181–185. https://doi.org/10.17221/210/2011-PSE
Bastias DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE (2017) Epichloë fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22:939–948. https://doi.org/10.1016/j.tplants.2017.08.005
Bastias DA, Martinez-Ghersa MA, Newman JA, Card SD, Mace WJ, Gundel PE (2018) The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell Environ 41(2):395–405. https://doi.org/10.1111/pce.13102
Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13(9):492–498. https://doi.org/10.1016/j.tplants.2008.07.001
Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP, Tuskan G, Schadt CW, Vilgalys R (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23(13):3356–3370. https://doi.org/10.1111/mec.12821
Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A (2017) Ecology and genomic insights on plant-pathogenic and -nonpathogenic endophytes. Annu Rev Phytopathol 55(1):61–83. https://doi.org/10.1146/annurev-phyto-080516-035641
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91–95. https://doi.org/10.1038/nature11336
Busby PE, Ridout M, Newcombe G (2015) Fungal endophytes: modifiers of plant disease. Plant Mol Biol 90(6):645–655. https://doi.org/10.1007/s11103-015-0412-0
Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15(3):e2001793. https://doi.org/10.1371/journal.pbio.2001793
Carroll GC (1986) The biology of endophytism in plants with particular reference to woody perennials. In: Fokkema NJ, van den Heuvel J (eds) Microbiology of the phyllosphere. ). Cambridge University Press, Cambridge, pp 205–222
Carroll G (1988) Fungal endophytes in stems and leaves - from latent pathogen to mutualistic symbiont. Ecology 69(1):2–9. https://doi.org/10.2307/1943154
Carvalho TLG, Ballesteros HGF, Thiebaut F, Ferreira PCG, Hemerly AS (2016) Nice to meet you: genetic, epigenetic and metabolic controls of plant perception of beneficial associative and endophytic diazotrophic bacteria in non-leguminous plants. Plant Mol Biol 90:561–574. https://doi.org/10.1007/s11103-016-0435-1
Chagas FO, Pessotti RD, Caraballo-Rodriguez AM, Pupo MT (2018) Chemical signaling involved in plant-microbe interactions. Chem Soc Rev 47(5):1652–1704. https://doi.org/10.1039/c7cs00343a
Che JX, Shi JL, Gao ZH, Zhang Y (2016a) A new approach to produce resveratrol by enzymatic bioconversion. J Microbiol Biotechnol 26(8):1348–1357. https://doi.org/10.4014/jmb.1512.12084
Che JX, Shi JL, Gao ZH, Zhang Y (2016b) Transcriptome analysis reveals the genetic basis of the resveratrol biosynthesis pathway in an endophytic fungus (Alternaria sp. MG1) isolated from Vitis Vinifera. Front Microbiol 7:1–12. https://doi.org/10.3389/fmicb.2016.01257
Clay K (1989) Clavicipitaceolls endophytes of grasses: their potential as biocontrol agents. Mycol Res 92:1–12. https://doi.org/10.1016/S0953-7562(89)80088-7
Cline LC, Schilling JS, Menke J, Groenhof E, Kennedy PG (2018) Ecological and functional effects of fungal endophytes on wood decomposition. Funct Ecol 32(1):181–191. https://doi.org/10.1111/1365-2435.12949
Cummins M, Huitema E (2017) Effector-decoy pairs: another countermeasure emerging during host-microbe co-evolutionary arms races? Mol Plant 10(5):662–664. https://doi.org/10.1016/j.molp.2017.03.008
De Bary A (1866) Morphologie und Physiologie der Pilze, Flechten und Myxomyceten. Hofmeister’s Handbook of Physiological Botany, Volume II. Engelmann, Leipzig, Germany
Douanla-Meli C, Langer E, Talontsi Mouafo F (2013) Fungal endophyte diversity and community patterns in healthy and yellowing leaves of Citrus limon. Fungal Ecol 6(3):212–222. https://doi.org/10.1016/j.funeco.2013.01.004
Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180(2):190–195. https://doi.org/10.1016/j.plantsci.2010.10.002
Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112(8):E911–E920. https://doi.org/10.1073/pnas.1414592112
Egamberdieva D, Wirth S, Alqarawi A, Abd Allah EF, Hashem A (2017a) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104. https://doi.org/10.3389/Fmicb.2017.02104
Egamberdieva D, Wirth SJ, Shurigin VV, Hashem A, Abd Allah EF (2017b) Endophytic bacteria improve plant growth, symbiotic performance of Chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8:1887. https://doi.org/10.3389/fmicb.2017.01887
Etalo D, Jeon JS, Raaijmakers JM (2018) Modulation of plant chemistry by beneficial root microbiota. Nat Prod Rep 35(5):398–409. https://doi.org/10.1039/c7np00057j
Fässler E, Evangelou MW, Robinson BH, Schulin R (2010) Effects of indole-3-acetic acid (IAA) on sunflower growth and heavy metal uptake in combination with ethylene diamine disuccinic acid (EDDS). Chemosphere 80(8):901–907. https://doi.org/10.1016/j.chemosphere.2010.04.077
Ferrara FIDS, Oliveira ZM, Gonzales HHS, Floh EIS, Barbosa HR (2012) Endophytic and rhizospheric enterobacteria isolated from sugar cane have different potentials for producing plant growth-promoting substances. Plant Soil 353(1-2):409–417. https://doi.org/10.1007/s11104-011-1042-1
Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Curr Opin Microbiol 32:103–112. https://doi.org/10.1016/j.mib.2016.05.008
Gagic M, Faville MJ, Zhang W, Forester NT, Rolston MP, Johnson RD, Ganesh S, Koolaard JP, Easton HS, Hudson D, Johnson LJ, Moon CD, Voisey CR (2018) Seed transmission of Epichloë endophytes in Lolium perenne is heavily influenced by host genetics. Front Plant Sci 9:1580. https://doi.org/10.3389/Fpls.2018.01580
Glynou K, Ali T, Buch AK, Haghi Kia S, Ploch S, Xia X, Celik A, Thines M, Macia-Vicente JG (2016) The local environment determines the assembly of root endophytic fungi at a continental scale. Environ Microbiol 18(8):2418–2434. https://doi.org/10.1111/1462-2920.13112
Gundale MJ, Almeida JP, Wallander H, Wardle DA, Kardol P, Nilsson M-C, Fajardo A, Pauchard A, Peltzer DA, Ruotsalainen S, Mason B, Rosenstock N, Austin A (2016) Differences in endophyte communities of introduced trees depend on the phylogenetic relatedness of the receiving forest. J Ecol 104(5):1219–1232. https://doi.org/10.1111/1365-2745.12595
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol R 79(3):293–320. https://doi.org/10.1128/Mmbr.00050-14
Hassani MA, Duran P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6(1):58. https://doi.org/10.1186/s40168-018-0445-0
Hiruma K, Gerlach N, Sacristan S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramirez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165(2):464–474. https://doi.org/10.1016/j.cell.2016.02.028
Hodgson S, de Cates C, Hodgson J, Morley NJ, Sutton BC, Gange AC (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4(8):1199–1208. https://doi.org/10.1002/ece3.953
Huang J, Gu L, Zhang Y, Yan T, Kong G, Kong L, Guo B, Qiu M, Wang Y, Jing M, Xing W, Ye W, Wu Z, Zhang Z, Zheng X, Gijzen M, Wang Y, Dong S (2017) An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun 8(1):2051. https://doi.org/10.1038/s41467-017-02233-5
Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33(33):163–173. https://doi.org/10.1002/yea.1639
Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schafer P (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica (vol 156, pg 726, 2011). Plant Physiol 157(1):531–531. https://doi.org/10.1104/pp.111.900420
Janda K, Hideg E, Szalai G, Kovács L, Janda T (2012) Salicylic acid may indirectly influence the photosynthetic electron transport. J Plant Physiol 169(10):971–978. https://doi.org/10.1016/j.jplph.2012.02.020
Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2013) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 35(1):62–74. https://doi.org/10.3109/07388551.2013.800018
Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9:2732. https://doi.org/10.3389/fmicb.2018.02732
Kunkel BA, Grewal PS, Quigley MF (2004) A mechanism of acquired resistance against an entomopathogenic nematode by Agrotis ipsilon feeding on perennial ryegrass harboring a fungal endophyte. Biol Control 29(1):100–108. https://doi.org/10.1016/S1049-9644(03)00119-1
Kusari S, Kosuth J, Cellarova E, Spiteller M (2011) Survival-strategies of endophytic Fusarium solani against indigenous camptothecin biosynthesis. Fungal Ecol 4(3):219–223. https://doi.org/10.1016/j.funeco.2010.11.002
Kusari S, Hertweck C, Spiteller M (2012a) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19(7):792–798. https://doi.org/10.1016/j.chembiol.2012.06.004
Kusari S, Verma VC, Lamshoeft M, Spiteller M (2012b) An endophytic fungus from Azadirachta indica A. Juss that produces azadirachtin. World J Microbiol Biotechnol 28(3):1287–1294. https://doi.org/10.1007/s11274-011-0876-2
Le Van A, Quaiser A, Duhamel M, Michon-Coudouel S, Dufresne A, Vandenkoornhuyse P (2017) Ecophylogeny of the endospheric root fungal microbiome of co-occurring Agrostis stolonifera. PeerJ 5:e3454. https://doi.org/10.7717/peerj.3454
Li XJ, Zhang Q, Zhang AL, Gao JM (2012) Metabolites from Aspergillus fumigatus, an endophytic fungus associated with Melia azedarach, and their antifungal, antifeedant, and toxic activities. J Agric Food Chem 60(13):3424–3431. https://doi.org/10.1021/jf300146n
Li XZ, Song ML, Yao X, Chai Q, Simpson WR, Li CJ, Nan ZB (2017) The effect of seed-borne fungi and Epichloë endophyte on seed germination and biomass of Elymus sibiricus. Front Microbiol 8:2488. https://doi.org/10.3389/Fmicb.2017.02488
Liu HW, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552
Lopez DC, Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53–60. https://doi.org/10.1016/j.biocontrol.2015.03.010
Lopezgomez M, Sandal N, Stougaard J, Boller T (2012) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot 63(1):393–401. https://doi.org/10.1093/jxb/err291
Lu Y, Shao DY, Shi JL, Huang QS, Yang H, Jin ML (2016) Strategies for enhancing resveratrol production and the expression of pathway enzymes. Appl Microbiol Biotechnol 100:7404–7421. https://doi.org/10.1007/s00253-016-7723-1
Lu Y, Ye C, Che JX, Xu XG, Shao DY, Jiang CM, Liu YL, Shi JL (2019) Genomic sequencing, genome-scale metabolic network reconstruction, and in silico flux analysis of the grape endophytic fungus Alternaria sp. MG1. Microb Cell Factories 18:13. https://doi.org/10.1186/s12934-019-1063-7
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Ma ZC, Song TQ, Zhu L, Ye WW, Wang Y, Shao YY, Dong SM, Zhang ZG, Dou DL, Zheng XB, Tyler BM, Wang YC (2015) A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell 27(7):2057–2072. https://doi.org/10.1105/tpc.15.00390
Ma ZC, Zhu L, Song TQ, Wang Y, Zhang Q, Xia YQ, Qiu M, Lin YC, Li HY, Kong L, Fang YF, Ye WW, Wang Y, Dong SM, Zheng XB, Tyler BM, Wang YC (2017) A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355(6326):710–714. https://doi.org/10.1126/science.aai7919
Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, Stitt J, Shi Z, Zhang YF, Guiltinan MJ, Maximova SN (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479. https://doi.org/10.3389/fmicb.2014.00479
Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, Mukherjee PK (2018) Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol Rev 32(2):62–85. https://doi.org/10.1016/j.fbr.2017.12.001
Mousa WK, Raizada MN (2015) Biodiversity of genes encoding anti-microbial traits within plant associated microbes. Front Plant Sci 6(231):231. https://doi.org/10.3389/Fpls.2015.00231
