Dark Septate Endophytes and Their Role in Enhancing Plant Resistance to Abiotic and Biotic Stresses

  • Iman Hidayat
Part of the Microorganisms for Sustainability book series (MICRO, volume 12)


In recent years, dark septate root endophytes (DSE) emerge as one of the potential microbial groups in enhancing plant health and resistance to environmental stresses. In this chapter, we describe the diversity of DSE, host specificity, and their role in nutrient uptake by the plant. The mechanism of plant stress tolerance to environmental stresses and possible application of DSE isolates in agricultural practices are also elucidated. Estimation of DSE diversity is difficult due to their sporulating and non-sporulating life forms of which generates problems in the DSE identification. In addition, majority members of DSE fungi showed no host specificity with their associated plant. During plant-DSE association, hyphae have shown to be important in nutrient transfer from the DSE to their host plant. Nutrients obtained by the hyphae from the soil will be translocated inter- and intracellularly into plant cells through various mechanisms. In extreme environmental condition, such as high Cd (cadmium), DSE affects plant physiology by regulating GSH (glutathione) metabolism and thiol compound contents in the host plant to alleviate Cd toxicity. Due to their potential for increasing crop productivity and resistance to abiotic and biotic stresses, the studies now focus on developing a simple and low-cost standardized formulation that is applicable to agricultural practices. It is supported by the fact that members of DSE are easily cultured and propagated in the laboratory. Current effective application of DSE involves the development of superior plant seedling through inoculation of the DSE isolates during plant propagation by tissue culture or seeds.


Agriculture Environmental stress Fungal endophytes Rhizosphere Symbiosis 


  1. Ab Rahman SFS, Singh E, Pieterse CMJ, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111. Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67. Scholar
  3. Ahonen-Jonnarth U, Van Hees PAW, Lundström US, Finlay RD (2000) Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminum and heavy metal concentrations. New Phytol 146:557–567. Scholar
  4. Akhter J, Monneveux P, SABIR SA, Ashraf MY, Lateef Z, Serraj R (2010) Selection of drought tolerant and high water use efficient rice cultivars through 13C isotope discrimination technique. Pak J Bot 42:3887–3897Google Scholar
  5. Andrade-Linares DR, Grosch R, Franken P, Rexer KH, Kost G, Restrepo S et al (2011) Colonization of roots of cultivated Solanum lycopersicum by dark septate and other ascomycetous endophytes. Mycologia 103:710–721. Scholar
  6. Babu AG, Shim J, Bang KS, Shea PJ, Oh BT (2014) Trichoderma virens PDR-28: a heavy metal–tolerant and plant growth–promoting fungus for remediation and bioenergy crop production on mine tailing soil. J Environ Manag 132:129–134. Scholar
  7. Bahrami-rad S, Hajboland R (2017) Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: comparison of root with a foliar application. Ann Agric Sci 62:121–130. Scholar
  8. Bajaj R, Hu W, Huang YY, Chen S, Prasad R, Varma A, Bushley KE (2015) The beneficial root endophyte Piriformospora indica reduces egg density of the soybean cyst nematode. Biol Control 90:193–199. Scholar
  9. Ban Y, Tang M, Chen H, Xu Z, Zhang H, Yang Y (2012) The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One 7:e47968. Scholar
  10. Barberon M, Geldner N (2014) Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol 166:528–537. Scholar
  11. Barrow JR, Aaltonen RE (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11:199–205. Scholar
  12. Bartholdy B, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals 14:33–42. Scholar
  13. Behie SW, Bidochka MJ (2014) Nutrient transfer in plant-fungal symbioses. Trends Plant Sci 19:734–740. Scholar
  14. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627. Scholar
  15. Benhamou N, Garand C (2001) Cytological analysis of defense-related mechanisms induced in pea tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47. Phytopathology 91:730–740. Scholar
