Abstract
Current rates of population growth require the development of new agricultural strategies to feed the world human and livestock. The massive use of agricultural chemicals causes serious damage to the environment, and to human and animal health. For this reason, the use of endophytic fungi represents a biological alternative in increasing agricultural productivity in a sustainable way. This group of microorganisms, which inhabit plant tissues and organs without causing symptoms of damage, includes a great diversity of filamentous fungi and yeasts that are capable of increasing agricultural productivity. Some of the mechanisms involved in promoting plant growth by means of endophytic fungi include the increasing access to nutrients (nitrogen, phosphorus, potassium, zinc, iron, etc.), production of plant hormones, the ethylene amount reduction, or increase in water acquisition rate. This review tries to compile all the works carried out in the last decades on endophytic fungi use as plant growth promoters with great potential in agriculture.
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References
Aban JL, Barcelo RC, Oda EE, Reyes GA, Balangcod TD, Gutierrez RM, Hipol RM (2017) Auxin production, phosphate solubilisation and ACC deaminase activity of root symbiotic fungi (RSF) from Drynaria quercifolia L. BEPLS 6:25–31
Adnan M, Alshammari E, Ashraf SA, Patel K, Lad K, Patel M (2018) Physiological and molecular characterization of biosurfactant producing endophytic fungi Xylaria regalis from the cones of Thuja plicata as a potent plant growth promoter with its potential application. Biomed Res Int 2018:11–11. https://doi.org/10.1155/2018/7362148
Afandhi A, Widjayanti T, Emi AAL, Tarno H, Afiyanti M, Handoko RNS (2019) Endophytic fungi Beauveria bassiana Balsamo accelerates growth of common bean (Phaeseolus vulgaris L.). Chem Biol Tech Agri 6:11. https://doi.org/10.1186/s40538-019-0148-1
Ahmad N, Hamayun M, Khan SA, Khan AL, Lee IJ, Shin DH (2010) Gibberellin-producing endophytic fungi isolated from Monochoria vaginalis. J Microbiol Biotechnol 20:1744–1749
Al-Hosni K, Shahzad R, Latif Khan A, Muhammad Imran Q, Al Harrasi A, Al Rawahi A et al (2018) Preussia sp. BSL-10 producing nitric oxide, gibberellins, and indole acetic acid and improving rice plant growth. J Plant Interact 13:112–118. https://doi.org/10.1080/17429145.2018.1432773
Ali S, Khan SA, Hamayun M, Iqbal A, Khan AL, Hussain A, Shah M (2019) Endophytic fungi from Caralluma acutangula can secrete plant growth promoting enzymes. Fresenius Environ Bull 28:2688–2696
Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845. https://doi.org/10.1007/s00253-011-3270-y
Amprayn KO, Rose MT, Kecskés M, Pereg L, Nguyen HT, Kennedy IR (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299. https://doi.org/10.1016/j.apsoil.2011.11.009
Ansari RA, Mahmood I, Rizvi R, Sumbul A (2017) Siderophores: augmentation of soil health and crop productivity. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics in agroecosystem.Springer, Singapure, pp. 291–312
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. https://doi.org/10.1016/j.fbr.2007.05.003
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549. https://doi.org/10.1890/05-1459
Asaf S, Khan AL, Waqas M, Kang SM, Hamayun M, Lee IJ, Hussain A (2019) Growth-promoting bioactivities of Bipolaris sp. CSL-1 isolated from Cannabis sativa suggest a distinctive role in modifying host plant phenotypic plasticity and functions. Acta Physiol Plant 41:65. https://doi.org/10.1007/s11738-019-2852-7
Baron NC, Costa NTA, Mochi DA, Rigobelo EC (2018) First report of Aspergillus sydowii and Aspergillus brasiliensis as phosphorus solubilizers in maize. Ann Microbiol 68:863–870. https://doi.org/10.1007/s13213-018-1392-5
Behie SW, Bidochka MJ (2014) Nutrient transfer in plant–fungal symbioses. Trends Plant Sci 19:734–740. https://doi.org/10.1016/j.tplants.2014.06.007
Bilal L, Asaf S, Hamayun M, Gul H, Iqbal A, Ullah I et al (2018) Plant growth promoting endophytic fungi Aspergillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis 76:117–127. https://doi.org/10.1007/s13199-018-0545-4
Boberg JB, Ihrmark K, Lindahl BD (2011) Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter. Fungal Ecol 4:110–114. https://doi.org/10.1016/j.funeco.2010.09.002
Botha A (2006) Yeasts in soil. In: Rosa CA, Péter G (eds) Biodiversity and ecophysiology of yeasts. Springer, Berlin, pp 221–240
Botha A (2011) The importance and ecology of yeasts in soil. Soil Biol Biochem 43:1–8. https://doi.org/10.1016/j.soilbio.2010.10.001