Mousa WK, Adrian S, Jeffrey D, Philip S, Liu H, Zhou T, France-Isabelle A, Raizada MN (2015) An endophytic fungus isolated from finger millet (Eleusine coracana) produces anti-fungal natural products. Front Microbiol 6:1157. https://doi.org/10.3389/Fmicb.2015.01157
Mousa WK, Shearer C, Limayrios V, Ettinger CL, Eisen JA, Raizada MN (2016) Root-hair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen. Nat Microbiol 1:16167. https://doi.org/10.1038/Nmicrobiol.2016.167
Muller H, Berg C, Landa BB, Auerbach A, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front Microbiol 6:138. https://doi.org/10.3389/fmicb.2015.00138
Nogueira-Lopez G, Greenwood DR, Middleditch M, Winefield C, Eaton C, Steyaert JM, Mendoza-Mendoza A (2018) The apoplastic secretome of Trichoderma virens during interaction with maize roots shows an inhibition of plant defence and scavenging oxidative stress secreted proteins. Front Plant Sci 9:409. https://doi.org/10.3389/fpls.2018.00409
Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 98(3):267–270. https://doi.org/10.1016/j.jip.2008.01.010
Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial Ecology of Leaves. Springer, New York, pp 179–197
Powell JR, Karunaratne S, Campbell CD, Yao H, Robinson L, Singh BK (2015) Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun 6:8444. https://doi.org/10.1038/ncomms9444
Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205(4):1431–1436. https://doi.org/10.1111/nph.13252
Ray S, Mishra S, Bisen K, Singh S, Sarma BK, Singh HB (2018) Modulation in phenolic root exudate profile of Abelmoschus esculentus expressing activation of defense pathway. Microbiol Res 207:100–107. https://doi.org/10.1016/j.micres.2017.11.011
Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289(5486):1920–1921. https://doi.org/10.1126/science.289.5486.1920
Rodrigo S, Santamaria O, Halecker S, Lledó S, Stadler M (2017) Antagonism between Byssochlamys spectabilis (anamorph Paecilomyces variotii) and plant pathogens: involvement of the bioactive compounds produced by the endophyte. Ann Appl Biol 171(3):464–476. https://doi.org/10.1111/aab.12388
Rodriguez RJ, Jr WJ, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–326. https://doi.org/10.1111/j.1469-8137.2009.02773.x
Rosier A, Bishnoi U, Lakshmanan V, Sherrier DJ, Bais HP (2016) A perspective on inter-kingdom signaling in plant-beneficial microbe interactions. Plant Mol Biol 90(6):537–548. https://doi.org/10.1007/s11103-016-0433-3
Ruhe J, Agler MT, Placzek A, Kramer K, Finkemeier I, Kemen EM (2016) Obligate biotroph pathogens of the genus albugo are better adapted to active host defense compared to niche competitors. Front Plant Sci 7:820. https://doi.org/10.3389/Fpls.2016.00820
Sasse J, Martinoia E, Northen T (2017) Feed your friends: doplant exudates shape the root microbiome? Trends Plant Sci 23(1):25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND (2013) Currencies of mutualisms: sources of alkaloid genes in vertically transmitted Epichloae. Toxins 5(6):1064–1088. https://doi.org/10.3390/toxins5061064
Schulz B, Römmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism. Myco Res 103:1275–1283. https://doi.org/10.1021/jo701704x
Schulz B, Haas S, Junker C, Andree N, Schobert M (2015) Fungal endophytes are involved in multiple balanced antagonisms. Curr Sci India 109(1):39–45
Shahzad R, Waqas M, Khan AL, Asaf S, Khan MA, Kang SM, Yun BW, Lee IJ (2016) Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243. https://doi.org/10.1016/j.plaphy.2016.05.006
Shahzad R, Khan AL, Bilal S, Waqas M, Kang SM, Lee IJ (2017) Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ Exp Bot 136:68–77. https://doi.org/10.1016/j.envexpbot.2017.01.010
Shehata HR, Ettinger CL, Eisen JA, Raizada MN (2016) Genes required for the anti-fungal activity of a bacterial endophyte isolated from a corn landrace grown continuously by subsistence farmers since 1000 BC. Front Microbiol 7:1548. https://doi.org/10.3389/fmicb.2016.01548