  16. Bhagobaty RK, Joshi SR (2009) Promotion of seed germination of a green gram and chickpea by Penicillium verruculosum RS7PF, a root endophytic fungus of Potentilla fulgens L. J Adv Biotechnol 8:16–18Google Scholar
  17. Bidartondo MI, Read DJ (2008) Fungal specificity bottlenecks during orchid germination and development. Mol Ecol 17:3707–3716. Scholar
  18. Bienfait B (1989) Prevention of stress in iron metabolism of plants. Acta Bot Neerlandica 38:105–129. Scholar
  19. Boari F, Donadio A, Pace B, Schiattone MI, Cantore V (2016) Kaolin improves salinity tolerance, water use efficiency and quality of tomato. Agric Water Manag 167:29–37. Scholar
  20. Bonfim JA, Vasconcellos RLF, Baldesin LF, Sieber TN, Cardoso EJBN (2016) Dark septate endophytic fungi of native plants along an altitudinal gradient in the Brazilian Atlantic forest. Fungal Ecol 20:202–210. Scholar
  21. Brodeur J (2012) Host specificity in biological control: insights from opportunistic pathogens. Evol Appl 5:470–480. Scholar
  22. Bryla DR, Duniway JM (1997) Water uptake by safflower and wheat roots infected with arbuscular mycorrhizal fungi. New Phytol 136:591–601. Scholar
  23. Bunnag S, Pongthai P (2013) Selection of rice (Oryza sativa L.) cultivars tolerant to drought stress at the vegetative stage under field conditions. Am J Plant Sci 4:1701–1708. Scholar
  24. Burgstaller W, Schinner E (1993) Leaching of metals with fungi. J Biotechnol 27:91–116. Scholar
  25. Bussay A, van der Velde M, Fumagalli D, Seguini L (2015) Improving operational maize yield forecasting in Hungary. Agric Syst 141:94–106. Scholar
  26. Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate root endophytes. Mycologia 92:230–232CrossRefGoogle Scholar
  27. Cantelaube P, Terres JM (2005) Seasonal weather forecasts for crop yield modeling in Europe. Tellus 57A:476–487. Scholar
  28. Cardoso AO, Pinto HS, de Ávila HMH, Dias PLS, Marin FR, Pilau F (2010) Extended time weather forecasts contribute to agricultural productivity estimates. Theor Appl Climatol 102:343–350. Scholar
  29. Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462. Scholar
  30. Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153:79–90. Scholar
  31. Ćosić M, Djurović N, Todorović M, Maletić R, Zečević B, Stričević R (2015) Effect of irrigation regime and application of kaolin on yield, quality and water use efficiency of sweet pepper. Agric Waste Manag 159:139–147. Scholar
  32. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jakobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792. Scholar
  33. Currah RS, Tsuneda A (1993) Vegetative and reproductive morphology of Phialocephala fortinii (Hyphomycetes, Mycelium radical atrovirens) in culture. Trans Mycol Soc Jpn 34:345–356Google Scholar
  34. Currah RS, Van Dyk M (1986) A survey of some perennial vascular plant species native to Alberta for the occurrence of mycorrhizal fungi. Can Field-Nat 100:330–342Google Scholar
  35. Currah RS, Tsuneda A, Murakami S (1993) Morphology and ecology of Phialocephala fortinii in roots of Rhododendron brachycarpum. Can J Bot 71:1639–1644. Scholar
  36. Deacon JC (1973) Phialophora radicola and Gaeumannomyces graminis on roots of grasses and cereals. Trans Br Mycol Soc 61:471–485. Scholar
  37. Diao YH, Li T, Zhao ZW (2013) Zinc accumulation characteristics of two Exophiala strains and their antioxidant response to Zn2+ stress. J Environ Prot 4:12–19. Scholar
  38. Diene O, Takahashi T, Yonekura A, Nitta Y, Narisawa K (2010) A new fungal endophyte, Helminthosporium velutinum, promoting the growth of a bioalcohol plant, sweet sorghum. Microbes Environ 25:216–219. Scholar
  39. Diene O, Wang W, Narisawa K (2013) Pseudosigmoidea ibarakiensis sp. nov., a dark septate endophytic fungus from a cedar forest in Ibaraki. Jpn Microbes Environ 28:381–387. Scholar
  40. Djurović N, Ćosić M, Stričević R, Savić S, Domazet M (2016) Effect of irrigation regime and application of kaolin on yield, quality and water use efficiency of tomato. Sci Hortic 201:271–278. Scholar
  41. Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture. Can J Bot 74:1071–1078. Scholar