Bunsangiam S, Sakpuntoon V, Srisuk N, Ohashi T, Fujiyama K, Limtong S (2019) Biosynthetic pathway of indole-3-acetic acid in Basidiomycetous yeast Rhodosporidiobolus fluvialis. Mycobiology 47:292–300. https://doi.org/10.1080/12298093.2019.1638672
Chaiharn M, Chunhaleuchanon S, Kozo A, Lumyong S (2008) Screening of rhizobacteria for their plant growth promoting activities. KMITL Sci Tech J 81:18–23
Chapela IH, Petrini O, Bielser G (1993) The physiology of ascospore eclosion in Hypoxylon fragiforme: mechanisms in the early recognition and establishment of an endophytic symbiosis. Mycol Res 97:157–162. https://doi.org/10.1016/S0953-7562(09)80237-2
Christian N, Herre EA, Clay K (2019) Foliar endophytic fungi alter patterns of nitrogen uptake and distribution in Theobroma cacao. New Phytol 222:1573–1583. https://doi.org/10.1111/nph.15693
Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592. https://doi.org/10.1104/pp.108.130369
Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356:260–264. https://doi.org/10.1016/j.rser.2015.11.043
del Carmen Orozco-Mosqueda M, Glick BR, Santoyo G (2020) ACC deaminase in plant growth-promoting bacteria (PGPB): an efficient mechanism to counter salt stress in crops. Microbiol Res 235:126439. https://doi.org/10.1016/j.micres.2020.126439
Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106. https://doi.org/10.1016/j.chemosphere.2016.10.097
Díaz-González S, Marín P, Sánchez R, Arribas C, Kruse J, González-Melendi P, Brunner F, Sacristán S (2020) Mutualistic fungal endophyte Colletotrichum tofieldiae Ct0861 colonizes and increases growth and yield of maize and tomato plants. Agronomy 10:1493. https://doi.org/10.3390/agronomy10101493
Diene O, Narisawa K (2009) The use of symbiotic fungal associations with crops in sustainable agriculture. J Sustain Agr 4:50–56. https://doi.org/10.11178/jdsa.4.50
Dolatabad HK, Javan-Nikkhah M, Shier WT (2017) Evaluation of antifungal, phosphate solubilisation, and siderophore and chitinase release activities of endophytic fungi from Pistacia vera. Mycol Prog 16:777–790. https://doi.org/10.1007/s11557-017-1315-z
Doty SL (2013) Endophytic yeasts: biology and applications. In: Aroca R (ed) Symbiotic endophytes. Springer, Berlin, pp 335–343
El-Tarabily KA (2004) Suppression of Rhizoctonia solani diseases of sugar beet by antagonistic and plant growth-promoting yeasts. J Appl Microbiol 96:69–75. https://doi.org/10.1046/j.1365-2672.2003.02043.x
El-Tarabily KA, Sivasithamparam K (2006) Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 47:25–35. https://doi.org/10.1007/S10267-005-0268-2
Escudero N, Lopez-Llorca LV (2012) Effects on plant growth and root-knot nematode infection of an endophytic GFP transformant of the nematophagous fungus Pochonia chlamydosporia. Symbiosis 57:33–42. https://doi.org/10.1007/s13199-012-0173-3
George TK, Subaida-Beevi S, Asok AK, Shaikmoideen JM (2019) Lant growth promoting endophytic yeast Geotrichum candidum (JX 477426) from roots of Bruguiera cylindrica. J Microbiol Biotechnol Food Sci 9:267. https://doi.org/10.15414/jmbfs.2019.9.2.267-272
Gundel PE, Maseda PH, Vila-Aiub MM, Ghersa CM, Benech-Arnold R (2006) Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability. Ann Bot 97:571–577. https://doi.org/10.1093/aob/mcl004
Hamayun M, Khan SA, Ahmad N, Tang DS, Kang SM, Na CI et al (2009a) Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max (L.) Merr. World J Microbiol Biotechnol 25:627–632. https://doi.org/10.1007/s11274-009-9982-9
Hamayun M, Khan SA, Kim HY, Chaudhary MF, Hwang YH, Shin DH et al (2009b) Gibberellin production and plant growth enhancement by newly isolated strain of Scolecobasidium tshawytschae. J Microbiol Biotechnol 19:560–565. https://doi.org/10.4014/jmb.0809.520
Hamayun M, Khan SA, Khan AL, Rehman G, Sohn EY, Shah AA et al (2009c) Phoma herbarum as a new gibberellin-producing and plant growth-promoting fungus. J Microbiol Biotechnol 19:1–6. https://doi.org/10.4014/jmb.0901.0030
Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I et al (2010) Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102:989–995. https://doi.org/10.3852/09-261
Hamayun M, Hussain A, Khan SA, Kim HY, Khan AL, Waqas M, Irshad M, Iqbal A, Rehman G, Jan S, Lee IJ (2017) Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt affected soybean. Front Microbiol 8:686. https://doi.org/10.3389/fmicb.2017.00686