Shikano I, Rosa C, Tan CW, Felton GW (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annu Rev Phytopathol 55:313–331. https://doi.org/10.1146/annurev-phyto-080516-035319
Shrivastava G, Ownley BH, Augé RM, Toler H, Dee M, Vu A, Köllner TG, Chen F (2015) Colonization by Arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis 65(2):65–74. https://doi.org/10.1007/s13199-015-0319-1
Siddaiah CN, Satyanarayana NR, Mudili V, Gupta VK, Gurunathan S, Rangappa S, Huntrike SS, Srivastava RK (2017) Elicitation of resistance and associated defense responses in Trichoderma hamatum induced protection against pearl millet downy mildew pathogen. Sci Rep 7:43991. https://doi.org/10.1038/Srep43991
Silva ACD, Suassuna JF, Melo ASD, Costa RR, Andrade WLD, Silva DCD, Silva ACD, Suassuna JF, Melo ASD, Costa RR (2017) Salicylic acid as attenuator of drought stress on germination and initial development of sesame. Rev Bras Eng Agr Amb 21(3):156–162. https://doi.org/10.1590/1807-1929/agriambi.v21n3p156-162
Soliman SSM, Raizada MN (2013) Interactions between co-habitating fungi elicit synthesis of taxol from an endophytic fungus in host taxus plants. Front Microbiol 4(1):3. https://doi.org/10.3389/fmicb.2013.00003
Soliman SSM, Greenwood JS, Bombarely A, Mueller LA, Tsao R, Mosser DD, Raizada MN (2015) An endophyte constructs fungicide-containing extracellular barriers for its host plant. Curr Biol 25(19):2570–2576. https://doi.org/10.1016/j.cub.2015.08.027
Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167(12):1009–1017. https://doi.org/10.1016/j.jplph.2010.02.013
Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Gopalan V (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54(1):19–30. https://doi.org/10.1007/s13225-012-0168-7
Terhonen E, Sipari N, Asiegbu FO (2016) Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biol Control 99:53–63. https://doi.org/10.1016/j.biocontrol.2016.04.006
Toju H, Yamamoto S, Sato H, Tanabe AS (2013) Sharing of diverse mycorrhizal and root-endophytic fungi among plant species in an oak-dominated cool-temperate forest. PLoS One 8(10):e78248. https://doi.org/10.1371/journal.pone.0078248
Vandenkoornhuyse P, Quaiser A, Duhamel M, Van AL, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206(4):1196–1206. https://doi.org/10.1111/nph.13312
Venugopalan A, Srivastava S (2015) Endophytes as in vitro production platforms of high value plant secondary metabolites. Biotechnol Adv 33(6):873–887. https://doi.org/10.1016/j.biotechadv.2015.07.004
Viterbo A, Chet I (2006) TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7(4):249–258. https://doi.org/10.1111/j.1364-3703.2006.00335.x
Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He J, Liu X, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. The ISME journal 7(7):1310–1321. https://doi.org/10.1038/ismej.2013.30
Wang JL, Li T, Liu GY, Smith JM, Zhao ZW (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Rep 6:22028. https://doi.org/10.1038/srep22028
Wani ZA, Mirza DN, Arora P, Riyaz-Ul-Hassan S (2016) Molecular phylogeny, diversity, community structure, and plant growth promoting properties of fungal endophytes associated with the corms of saffron plant: An insight into the microbiome of Crocus sativus Linn. Fungal biol-UK 120(12):1509–1524. https://doi.org/10.1016/j.funbio.2016.07.011
Wawra S, Fesel P, Widmer H, Timm M, Seibel J, Leson L, Kesseler L, Nostadt R, Hilbert M, Langen G, Zuccaro A (2016) The fungal-specific beta-glucan-binding lectin FGB1 alters cell-wall composition and suppresses glucan-triggered immunity in plants. Nat commun 7:13188. https://doi.org/10.1038/Ncomms13188