  42. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  43. Fomina MA, Alexander IJ, Hillier S, Gadd GM (2004) Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiol J 21:351–366. Scholar
  44. Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464. Scholar
  45. Frieden E, Osaki S (1974) Ferroxidases and ferrireductase: their role in iron metabolism. Adv Exp Med Biol 48:235–265CrossRefGoogle Scholar
  46. Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology, and biogeochemical processes. Adv Microb Physiol 41:47–92. Scholar
  47. Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279. Scholar
  48. Gasoni L, De Gurfinkel BS (1997) The endophyte Cladorrhinum forcundissimum in cotton roots: phosphorus uptake and host growth. Mycol Res 101:867–870CrossRefGoogle Scholar
  49. Ghag SB, Shekhawat UKS, Ganapathi TR (2015) Fusarium wilt of banana: biology, epidemiology, and management. Int J Pest Manag 61:1–14. Scholar
  50. Griffiths H, Parry MAJ (2002) Plant responses to water stress. Ann Bot 89:801–802. Scholar
  51. Grünig CR, Sieber TN (2005) Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen. et sp. nov., formerly known as dark-septate endophyte type 1. Mycologia 97:628–640. Scholar
  52. Grünig CR, Queloz V, Duò A et al (2009) Phylogeny of Phaeomollisia piceae gen. sp. nov.: a dark septate conifer-needle endophyte and its relationships to Phialocephala and Acephala. Mycol Res 113:207–221. Scholar
  53. Grünig CR, Queloz V, Sieber TN (2011) Structure of diversity in dark septate endophytes: from species to genes. In: Pirttilä AM, Frank CA (eds) Endophytes of forest trees: biology and applications. Springer, Dordrecht, pp 3–30. Scholar
  54. Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526. Scholar
  55. Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629. Scholar
  56. Haselwandter K (1987) Mycorrhizal infection and its possible ecological significance in climatically and nutritionally stressed alpine plant communities. Angew Bot 61:107–114Google Scholar
  57. Hashiba T, Narisawa K (2005) The development and endophytic nature of the fungus Heteroconium chaetospira. FEMS Microbiol Lett 252:191–196. Scholar
  58. Hidayat I, Radiastuti N, Rahayu G, Achmadi S, Okane I (2016) Three Quinine and Cinchonidine producing Fusarium species from Indonesia. Curr Res Environ Appl Mycol 6(1):20–34. Scholar
  59. 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. Scholar
  60. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  61. IPCC (Intergovernmental Panel on Climate Change) (2007) Climate change 2007: impacts, adaptation, and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contribution of working group II to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge, pp 1–976Google Scholar
  62. Iqbal M, Ashraf M (2010) Gibberellic acid-mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield, and hormonal homeostasis. Environ Exp Bot 86:76–85. Scholar
  63. Jie L, Zifeng W, Lixiang C, Hongming T, Patrik I, Zide J, Shining Z (2009) Artificial inoculation of banana tissue culture plantlets with indigenous endophytes originally derived from native banana plants. Biol Control 51:427–434. Scholar
  64. Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, Varma A, Oelmüller R, Tuteja N, Johri AK (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav 8(10):e26891. Scholar
  65. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root colonizing fungi. New Phytol 140:295–310. Scholar
  66. Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265. Scholar
  67. Kageyama SA, Mandyam KG, Jumpponen A (2008) Diversity, function and potential applications of the root-associated endophytes. In: Varma A (ed) Mycorrhiza. Springer, Berlin/Heidelberg. Scholar
  68. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728. Scholar
  69. Kaushal M, Wani SP (2016) Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agric Ecosyst Environ 231:68–78. Scholar
  70. Khastini RO, Ohta H, Narisawa K (2012) The role of a dark septate endophytic fungus, Veronaeopsis simplex Y34, in Fusarium disease suppression in Chinese cabbage. J Microbiol 50:618–624. Scholar