Hamayun M, Hussain A, IqbalA KSA, Lee IJ (2018) Endophytic fungus Aspergillus japonicus mediates host plant growth under normal and heat stress conditions. Biomed Res Int 2018:7696831–7696811. https://doi.org/10.1155/2018/7696831
Hassan SED (2017) Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L. J Adv Res 8: 687–695.https://doi.org/10.1016/j.jare.2017.09.001
Hendry SJ, Boddy L, Lonsdale D (2002) Abiotic variables effect differential expression of latent infections in beech (Fagus sylvatica). New Phytol 155:449–460. https://doi.org/10.1046/j.1469-8137.2002.00473.x
Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2005) Influence of water supply and endophyte infection (Neotyphodium spp.) on vegetative and reproductive growth of two Lolium perenne L. genotypes. Eur J Agron 22:45–54. https://doi.org/10.1016/j.eja.2003.12.002
Hidayat I (2019) Dark septate endophytes and their role in enhancing plant resistance to abiotic and biotic stresses. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant growth promoting Rhizobacteria for sustainable stress management. Springer, Singapore, pp 35–63
Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O’Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474. https://doi.org/10.1016/j.cell.2016.02.028
Hosseini F, Mosaddeghi MR, Hajabbasi MA, Sabzalian MR (2016) Role of fungal endophyte of tall fescue (Epichloë coenophiala) on water availability, wilting point and integral energy in texturally-different soils. Agric Water Manag 163:197–211. https://doi.org/10.1016/j.agwat.2015.09.024
Hoyos-Carvajal L, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51:409–416. https://doi.org/10.1016/j.biocontrol.2009.07.018
Hussin S, Khalifa W, Geissler N, Koyro HW (2017) Influence of the root endophyte Piriformospora indica on the plant water relations, gas exchange and growth of Chenopodium quinoa at limited water availability. J Agron Crop Sci 203:373–384. https://doi.org/10.1111/jac.12199
Ikram M, Ali N, Jan G, Jan FG, Rahman IU, Iqbal A, Hamayun M (2018) IAA producing fungal endophyte Penicillium roqueforti Thom., enhances stress tolerance and nutrients uptake in wheat plants grown on heavy metal contaminated soils. PloS One 13:e0208150. https://doi.org/10.1371/journal.pone.0208150
Isaeva OV, Glushakova AM, Garbuz SA, Kachalkin AV, Chernov IY (2010) Endophytic yeast fungi in plant storage tissues. Biol Bull 37:26–34. https://doi.org/10.1134/S1062359010010048
Jaiswal DK, VermaJP PS, Meena VS, Meena RS (2016) Potassium as an important plant nutrient in sustainable agriculture: a state of the art. In: MeenaVS MBR, Verma JP (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 21–29
Jia M, Chen L, Xin HL, Zheng CJ, Rahman K, Han T, Qin LP (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906. https://doi.org/10.3389/fmicb.2016.00906
Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in cropplants. J Trop Agr 52:103–122
Joubert PM, Doty SL (2018) Endophytic yeasts: biology, ecology and applications. In: Pirttilä AM, Frank C (eds) Endophytes of Forest trees. Springer, Cham, pp 3–14
Karimi S, Mirlohi A, Sabzalian MR, Sayed-Tabatabaei BE, Sharifnabi B (2012) Molecular evidence for Neotyphodium fungal endophyte variation and specificity within host grass species. Mycologia 104:1281–1290. https://doi.org/10.3852/11-316
Kauppinen M, Saikkonen K, Helander M, Pirttilä AM, Wäli PR (2016) Epichloë grass endophytes in sustainable agriculture. Nature Plants 2:1–7. https://doi.org/10.1038/nplants.2015.224
Kedar A, Rathod D, Yadav A, Agarkar G, Rai M (2014) Endophytic Phoma sp. isolated from medicinal plants promote the growth of Zea mays. Nusantara Biosci 6:132–139. https://doi.org/10.13057/nusbiosci/n060205
Khan SA, Hamayun M, Yoon H, Kim HY, Suh SJ, Hwang SK, Kim JM, Lee IJ, Choo YS, Yoon UH, Kong WS, Lee BM, Kim JG (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231. https://doi.org/10.1186/1471-2180-8-231
Khan SA, Hamayun M, Kim HY, Yoon HJ, Lee IJ, Kim JG (2009) Gibberellin production and plant growth promotion by a newly isolated strain of Gliomastix murorum. World J Microbiol Biotechnol 25:829–833. https://doi.org/10.1007/s11274-009-9981-x
Khan AL, Hamayun M, Kim Y-H, Kang S-M, Lee I-J (2011) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–861. https://doi.org/10.1016/j.plaphy.2011.03.005
Khan Z, Guelich G, Phan H, Redman R, Doty S (2012a) Bacterial and yeast endophytes from poplar and willow promote growth in crop plants and grasses. ISRN Agronomy 2012:890280–890211. https://doi.org/10.5402/2012/890280
Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (2012b) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3. https://doi.org/10.1186/1471-2180-12-3
