Endophytic Fungi and Their Prospects

doi:10.16409/j.cnki.2095-039x.2015.05.014

Abstract

Abstract: Endophytic fungi are very common and widespread in nature. Some endophytic fungi can promote their hosts to take nutrition from soil, and improve hosts resistance against pests and abiotic stress, and also may stimulate their hosts to produce active compounds. Therefore, endophytic fungus is one of the important research contents in the field of biological control of plant pests. In this paper, the molecular basis for mutualistic symbiosis between endophytic fungi and their hosts, the mechanism that the endophytic fungi affects their hosts, the specific interaction between endophytic fungi and their hosts, the plant pathogenic fungi as specific endophytes, the possible mechanism for the formation of endophytic were discussed. The prospects for future studies on endophytic fungi were also discussed.

Key words: endophytic fungi, plant pathogenic fungi, mutualistic symbiosis, plant holobiont, biological control, microbiome

CLC Number:

S476

JIANG Daohong. Endophytic Fungi and Their Prospects[J]. journal1, 2015, 31(5): 742-749.

References

[1] Lyons P C, Plattner R D, Bacon C W. Occurrence of peptide and clavine ergot alkaloids in tall fescue grass[J]. Science, 1986, 232(4749): 487-489.
[2] Omacini M, Chaneton E J, Ghersa C M, et al. Symbiotic fungal endophytes control insect host-parasite interaction webs[J]. Nature, 2001, 409(6816): 78-81.
[3] Arnold A E, Mejia L C, Kyllo D, et al. Fungal endophytes limit pathogen damage in a tropical tree[J]. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(26): 15649-15654.
[4] Waller F, Achatz B, Baltruschat H, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance disease resistance and higher yield[J]. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(38): 13386-13391.
[5] Li C, Gao J, Nan Z. Interactions of Neotyphodium gansuense, Achnatherum inebirians and plant-pathogenic fungi[J]. Mycological Research, 2007, 111(10): 1220-1227.
[6] Tian P, Nan Z, Li C, et al. Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens[J]. European Journal of Plant Pathology, 2008, 122(4): 593-602.
[7] Porras-Alfaro A, Bayman P. Hidden fungi, emergent properties: endophytes and microbiomes[J]. Annual Review of Phytopathology, 2011, 49: 291-315.
[8] Behie S W, Zelisko P M, Bidochka M J. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants[J]. Science, 2012, 336(6088): 1576-1577.
[9] Zhang X, Li C, Nan Z. Effects of cadmium stress on seed germination and seedling growth of Elymus dahuricus infected with the Neotyphodium endophyte[J]. Science China-Life Sciences, 2012, 55(9): 793-799.
[10] Zhang X, Li C, Nan Z, et al. Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators[J]. Weed Research, 2012, 52(1): 70-78.
[11] Peng Q, Li C, Song M, et al. Effects of seed hydropriming on growth of Festuca sinensis infected with Neotyphodium endophyte[J]. Fungal Ecology, 2013, 6(1): 83-91.
[12] Oberhofer M, Gusewell S, Leuchtmann A. Effects of natural hybrid and non-hybrid Epichloe endophytes on the response of Hordelymus europaeus to drought stress[J]. New Phytologist, 2014, 201(1): 242-253.
[13] Su Z, Mao L, Li N, et al. Evidence for biotrophic life style and biocontrol potential of dark septate endophyte Harpophora oryzae to rice blast disease[J]. PLoS ONE, 2013, 8(4): e61332.
[14] Xia C, Zhang X, Christensen M J, et al. Epichloe endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunkenhorse grass (Achnatherum inebrians)[J]. Fungal Ecology, 2015, 16: 26-33.
[15] Shoresh M, Harman G E, Mastouri F. Induced systemic resistance and plant responses to fungal biocontrol agents[J]. Annual Review of Phytopathology, 2010, 48: 21-43.