  71. Khastini RO, Ogawara T, Sato Y, Narisawa K (2014) Control of Fusarium wilt in melon by the fungal endophyte, Cadophora sp. Eur J Plant Pathol 139:339–348. Scholar
  72. Kirk P, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, WallingfordCrossRefGoogle Scholar
  73. Knapp DG, Pintye A, Kovács GM (2012) The dark side is not fastidious – dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS One 7(2):e32570. Scholar
  74. Knapp DG, Kovács GM, Jazta E, Groenewald JZ, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100. Scholar
  75. Ko Ko TW, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120. Scholar
  76. Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite – what decides? Curr Opin Plant Biol 9:358–363. Scholar
  77. Kormanik PP, Bryan WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrhizal assay. Can J Microbiol 26:536–538CrossRefGoogle Scholar
  78. Kosman DJ (2003) Molecular mechanisms of iron uptake in fungi. Mol Microbiol 47:1185–1197. Scholar
  79. Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790. Scholar
  80. Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot 65:6265–6278. Scholar
  81. Kwaśna H, Bateman GL (2007) Microdochium trticicola sp. nov. from the roots of Triticum aestivum in the United Kingdom. Mycologia 99:765–776CrossRefGoogle Scholar
  82. Larsson B, Tjälve H (1978) Studies on the melanin-affinity of metal ions. Acta Physiol 104:479–484CrossRefGoogle Scholar
  83. Leake JR (1994) The biology of mycoheterotrophic (‘saprophytic’) plants. New Phytol 127:171–216. Scholar
  84. Leong SA, Winkelmann G (1998) Molecular biology of iron transport in fungi. Met Ions Biol Syst 35:147–186PubMedGoogle Scholar
  85. Li C, Chen S, Zuo C, Sun Q, Ye Q, Yi G, Huang B (2011) The use of GFP-transformed isolates to study infection of banana with Fusarium oxysporum f. sp. cubense race 4. Eur J Plant Pathol 131:327–340. Scholar
  86. Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206. Scholar
  87. Liu H, Li T, Ding Y, Yang Y, Zhao Z (2017) Dark septate endophytes colonizing the roots of ‘non-mycorrhizal’ plants in a mine tailing pond and in a relatively undisturbed environment, Southwest China. J Plant Interact 12:264–271. Scholar
  88. Lopez JR, Winter JM, Elliott J, Ruane AC, Hoogenboom G, Porter C (2017) Integrating growth stage deficit irrigation into a process-based crop model. Agric For Meteorol 243:84–92. Scholar
  89. Lukešová T, Kohout P, Větrovský T, Vohník M (2015) The potential of dark septate endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle european forest plants. PLoS One 10:e0124752. Scholar
  90. Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS One 8:e78746CrossRefGoogle Scholar
  91. Mandeel QA (2007) Modeling competition for infection sites on roots by nonpathogenic strains of Fusarium oxysporum. Mycopathologia 163:9–20. Scholar
  92. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonizing dark septate endophytic fungi. Stud Mycol 53:173–189. Scholar
  93. Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821CrossRefGoogle Scholar
  94. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant—three way symbiosis required for thermal tolerance. Science 315:513–515. Scholar
  95. Marschner H, Römheld V (1994) Strategies of plants for the acquisition of iron. Plant Soil 165:275–283. Scholar
  96. Martins MA, Tomasella J, Rodriguez DA, Alvalá RCS, Giarolla A, Garofolo LL, Júnior JLS, Paolicchi LTLC, Pinto GLN (2018) Improving drought management in the Brazilian semiarid through crop forecasting. Agric Syst 160:21–30. Scholar
  97. Marulanda A, Azcón R, Ruíz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533. Scholar
  98. Marulanda A, Porcel R, Barea JM, Azcón R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54:543–552. Scholar
  99. Marulanda A, Jose-Miguel B, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. Scholar
  100. Mastouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221. Scholar
  101. Menkis A, Allmer J, Vasiliauskas R, Lygis V, Stenlid J, Finlay R (2004) Ecology and molecular characterization of dark septate fungi from roots, living stems, coarse and fine woody debris. Mycol Res 108:965–973. Scholar