Khan AL, Waqas M, Khan AR, Hussain J, Kang SM, Gilani SA et al (2013) Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity. World J Microbiol Biotechnol 29:2133–2144. https://doi.org/10.1007/s11274-013-1378-1
Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Musarrat J (ed) Khan MA, ZaidisA. Phosphate Solubilizing Microorganisms. Springer, Cham, pp 31–62
Khan AR, Ullah I, Waqas M, Shahzad R, Hong SJ, Park GS et al (2015) Plant growth-promoting potential of endophytic fungi isolated from Solanum nigrum leaves. World J Microbiol Biotechnol 31:1461–1466. https://doi.org/10.1007/s11274-015-1888-0
Khan AL, Al-Harrasi A, Al-Rawahi A, Al-Farsi Z, Al-Mamari A, Waqas M et al (2016) Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS One 11:e0158207. https://doi.org/10.1371/journal.pone.0158207
Koulman A, Lee TV, Fraser K, Johnson L, Arcus V, Lott JS et al (2012) Identification of extracellular siderophores and a related peptide from the endophytic fungus Epichloë festucae in culture and endophyte-infected Lolium perenne. Phytochem 75:128–139. https://doi.org/10.1016/j.phytochem.2011.11.020
Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV (2018a) Importance of phosphorus supply through endophytic Metarhizium brunneum for root: shoot allocation and root architecture in potato plants. Plant Soil 430:87–97. https://doi.org/10.1007/s11104-018-3718-2
Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV (2018b) Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecol 34:43–49. https://doi.org/10.1016/j.funeco.2018.04.002
Kumar VV (2016) Plant growth-promoting microorganisms: interaction with plants and soil. In: Hakeem KR, AkhtarMS, Abdullah SNA (eds) Plant. Soil and Microbes. Springer, Cham, pp 1–16
Kumar V, Sarma MVRK, Saharan K, Srivastava R, Kumar L, Sahai V et al (2012) Effect of formulated root endophytic fungus Piriformospora indica and plant growth promoting rhizobacteria fluorescent pseudomonads R62 and R81 on Vigna mungo. World J Microb Biot 28:595–603. https://doi.org/10.1007/s11274-011-0852-x
Kumawat N, Kumar R, Khandkar UR, Yadav RK, Saurabh K, Mishra JS, Dotaniya ML, Hans H (2019) Silicon (Si)-and zinc (Zn)-solubilizing microorganisms: role in sustainable agriculture. In: Giri B, Prasad R, Wu QS, Varma A (eds) Biofertilizers for sustainable agriculture and environment. Springer, Cham, pp 109–135
Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798. https://doi.org/10.1016/j.chembiol.2012.06.004
Larriba E, Jaime MD, Nislow C, Martín-Nieto J, Lopez-Llorca LV (2015) Endophytic colonization of barley (Hordeum vulgare) roots by the nematophagous fungus Pochonia chlamydosporia reveals plant growth promotion and a general defense and stress transcriptomic response. J Plant Res 128:665–678. https://doi.org/10.1007/s10265-015-0731-x
Le Cocq K, Gurr SJ, Hirsch PR, Mauchline TH (2017) Exploitation of endophytes for sustainable agricultural intensification. Mol Plant Pathol 18:469–473. https://doi.org/10.1111/mpp.12483
Li X, Zhou J, Xu RS, Meng MY, Yu X, Dai CC (2018) Auxin, cytokinin, and ethylene involved in rice N availability improvement caused by endophyte Phomopsis liquidambari. J Plant Growth Regul 37:128–143. https://doi.org/10.1007/s00344-017-9712-8
Ling L, Li Z, Jiao Z, Zhang X, Ma W, Feng J et al (2019) Identification of novel endophytic yeast strains from tangerine peel. Curr Microbiol 76:1066–1072. https://doi.org/10.1007/s00284-019-01721-9
Lubna Asaf S, Hamayun M, Gul H, Lee IJ, Hussain A (2018) Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. J Plant Interact 13:100–111. https://doi.org/10.1080/17429145.2018.1436199
Lugtenberg BJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92:fiw194. https://doi.org/10.1093/femsec/fiw194
Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS One 8:e78746. https://doi.org/10.1371/journal.pone.0078746
Martínez C, Espinosa-Ruiz A, Prat S (2018) Gibberellins and plant vegetative growth. Annu Rev Plant Biol 49:285–322. https://doi.org/10.1002/9781119312994.apr0539
Mehmood A, Irshad M, Husna AA, Hussain A (2018a) In vitro maize growth promotion by endophytic Fusarium oxysporum WLW. J Appl Environ Biol Sci 8:30–35
Mehmood A, Khan N, Irshad M, Hamayun M (2018b) IAA producing endopytic fungus Fusariun oxysporum WLW colonize maize roots and promoted maize growth under hydroponic condition. Eur Exp Biol 8(24). https://doi.org/10.21767/2248-9215.100065