[16] Harman G E, Herrera-Estrella A H, Horwitz B A, et al. Special issue: Trichoderma – from basic biology to biotechnology[J]. Microbiology, 2012, 158(1): 1-2.
[17] Stierle A, Strobel G A, Stierle D. Taxol and taxane production by Taxomyces andreanae[J]. Science, 1993, 260(5105): 214-216.
[18] Ludwig-Muller J. Plants and endophytes: equal partners in secondary metabolite production?[J]. Biotechnology Letter, 2015, 37: 1325-1334.
[19] Takemoto D, Tanaka A, Scott B. A p67 (Phox)-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis[J]. Plant Cell, 2006, 18(10): 2807-2821.
[20] Tanaka A, Christensen M J, Takemoto D, et al. Reactive oxygen species play a role in regulating a fungus-perennial ryegrass mutualistic interaction[J]. Plant Cell, 2006, 18(4): 1052-1066.
[21] Tanaka A, Takemoto D, Hyon G S, et al. NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloe festucae and perennial ryegrass[J]. Molecular Microbiology, 2008, 68(5): 1165-1178.
[22] Eaton C J, Cox M P, Ambrose B, et al. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis[J]. Plant Physiology, 2010, 153(4): 1780-1794.
[23] Eaton C J, Cox M P, Scott B. What triggers grass endophytes to switch from mutualism to pathogenism?[J]. Plant Science, 2011, 180(2): 190-195.
[24] Tanaka A, Takemoto D, Chujo T, et al. Fungal endophytes of grasses[J]. Current Opinion in Plant Biology, 2012, 15(4): 462-468.
[25] Kayano Y, Tanaka A, Akano F, et al. Differential roles of NADPH oxidases and associated regulators in polarized growth conidiation and hyphal fusion in the symbiotic fungus Epichloe festucae[J]. Fungal Genetics and Biology, 2013, 56: 87-97.
[26] Johnson L J, Koulman A, Christensen M, et al. An extracellular siderophore is required to maintain the mutualistic interaction of Epichloe festucae with Lolium perenne[J]. PLoS Pathogens, 2013, 9(5): e1003332.
[27] Charlton N D, Shoji J Y, Ghimire S R, et al. Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte Epichloe festucae and the host plant[J]. Eukayotic Cell, 2012, 11(12): 1463-1471.
[28] Nishimura R, Hayashi M, Wu G J, et al. HAR1 mediates systemic regulation of symbiotic organ development[J]. Nature, 2002, 420(6914): 426-429.
[29] Goh C H, Vallejos D F V, Nicotra A B, et al. The impact of beneficial plant-associated microbes on plant phenotypic plasticity[J]. Journal of Chemical Ecology, 2013, 39(7): 826-839.
[30] Verma S, Varma A, Rexer K H, et al. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus[J]. Mycologia, 1998, 90(5): 896-903.
[31] Das A, Kamal S, Shakil N A, S et al. The root endophyte fungus Piriformospora indica leads to early flowering higher biomass and altered secondary metabolites of the medicinal plant Coleus forskohlii[J]. Plant Signaling and Behavior, 2012, 7(1): 103-112.
[32] Camehl I, Drzewiecki C, Vadassery J, et al. The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis[J]. PLoS Pathogens, 2011, 7(5): e1002051.
[33] Waqas M, Khan A L, Kamran M, et al. Endophytic fungi produce gibberellins and indoleacetic acid and promote host-plant growth during stress[J]. Molecules, 2012, 17(9): 10754-10773.
[34] Ren C, Dai C. Nitric oxide and brassinosteroids mediated fungal endophyte-induced volatile oil production through protein phosphorylation pathways in Atractylodes lancea plantlets[J]. Journal of Integrative Plant Biology, 2013, 55(11): 1136-1146.
[35] Marquez L M, Redman R S, Rodriguez R J, et al. A virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance[J]. Science, 2007, 315(5811): 513-515.
[36] Shoresh M, Harman G E. Differential expression of maize chitinases in the presence or absence of Trichoderma harzianum strain T22 and indications of a novel exoendo-heterodimeric chitinase activity[J]. BMC Plant Biology, 2010, 10: 136.