  102. Narisawa K, Tokumasu S, Hashiba T (1998) Suppression of clubroot formation in Chinese cabbage by the root endophytic fungus, Hereroconium chaetospira. Plant Pathol 47:206–210CrossRefGoogle Scholar
  103. Narisawa K, Ohki T, Hashiba T (2000) Suppression of clubroot and Verticillium yellows in Chinese cabbage in the field by the root endophytic fungus, Heteroconium chaetospira. Plant Pathol 49:141–146. Scholar
  104. Narisawa K, Kawamata H, Currah RS, Hashiba T (2002) Suppression of Verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109. Scholar
  105. Narisawa K, Usuki F, Hashiba T (2004) Control of Verticillium yellows in Chinese cabbage by the dark-septate endophytic fungus LtVB3. Phytopathology 94:412–418. Scholar
  106. Narisawa K, Hambleton S, Currah RS (2007) Heteroconium chaetospira, a dark septate root endophyte allied to the Herpotrichiellaceae (Chaetothyriales) obtained from some forest soil samples in Canada using bait plants. Mycoscience 48:274–281. Scholar
  107. Newsham KK (1999) Phialophora graminicola, a dark septate fungus, is a beneficial associate of the grass Vulpia ciliata ssp. ambiqua. New Phytol 144:517–524. Scholar
  108. Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate endophytes in polar regions. Fungal Ecol 2:10–20. Scholar
  109. Ngwene B, George E, Claussen W, Neumann E (2010) Phosphorus uptake by cowpea plants from sparingly available or soluble sources as affected by nitrogen form and arbuscular-mycorrhiza-fungal inoculation. J Plant Nutr Soil Sci 173:353–359. Scholar
  110. Ngwene B, Gabriel E, George E (2013) Influence of different mineral nitrogen sources (NO3 – N vs. NH4+ − N) on arbuscular mycorrhiza development and N transfer in a Glomus intraradices – cowpea symbiosis. Mycorrhiza 23:107–117. Scholar
  111. Niemi K, Scagel C, Häggman H (2004) Application of ectomycorrhizal fungi in vegetative propagation of conifers. Plant Cell Tissue Organ Cult 78:83–91CrossRefGoogle Scholar
  112. Nurdebyandaru N, Hidayat I, Rahayu G, Narisawa K (2013) Interaction between fungal endophyte and plant under stress condition (high temperature), Master thesis. Ibaraki University, JapanGoogle Scholar
  113. O’Dell TE, Massicotte HB, Trappe JM (1993) Root colonization of Lupinus latifolius Agardh. and Pinus contorta Dougl. by Phialocephala fortinii Wang & Wilcox. New Phytol 124:93–100. Scholar
  114. Ohtaka N, Narisawa K (2008) Molecular characterization and endophytic nature of the root-associated fungus Meliniomyces variabilis (LtVB3). J Gen Plant Pathol 74:24–31. Scholar
  115. Paparu P, Dubois T, Gold CS, Adpala E, Niere B, Coyne D (2004) Inoculation, colonization, and distribution of fungal endophytes in Musa tissue culture plants. Uganda J Agric Sci 9:583–589Google Scholar
  116. Pereyra MA, García P, Colabelli MN, Barassi CA, Creus CM (2012) A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Appl Soil Ecol 53:94–97. Scholar
  117. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  118. Pócsi I (2011) Toxic metal/metalloid tolerance in fungi—a biotechnology-oriented approach. In: Banfalvi G (ed) Cellular effects of heavy metals. Springer, New York, pp 31–58. Scholar
  119. Poirier Y, Bucher M (2002) Phosphate transport and homeostasis. In: Somerville CR, Meyerowitz EM (eds) Arabidopsis. American Society of Plant Biologists, Rockville. Scholar
  120. Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM (2017) Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant Aquaporins than in a drought-tolerant cultivar. Front Plant Sci 8:1056. Scholar
  121. Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:23–128. Scholar
  122. Rains KC, Nadkarni NM, Bledsoe CS (2003) Epiphytic and terrestrial mycorrhizas in a lower montane Costa Rican cloud forest. Mycorrhiza 13:257–264. Scholar
  123. Read DJ, Haselwandter K (1981) Observations on the mycorrhizal status of some alpine plant communities. New Phytol 88:341–352CrossRefGoogle Scholar
  124. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581. Scholar