Mehmood A, Hussain A, Irshad M, Hamayun M, Iqbal A, Khan N (2019) In vitro production of IAA by endophytic fungus Aspergillus awamori and its growth promoting activities in Zea mays. Symbiosis 77:225–235. https://doi.org/10.1007/s13199-018-0583-y
Mei C, Flinn BS (2010) The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Pat Biotech 4:81–95. https://doi.org/10.2174/187220810790069523
Moricca S, Ragazzi A (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathol 98:380–386. https://doi.org/10.1094/PHYTO-98-4-0380
Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456. https://doi.org/10.1111/jac.12366
Munasinghe MVK, Kumar NS, Jayasinghe L, Fujimoto Y (2017) Indole-3-acetic acid production by Colletotrichum siamense, an endophytic fungus from Piper nigrum leaves. J Biol Acti Prod Nat 7:475–479. https://doi.org/10.1080/22311866.2017.1408429
Nakamura T, Murakami T, Saotome M, Tomita K, Kitsuwa T, Meyers SP (1991) Identification of indole-3-acetic acid in Pichia spartinae, an ascosporogenous yeast from Spartina alterniflora marshland environments. Mycologia 83:662–664. https://doi.org/10.1080/00275514.1991.12026067
Nakayan P, Hameed A, Singh S, Young LS, Hung MH, Young CC (2013) Phosphate-solubilizing soil yeast Meyerozyma guilliermondii CC1 improves maize (Zea mays L.) productivity and minimizes requisite chemical fertilization. Plant Soil 373:301–315. https://doi.org/10.1007/s11104-013-1792-z
Narisawa K (2017) The dark septate endophytic fungus Phialocephala fortinii is a potential decomposer of soil organic compounds and a promoter of Asparagus officinalis growth. Fungal Ecol 28:1–10. https://doi.org/10.1016/j.funeco.2017.04.001
Narisawa K, Usuki F, Hashiba T (2004) Control of Verticillium yellows in Chinese cabbage by the dark septate endophytic fungus LtVB3. Phytopathol 94:412–418. https://doi.org/10.1094/PHYTO.2004.94.5.412
Nassar AH, El-Tarabily KA, Sivasithamparam K (2005) Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fert Soils 42:97–108. https://doi.org/10.1007/s00374-005-0008-y
Nath R, Sharma GD, Barooah M (2015) Plant growth promoting endophytic fungi isolated from tea (Camellia sinensis) shrubs of Assam, India. Appl Ecol Environ Res 13:877–891. https://doi.org/10.15666/aeer/1303_877891
Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microb Pathog 82:50–59. https://doi.org/10.1016/j.micpath.2015.04.001
Numponsak T, Kumla J, Suwannarach N, Matsui K, Lumyong S (2018) Biosynthetic pathway and optimal conditions for the production of indole-3-acetic acid by an endophytic fungus, Colletotrichum fructicola CMU-A109. PLoS One 13:e0205070. https://doi.org/10.1371/journal.pone.0205070
Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2014) Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biol 118:683694. https://doi.org/10.1016/j.funbio.2014.04.010
Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2016) Fed-batch fermentation of indole-3-acetic acid production in stirred tank fermenter by red yeast Rhodosporidium paludigenum. Biotechnol Bioproc E 21:414–421. https://doi.org/10.1007/s12257-015-0819-0
Odokonyero K, Acuña TB, Cardoso JA, de la Cruz JJ, Rao IM (2016) Fungal endophyte association with Brachiaria grasses and its influence on plant water status, total non-structural carbohydrates and biomass production under drought stress. Plant Soil 409:273–282. https://doi.org/10.1007/s11104-016-2947-5
Padash A, Shahabivand S, Behtash F, Aghaee A (2016) A practicable method for zinc enrichment in lettuce leaves by the endophyte fungus Piriformospora indica under increasing zinc supply. Sci Hortic 213:367–372. https://doi.org/10.1016/j.scienta.2016.10.040
Pal S, Singh HB, Farooqui A, Rakshit A (2015) Fungal biofertilizers in Indian agriculture: perception, demand and promotion. J Eco-Friend Agri 10:101–113
Paul K, Saha C, Nag M, Mandal D, Naiya H, Sen D et al (2020) A tripartite interaction among the basidiomycete Rhodotorula mucilaginosa, N2-fixing endobacteria, and rice improves plant nitrogen nutrition. Plant Cell 32:486–507. https://doi.org/10.1105/tpc.19.00385
Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb RI, Sagulenko E, Näsholm T, Lonhienne TG (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS One 5:e11915. https://doi.org/10.1371/journal.pone.0011915
Petrini O (1991) Fungal endophytes of tree leaves. In: AndrewsJH, HiranoSS (eds) Microbial ecology of leaves. Springer, Berlin, pp179–197
Phaff HJ, Miller MW, Mark EM (1978) The life of yeasts. Harvard University Press
Poveda J (2020) Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy 10:118. https://doi.org/10.3390/agronomy10010118