[37] Lamdan N L, Shalaby S, Ziv T, et al. Secretome of Trichoderma interacting with maize roots: role in induced systemic resistance[J]. Molecular and Cellular Proteomics, 2015, 14: 1054-1063.
[38] Djonovic S, Pozo M J, Dangott L J, et al. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance[J]. Molecular Plant-Microbe Interactions, 2006, 19(8): 838-853.
[39] Crutcher F K, Moran-Diez M E, Ding S, et al. A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens[J]. Fungal Biology, 2015, 119(6): 476-486.
[40] Deshmukh S, Hueckelhoven R, Schaefer P, et al. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(49): 18450-18457.
[41] Lahrmann U, Ding Y, Banhara A, et al. Host-related metabolic cues affect colonization strategies of a root endophyte[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(34): 13965-13970.
[42] Sherameti I, Tripathi S, Varma A, et al. The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves[J]. Molecular Plant-Microbe Interactions, 2008, 21(6): 799-807.
[43] Camehl I, Sherameti I, Venus Y, et al. Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana[J]. New Phytologist, 2010, 185(4): 1062-1073.
[44] Eaton C J, Dupont P Y, Solomon P, et al. A core gene set describes the molecular basis of mutualism and antagonism in Epichloe spp.[J]. Molecular Plant-Microbe Interactions, 2015, 28(3): 218-231.
[45] Malcolm G M, Kuldau G A, Gugino B K, et al. Hidden host plant associations of soilborne fungal pathogens: An ecological perspective[J]. Phytopathology, 2013, 103(6): 538-544.
[46] Robb J. Verticillium tolerance: resistance, susceptibility, or mutualism?[J]. Canadian Journal of Botany-Revue Canadienne De Botanique, 2007, 85(10): 903-910.
[47] Freeman S, Horowitz S, Sharon A. Pathogenic and nonpathogenic lifestyles in Colletotrichum acutatum from strawberry and other plants[J]. Phytopathology, 2001, 91: 986-992.
[48] Rojas E I, Rehner S A, Samuels G J, et al. Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes[J]. Mycologia, 2010, 102(6): 1318-1338.
[49] Nicole B, Chantal G. Cytological analysis of defense-related mechanisms induced in pea root tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47[J]. Phytopathology, 2001, 91(8): 730-740.
[50] Martinuz A, Schouten A, Menjivar R D, et al. Effectiveness of systemic resistance toward Aphis gossypii (Hom., Aphididae) as induced by combined applications of the endophytes Fusarium oxysporum Fo162 and Rhizobium etli G12[J]. Biological Control, 2012, 62(3): 206-212.
[51] Paparu P, Dubois T, Coyne D, et al. Differential gene expression in east African highland bananas (Musa spp.): interactions between non-pathogenic Fusarium oxysporum V5w2 and Radopholus similis[J]. Physiological and Molecular Plant Pathology, 2013, 82: 56-63.
[52] Gonzaga L L, Costa L E O, Santos T T, et al. Endophytic fungi from the genus Colletotrichum areabundant in the Phaseolus vulgaris and have high genetic diversity[J]. Journal of Applied Microbiology, 2014, 118(2): 485-496.
[53] Amselem J, Cuomo C A, van Kan J A, et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea[J]. PLoS Genetics, 2011, 7(8): e1002230.
[54] Barnes S E, Shaw M W. Factors affecting symptom production by latent Botrytis cinerea in Primulax polyantha[J]. Plant Pathology, 2002, 51: 746-754.
[55] Sowley E N K, Dewey F M, Shaw M W. Persistent, symptomless, systemic, and seed-borne infection of lettuce by Botrytis cinerea[J]. European Journal of Plant Pathology, 2010, 126(1): 61-71.
[56] Shipunov A, Newcombe G, Raghavendra A K H, et al. Hidden diversity of endophytic fungi in and invasive plant[J]. American Journal of Botany, 2008, 95(9): 1096-1108.