  125. Reeve JR, Smith JL, Carpenter-Boggs L, Reganold JP (2008) Soil-based cycling and differential uptake of amino acids by three species of strawberry (Fragaria spp.) plants. Soil Biol Biochem 40:2547–2552. Scholar
  126. Robertson NF (1954) Studies on the mycorrhiza of Pinus sylvestris. I. Patterns of development of mycorrhizal roots and its significance for experimental studies. New Phytol 53:253–283CrossRefGoogle Scholar
  127. Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114. Scholar
  128. Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high-stress environments. Mitig Adapt Strateg Glob Chang 9:261–272. Scholar
  129. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. Int Soc Microb Ecol 2:404–416. Scholar
  130. Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. Scholar
  131. Ruotsalainen AL, Väre H, Vestberg M (2002) Seasonality of root fungal colonization in low-alpine herbs. Mycorrhiza 12:29–36. Scholar
  132. Ruttenberg KC (2003) The global phosphorus cycle. Treatise Geochem 8:585–643. Scholar
  133. Schadt CW, Schmidt SK, Mullen RB (2001) Isolation and phylogenetic identification of a dark-septate fungus associated with the alpine plant Ranunculus adoneus. New Phytol 150:747–755. Scholar
  134. Schardl CL (1996) Epichloë species: fungal symbionts of grasses. Annu Rev Phytopathol 34:109–130. Scholar
  135. Schimel JP, Bennett J (2004) Nitrogen mineralization challenges of a changing paradigm. Ecology 85:591–602. Scholar
  136. Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA, Halloy SRP, Schadt CW (2008) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and the Rocky Mountains. Arct Antarct Alp Res 40:576–583.[SCHMIDT]2.0.CO;2CrossRefGoogle Scholar
  137. Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531. Scholar
  138. Serra-Wittling C, Houot S, Alabouvette C (1996) Increased soil suppressiveness to Fusarium wilt of flax after addition of municipal solid waste compost. Soil Biol Biochem 28:1207–1214. Scholar
  139. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. 2nd edn. Academic Press, LondonGoogle Scholar
  140. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystems scales. Annu Rev Plant Biol 63:227–250. Scholar
  141. Steppe TF (1996) Consortial N fixation: a strategy for meeting the nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21:149–156. Scholar
  142. Stoyke G, Currah RS (1991) Endophytic fungi from the mycorrhizae of alpine ericoid plants. Can J Bot 69:347–352. Scholar
  143. Stoyke G, Currah RS (1993) Resynthesis in pure culture of a common subalpine fungus-root association using Phialocephala fortinii and Menziesia ferruginea (Ericaceae). Arct Alp Res 25:89–193CrossRefGoogle Scholar
  144. Sullia SB (1991) Use of vesicular-arbuscular mycorrhiza (VAM) as biofertilizer for horticultural plants in developing countries. In: Prakash J, Pierik RLM (eds) Horticulture – new technologies and applications, current plant science and biotechnology in agriculture, vol 12. Springer, Dordrecht. Scholar
  145. Sun C, Johnson JM, Cai D, Sherameti I, Oelmuller 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 167:1009–1017. Scholar
  146. Surono, 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. Scholar
  147. Swain P, Raman A, Singh SP, Kumar A (2017) Breeding drought tolerant rice for the shallow rainfed ecosystem of eastern India. Field Crop Res 209:168–178. Scholar
  148. Takashima Y, Narisawa K, Hidayat I, Rahayu G (2014) First report on fungal symbionts of Lycopodiaceae root from Mount Gede Pangrango National Park Indonesia. J Dev Sustain Agric 9:81–88. Scholar
  149. Tefera T, Vidal S (2009) Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54:663–669. Scholar
  150. Tian C, Kasiborski B, Koul R, Lammers PJ, Bucking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153(3):1175–1187. Scholar
  151. Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310. Scholar
  152. Tsai HF, Liu JS, Staben C, Christensen MJ, Latch GCM, Siegel MR, Schardl CL (1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proc Natl Acad Sci USA 91:2542–2546CrossRefGoogle Scholar
  153. Umar A (2017) Phytohyperaccumulator-AMF (arbuscular mycorrhizal fungi) interaction in heavy metals detoxification of soil. Acta Biol Paranaen Curitiba 46:123–148. Scholar