Poveda J (2021a) Insect frass in the development of sustainable agriculture. A review. Agron Sust Develop 41:1–10. https://doi.org/10.1007/s13593-020-00656-x
Poveda J (2021b) Glucosinolates profile of Arabidopsis thaliana modified root colonization of Trichoderma species. Biol Control 155:104522. https://doi.org/10.1016/j.biocontrol.2020.104522
Poveda J, Abril-Urias P, Escobar C (2020a) Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front Microbiol 11:992. https://doi.org/10.3389/fmicb.2020.00992
Poveda J, Zabalgogeazcoa I, Soengas P, Rodríguez VM, Cartea ME, Abilleira R, Velasco P (2020b) Brassica oleracea var. acephala (kale) improvement by biological activity of root endophytic fungi. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-77215-7
Qi W, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53:355–364. https://doi.org/10.1002/jobm.201200031
Qiang X, Ding J, Lin W, Li Q, Xu C, Zheng Q, Li Y (2019) Alleviation of the detrimental effect of water deficit on wheat (Triticum aestivum L.) growth by an indole acetic acid-producing endophytic fungus. Plant Soil 439:373–391. https://doi.org/10.1007/s11104-019-04028-7
Rahman MH, Saiga S (2005) Endophytic fungi (Neotyphodium coenophialum) affect the growth and mineral uptake, transport and efficiency ratios in tall fescue (Festuca arundinacea). Plant Soil 272:163–171. https://doi.org/10.1007/s11104-004-4682-6
Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Pastore GM, Junior MRM (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79. https://doi.org/10.1007/s13199-014-0273-3
Rajini SB, Nandhini M, Udayashankar AC, Niranjana SR, Lund OS, Prakash HS (2020) Diversity, plant growth-promoting traits, and biocontrol potential of fungal endophytes of Sorghum bicolor. Plant Pathol 69:642–654. https://doi.org/10.1111/ppa.13151
Ren AZ, Gao YB, Zhou F (2007) Response of Neotyphodium lolii-infected perennial ryegrass to phosphorus deficiency. Plant Soil Environ 53:113–119
Řezanka T, Palyzová A, Faltýsková H, Sigler K (2019) Siderophores: amazing metabolites of microorganisms. In: Rahman AU (ed) Studies in natural products chemistry. Elsevier, Amsterdam, pp 157–188
Rinu K, Sati P, Pandey A (2014) Trichoderma gamsii (NFCCI 2177): a newly isolated endophytic, psychrotolerant, plant growth promoting, and antagonistic fungal strain. J Basic Microbiol 54:408–417. https://doi.org/10.1002/jobm.201200579
Ripa FA, Cao WD, Tong S, Sun JG (2019) Assessment of plant growth promoting and abiotic stress tolerance properties of wheat endophytic fungi. Biomed Res Int 2019:6105865–6105812. https://doi.org/10.1155/2019/6105865
Rodriguez RJ, Woodward CJ, Redman RS (2012) Fungal influence on plant tolerance to stress. In: Southworth D (ed) Biocomplexity of plant-fungal interactions. Wiley-Blackwell, Oxford, pp 155–163
Rudgers JA, Koslow JM, Clay K (2004) Endophytic fungi alter relationships between diversity and ecosystem properties. Ecol Lett 7:42–51. https://doi.org/10.1046/j.1461-0248.2003.00543.x
Sabra M, Aboulnasr A, Franken P, Perreca E, Wright LP, Camehl I (2018) Beneficial root endophytic fungi increase growth and quality parameters of sweet basil in heavy metal contaminated soil. Front Plant Sci 9:1726. https://doi.org/10.3389/fpls.2018.01726
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut R 23:3984–3999
Saia S, Colla G, Raimondi G, Di Stasio E, Cardarelli M, Bonini P et al (2019) An endophytic fungi-based biostimulant modulated lettuce yield, physiological and functional quality responses to both moderate and severe water limitation. Sci Hortic 256:108595. https://doi.org/10.1016/j.scienta.2019.108595
Saldajeno MGB, Hyakumachi M (2011) The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae stimulate plant growth and reduce severity of anthracnose and damping-off diseases in cucumber (Cucumis sativus) seedlings. Ann Appl Biol 159:28–40. https://doi.org/10.1111/j.1744-7348.2011.00471.x
Sarabia M, Cornejo P, Azcón R, Carreón-Abud Y, Larsen J (2017) Mineral phosphorus fertilization modulates interactions between maize, rhizosphere yeasts and arbuscular mycorrhizal fungi. Rhizosphere 4:89–93. https://doi.org/10.1016/j.rhisph.2017.09.001
Sarabia M, Jakobsen I, Grønlund M, Carreon-Abud Y, Larsen J (2018a) Rhizosphere yeasts improve P uptake of a maize arbuscular mycorrhizal association. Appl Soil Ecol 125:18–25. https://doi.org/10.1016/j.apsoil.2017.12.012