[57] Grant-Downton R T, Terhem R B, Kapralov M V, et al. A novel Botrytis species is associated with a newly emergent foliar disease in cultivated Hemerocallis[J]. PLoS One, 2014, 9: e0089272.
[58] Rouxel T, Balesdent M H. The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era[J]. Molecular Plant Pathology, 2005, 6(3): 225-241.
[59] Junker C, Draeger S, Schulz B. A fine line - endophytes or pathogens in Arabidopsis thaliana[J]. Fungal Ecology, 2012, 5(6): 657-662.
[60] García E, Alonso A, Platas G, et al. The endophytic mycobiota of Arabidopsis thaliana[J]. Fungal Diversity, 2013, 60(1): 71-89.
[61] Vettraino A M, Paolacci A, Vannini A. Endophytism of Sclerotinia pseudotuberosa: PCR assay for specific detection in chestnut tissues[J]. Mycological Research, 2005, 109: 96-102.
[62] Wunderle J, Leclerque A, Schaffrath U, et al. Assessment of the loose smut fungi (Ustilago nuda and U. tritici) in tissues of barley and wheat by fluorescence microscopy and real-time PCR[J]. European Journal of Plant Pathology, 2012, 133: 865-875.
[63] Ploch S, Thines M. Obligate biotrophic pathogens of the genus Albugo are wide spread as asymptomatic endophytes in natural populations of Brassicaceae[J]. Molecular Ecology, 2011, 20(17): 3692-3699.
[64] Crone M, McComb J A, O’Brien P A, et al. Annual and herbaceous perennial native Australian plant species are asymptomatic hosts of Phytophthora cinnamomi in the Eucalyptus marginata (jarrah) forest of Western Australia[J]. Plant Pathology, 2012, 65(5): 1057-1062.
[65] Crone M, McComb J A, O’Brien P A, et al. Survival of Phytophthora cinnamomi as oospores, stromata, and thick-walled chlamydospores in roots of symptomatic and asymptomatic annual and herbaceous perennial plant species[J]. Fungal Biololgy, 2013, 117(2): 112-123.
[66] Xu X, Su Z, Wang C, et al. The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte[J]. Scientific Reports, 2014, 4: 5783.
[67] Freeman S, Rodriguez R J. Genetic conversion of a fungal plant pathogen to a nonpathogenic, endophytic mutualist[J]. Science, 1993, 260(5104): 75-78.
[68] Redman R S, Ranson J C, Rodriguez R J. Conversion of the pathogenic fungus Colletotrichum magna to a nonpathogenic, endophytic mutualist by gene disruption[J]. Molecular Plant-Microbe Interactions, 1999, 12(11): 969-975.
[69] Bao X D, Roossinck M J. Multiplexed interactions: Viruses of endophytic fungi[J]. Advances in Virus Research, 2013, 86: 37-58.
[70] van Kan J A L, Shaw M W, Grant-Downton R. Botrytis species: relentless necrotrophic thugs or endophytes gone rogue?[J]. Molecular Plant Pathology, 2014, 15(9): 957-962.
[71] Vandenkoornhuyse P, Quaiser A, Duhamel M, et al. The importance of the microbiome of the plant holobiont[J]. New Phytologist, 2015, 206(4): 1196-1206.
[72] Reinhold-Hurek B, Bunger W, Burbano C S, et al. Roots shaping their microbiome: Global hotspots for microbial activity[J]. Annual Review of Phytopathology, 2015, 53: 403-424.
[73] Bulgarelli D, Rott M, Schlaeppi K, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota[J]. Nature, 2012, 488(7409): 91-95.
[74] Lundberg D S, Lebeis S L, Paredes S H, et al. Defining the core Arabidopsis thaliana root microbiome[J]. Nature, 488(7409): 86-90.
[75] Atsatt P R, Whiteside M D. Novel symbiotic protoplasts formed by endophytic fungi explain their hidden existence, lifestyle switching, and diversity within the plant kingdom[J]. PLoS ONE, 2014, 9(4): e95266.
[76] Yan J F, Broughton S J, Gange A C. Do endophytic fungi grow through their hosts systemically?[J]. Fungal Ecology, 2015, 13: 53-59.
[77] Schulz B, Haas S, Junker C, et al. Fungal endophytes are involved in multiple balanced antagonisms[J]. Current Science, 2015, 109(1): 39-45.