Wiewiora B, Zurek G, Panka D (2015) Is the vertical transmission of Neotyphodium lolii in perennial ryegrass the only possible way to the spread of endophytes? PLoS One 10(2):e0117231. https://doi.org/10.1371/journal.pone.0117231
Xie ZC, Chu YK, Zhang WJ, Lang DY (2019) Zhang XH (2019) Bacillus pumilus alleviates drought stress and increases metabolite accumulation in Glycyrrhiza uralensis Fisch. Environ Exp Bot 158:99–106. https://doi.org/10.1016/j.envexpbot.2018.11.021
Yan L, Zhao HB, Zhao XX, Xu XG, Di YC, Jiang CM, Shi JL, Shao DY, Huang QS, Yang H, Jin ML (2018) Production of bioproducts by endophytic fungi: chemical ecology, biotechnological applications, bottlenecks, and solutions. Appl Microbiol Biotechnol 102(15):6279–6298. https://doi.org/10.1007/s00253-018-9101-7
Yang YF, Zhao HN, Barrero RA, Zhang BH, Sun GL, Wilson IW, Xie FL, Walker KD, Parks JW, Bruce R, Guo GW, Chen L, Zhang Y, Huang X, Tang Q, Liu HW, Bellgard MI, Qiu DY, Lai JS, Hoffman A (2014) Genome sequencing and analysis of the paclitaxel-producing endophytic fungus Penicillium aurantiogriseum NRRL 62431. BMC Genomics 15:69. https://doi.org/10.1186/1471-2164-15-69
Yao YQ, Lan F, Qiao YM, Wei JG, Huang RS, Li LB (2017) Endophytic fungi harbored in the root of Sophora tonkinensis gapnep: diversity and biocontrol potential against phytopathogens. Microbiologyopen 6(3):e00437. https://doi.org/10.1002/mbo3.437
Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65(3):1061–1070. https://doi.org/10.1002/(SICI)1097-0290(19990305)62:5<609::AID-BIT13>3.0.CO;2-C
Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe In 25(2):139–150. https://doi.org/10.1094/MPMI-06-11-0179
Zhang Y, Shi JL, Gao Z, Yangwu R, Jiang H, Che J, Liu YL (2015) Production of pinoresinol diglucoside, pinoresinol monoglucoside, and pinoresinol by Phomopsis sp. XP-8 using mung bean and its major components. Appl Microbiol Biotechnol 99:4629–4643. https://doi.org/10.1007/s00253-015-6491-7
Zhang YW, Zhao HB, Di YC, Li Q, Shao DY, Shi JL, Huang QS (2018) Antitumor activity of Pinoresinol in vitro: Inducing apoptosis and inhibiting I HepG2 invasion. J Funct Foods 45:206–214. https://doi.org/10.1016/j.jff.2018.04.009
Zhao XX, Zhang Y, Shi JL, Liu YL, Lu Y, Lian ZY (2019) Biosynthesis of antibacterial compound against multidrug resistant foodborne pathogens by Phomopsis sp. XP-8. Food Control 96:223–231. https://doi.org/10.1016/j.foodcont.2018.08.007
Zhu J, Yan L, Xu X, Zhang Y, Shi J, Jiang C, Shao D (2018) Strategies to enhance the production of pinoresinol and its glucosides by endophytic fungus (Phomopsis sp. XP-8) isolated from Tu-chung bark. AMB Express 8(1):55. https://doi.org/10.1186/s13568-018-0584-5
Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543(7645):328–336. https://doi.org/10.1038/nature22009
Zuccaro A, Lahrmann U, Langen G (2014) Broad compatibility in fungal root symbioses. Curr Opin Plant Biol 20:135–145. https://doi.org/10.1016/j.pbi.2014.05.013
Funding
This review is supported by the National Natural Science Fund of China (Grant No. 31471718, 31701722), the Modern Agricultural Industry Technology System (CARS-30), the National Key R&D Program of China (2017YFE0105300), the Key Research and Development Plan of Shaanxi Province (2017ZDXL-NY-0304), the China Postdoctoral Science Foundation (No. 2017M620471), the Shaanxi Provincial Natural Science Foundation (No. 2018JQ3054), and the Postdoctoral Research Project of Shaanxi Province (No. 2017BSHEDZZ103)
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Yan, L., Zhu, J., Zhao, X. et al. Beneficial effects of endophytic fungi colonization on plants. Appl Microbiol Biotechnol 103, 3327–3340 (2019). https://doi.org/10.1007/s00253-019-09713-2
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DOI: https://doi.org/10.1007/s00253-019-09713-2