Sarabia M, Cazares S, González-Rodríguez A, MoraF C-AY, Larsen J (2018b) Plant growth promotion traits of rhizosphere yeasts and their response to soil characteristics and crop cycle in maize agroecosystems. Rhizosphere 6:67–73. https://doi.org/10.1016/j.rhisph.2018.04.002
Scarcella ASDA, Bizarria Junior R, Bastos RG, Magri MMR (2017) Temperature, pH and carbon source affect drastically indole acetic acid production of plant growth promoting yeasts. Braz J Chem Eng 34:429–438. https://doi.org/10.1590/0104-6632.20170342s20150541
Schulz B, Haas S, Junker C, Andrée N, Schobert M (2015) Fungal endophytes are involved in multiple balanced antagonisms. Curr Sci 1:39–45
Sembiring M, Wahyuni M (2018) The inoculation of mycorrhiza and Talaromyces pinophilus toward the improvement in growth and phosphorus uptake of oil palm seedlings (Elaeis guineensis Jacq) on saline soil media. Bulg J Agri Sci 28:617–622
Sieber TN, Sieber-Canavesi F, Petrini O, Ekramoddoullah AKM, Dorworth CE (1991) Characterization of Canadian and European Melanconium from some Alnus species by morphological, cultural, and biochemical studies. Can J Bot 69:2170–2176. https://doi.org/10.1139/b91-272
Šišić A, Baćanović J, Finckh MR (2017) Endophytic Fusarium equiseti stimulates plant growth and reduces root rot disease of pea (Pisum sativum L.) caused by Fusarium avenaceum and Peyronellaea pinodella. Eur J Plant Pathol 148:271–282. https://doi.org/10.1007/s10658-016-1086-4
Song S, Otkur M, Zhang Z, Tang Q (2007) Isolation and characterization of endophytic microorganisms in Glaycyrrhiza inflat Bat. from Xinjiang. Microbiology 5:867–870. https://doi.org/10.3969/j.issn.0253-2654.2007.05.010
Spagnoletti FN, Tobar NE, Di Pardo AF, Chiocchio VM, Lavado RS (2017) Dark septate endophytes present different potential to solubilize calcium, iron and aluminum phosphates. Appl Soil Ecol 111:25–32. https://doi.org/10.1016/j.apsoil.2016.11.010
Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30. https://doi.org/10.1080/07352680091139169
Sun K, Cao W, Hu LY, Fu WQ, Gong JH, Kang N, Dai CC (2019a) Symbiotic fungal endophyte Phomopsis liquidambari-rice system promotes nitrogen transformation by influencing below-ground straw decomposition in paddy soil. J Appl Microbiol 126:191–203. https://doi.org/10.1111/jam.14111
Sun K, Zhang FM, Kang N, Gong JH, Zhang W, Chen Y, Dai CC (2019b) Rice carbohydrate dynamics regulate endophytic colonization of Diaporthe liquidambaris in response to external nitrogen. Fungal Ecol 39:213–224. https://doi.org/10.1016/j.funeco.2019.02.010
Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639. https://doi.org/10.1017/S0953756205002753
Taghinasab M, Imani J, Steffens D, Glaeser SP, Kogel KH (2018) The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat. Plant Soil 426:339–348. https://doi.org/10.1007/s11104-018-3624-7
Tang MJ, Zhu Q, Zhang FM, Zhang W, Yuan J, Sun K, Xu FJ, Dai CC (2019) Enhanced nitrogen and phosphorus activation with an optimized bacterial community by endophytic fungus Phomopsis liquidambari in paddy soil. Microbiol Res 221:50–59. https://doi.org/10.1016/j.micres.2019.02.005
Tian B, Xie J, Fu Y, Cheng J, Li B, Chen T, Zhao Y, Gao Z, Yang P, Barbetti MJ, Tyler BM, Jiang D (2020) A cosmopolitan fungal pathogen of dicots adopts an endophytic lifestyle on cereal crops and protects them from major fungal diseases. ISME J 14:3120–3135. https://doi.org/10.1038/s41396-020-00744-6
Toscano-Verduzco FA, Cedeño-Valdivia PA, Chan-Cupul W, Hernández-Ortega HA, Ruiz-Sánchez E, Galindo-Velasco E, Cruz-Crespo E (2020) Phosphates solubilization, indol-3-acetic acid and siderophores production by Beauveria brongniartii and its effect on growth and fruit quality of Capsicum chinense. J Hortic Sci Biotech 95:235–246. https://doi.org/10.1080/14620316.2019.1662737
Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184. https://doi.org/10.1080/15572536.2007.11832577
Vazquez de Aldana BR, Bills G, Zabalgogeazcoa I (2013) Are endophytes an important link between airborne spores and allergen exposure? Fungal Divers 60:33–42. https://doi.org/10.1007/s13225-013-0223-z
Vázquez-de-Aldana BR, García-Ciudad A, Garcia-Criado B, Vicente-Tavera S, Zabalgogeazcoa I (2013) Fungal endophyte (Epichloë festucae) alters the nutrient content of Festuca rubra regardless of water availability. PLoS One 8:e84539. https://doi.org/10.1371/journal.pone.0084539
Velázquez E, Silva LR, Ramírez-Bahena MH, Peix A (2016) Diversity of potassium-solubilizing microorganisms and their interactions with plants. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 99–110
Vidal S, Jaber LR (2015) Entomopathogenic fungi as endophytes: plant– endophyte–herbivore interactions and prospects for use in biological control. Curr Sci 109:46–54
Vignale MV, Iannone LJ, Scervino JM, Novas MV (2018) Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil 422:267–281. https://doi.org/10.1007/s11104-017-3173-5
Vila-Aiub MM, Gundel PE, Ghersa CM (2005) Fungal endophyte infection changes growth attributes in Lolium multiflorum Lam. Austral Ecol 30:49–57. https://doi.org/10.1111/j.1442-9993.2005.01423.x
Wakelin SA, Gupta VV, Harvey PR, Ryder MH (2007) The effect of Penicillium fungi on plant growth and phosphorus mobilization in neutral to alkaline soils from southern Australia. Can J Microbiol 53:106–115. https://doi.org/10.1139/w06-109
Wang WL, Chi ZM (2009) Siderophore production by the marine derived Aureobasidium pullulans and its antimicrobial activity. Bioresour Technol 100:2639–2641. https://doi.org/10.1016/j.biortech.2008.12.010
Wang Z, Li C, White J (2019) Effects of Epichloë endophyte infection on growth, physiological properties and seed germination of wild barley under saline conditions. J Agron Crop Sci 206:43–51. https://doi.org/10.1111/jac.12366
Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773. https://doi.org/10.3390/molecules170910754
Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276. https://doi.org/10.2307/3545919
Wu M, Wei Q, Xu L, Li H, Oelmüller R, Zhang W (2018) Piriformospora indica enhances phosphorus absorption by stimulating acid phosphatase activities and organic acid accumulation in Brassica napus. Plant Soil 432:333–344. https://doi.org/10.1007/s11104-018-3795-2
Wu JR, Xu FJ, Cao W, Zhang W, Guan YX, Dai CC (2019) Fungal endophyte Phomopsis liquidambari B3 enriches the diversity of nodular culturable endophytic bacteria associated with continuous cropping of peanut. Arch Agron Soil Sci 65:240–252. https://doi.org/10.1080/03650340.2018.1493198
Xin G, Glawe D, Doty SL (2009) Characterization of three endophytic, indole-3-acetic acid-producing yeasts occurring in Populus trees. Mycol Res 113:973–980. https://doi.org/10.1016/j.mycres.2009.06.001
Yan L, Zhu J, Zhao X, Shi J, Jiang C, Shao D (2019) Beneficial effects of endophytic fungi colonization on plants. Appl Microbiol Biotechnol 103:3327–3340. https://doi.org/10.1007/s00253-019-09713-2
Yang B, Ma HY, Wang XM, Jia Y, Hu J, Li X, Dai CC (2014) Improvement of nitrogen accumulation and metabolism in rice (Oryza sativa L.) by the endophyte Phomopsis liquidambari. Plant Physiol Biochem 82:172–182. https://doi.org/10.1016/j.plaphy.2014.06.002
Yang B, Wang X, Ma H, Yang T, Jia Y, Zhou J, Dai C (2015) Fungal endophyte Phomopsis liquidambari affects nitrogen transformation processes and related microorganisms in the rice rhizosphere. Front Microbiol 6:982. https://doi.org/10.3389/fmicb.2015.00982
Yihui B, Zhouying XU, Yurong Y, Zhang H, Hui C, Ming T (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27:283–292. https://doi.org/10.1016/S1002-0160(17)60316-3
Yoo SJ, Shin DJ, Won HY, Song J, Sang MK (2018) Aspergillus terreus JF27 promotes the growth of tomato plants and induces resistance against Pseudomonas syringae pv. tomato. Mycobiology 46:147–153. https://doi.org/10.1080/12298093.2018.1475370
You YH, Kwak TW, Kang SM, Lee MC, Kim JG (2015) Aspergillus clavatus Y2H0002 as a new endophytic fungal strain producing gibberellins isolated from Nymphoides peltata in fresh water. Mycobiology 43:87–91. https://doi.org/10.5941/MYCO.2015.43.1.87
Zabalgogeazcoa Í, Ciudad AG, de Aldana BRV, Criado BG (2006) Effects of the infection by the fungal endophyte Epichloë festucae in the growth and nutrient content of Festuca rubra. Eur J Agron 24:374–384. https://doi.org/10.1016/j.eja.2006.01.003
Zhang F, Yuan J, Yang X, Cui Y, Chen L, Ran W, Shen Q (2013) Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368:433–444. https://doi.org/10.1007/s11104-012-1519-6
Zhang H, Xie J, Fu Y, Cheng J, Qu Z, Zhao Z, Cheng S, Chen T, Li B, Wang Q, Liu X, Tian B, Collinge DB, Jiang D (2020) A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for Brassica protection and yield enhancement. Mol Plant 13:1420–1433. https://doi.org/10.1016/j.molp.2020.08.016
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Poveda, J., Eugui, D., Abril-Urías, P. et al. Endophytic fungi as direct plant growth promoters for sustainable agricultural production. Symbiosis 85, 1–19 (2021). https://doi.org/10.1007/s13199-021-00789-x
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DOI: https://doi.org/10.1007/s13199-021-00789-x