  154. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122. Scholar
  155. Upson R, Newsham KK, Bridge PD, Pearce DA, Read DJ (2009) Taxonomic affinities of dark septate root endophytes of Colobanthus quitensis and Deschampsia Antarctica, the two native Antarctic vascular plant species. Fungal Ecol 2:184–196. Scholar
  156. Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184CrossRefGoogle Scholar
  157. Usuki F, Narisawa K, Yonezawa M, Kakishima M, Hashiba T (2002) An efficient inoculation method for colonization of Chinese cabbage seedlings by the root endophytic fungus Heteroconium chaetospira. J Gen Plant Pathol 68:326–332. Scholar
  158. Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. Scholar
  159. Varma A, Sudha S, Franken P (1999) Piriformospora indica cultivable plant growth promoting root endophyte with similarities to arbuscular mycorrhizal fungi. Appl Environ Microbiol 65:2741–2744PubMedPubMedCentralGoogle Scholar
  160. Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012) Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agric Res 1:117–131. Scholar
  161. Vergara C, Araujo KEC, Urquiaga S, Schultz N, Balieiro FC, Medeiros PS, Santos LA, Xavier GR, Zilli JE (2017) Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material. Front Microbiol 8:1–12. Scholar
  162. Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24. Scholar
  163. Walker JW, Johnson LC, Simpson NB, Bill M, Jumpponen A (2010) Application of fungistatic in soil reduces N uptake by an arctic ericoid shrub (Vaccinium vitisidea). Mycologia 102:822–834CrossRefGoogle Scholar
  164. Wang SX, Xia ST, Peng KQ, Kuang FC, Cao Y, Xiao LT (2007) Effects of formulated fertilizer synergist on abscisic acid accumulation, proline content and photosynthetic characteristics of rice under drought. Rice Sci 14:42–48. Scholar
  165. War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792. Scholar
  166. Weishample PA, Bedford BL (2006) Wetland dicots and monocots differ in colonization by arbuscular mycorrhizal fungi and dark septate endophytes. Mycorrhiza 16:495–502. Scholar
  167. Wilcox HE, Wang CJK (1987) Ectomycorrhizal and ectendomycorrhizal associations of Phialophora finlandia with Pinus resinosa, Picea rubens, and Betula alleghaensis. Can J For Res 17:976–990. Scholar
  168. Winter JM, Young CA, Mehta VK, Ruane AC, Azarderakhsh M, Davitt A, McDonald K, Haden VR, Rosenzweig C (2017) Integrating water supply constraints into irrigated agricultural simulations of California. Environ Model Softw 96:335–346. Scholar
  169. Wu H, Chen C, Du J, Liu H, Cui Y, Zhang Y et al (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800. Scholar
  170. Xu R, Li T, Cui H, Wang J, Yu X, Ding Y, Wang C, Yang Z, Zhao Z (2015) Diversity and characterization of Cd-tolerant dark septate endophytes (DSEs) associated with the roots of Nepal alder (Alnus nepalensis) in a metal mine tailing of southwest China. Appl Soil Ecol 93:11–18. Scholar
  171. Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544. Scholar
  172. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132. Scholar
  173. Yu T, Nassuth A, Peterson RL (2001) Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Can J Microbiol 47:741–753. Scholar
  174. Zhan F, Li T, He Y, Zhao Z, Zu Y (2011) Characterization of melanin isolated from a dark septate endophyte (DSE), Exophiala pisciphila. World J Microbiol Biotechnol 27:2483–2489. Scholar
  175. Zhang Y, Zhang Y, Liu M, Shi X, Zhao Z (2008) Dark septate endophyte (DSE) fungi isolated from metal polluted soils: their taxonomic position, tolerance, and accumulation of heavy metals in vitro. J Microbiol 46:624–632. Scholar
  176. Zhang X, St. Leger RJ, Fang W (2017) Pyruvate accumulation is the first line of cell defense against heat stress in a fungus. MBio 8:e01284–e01217. Scholar
  177. Zhao D, Li T, Shen M, Wang J, Zhao Z (2015) Diverse strategies conferring extreme cadmium (Cd) tolerance in the dark septate endophyte (DSE), Exophiala pisciphila: evidence from RNA-Seq data. Microbiol Res 170:27–35. Scholar
  178. Zu X, La H, Lu Y, Wang Q, Chu P, Miao W, Wang H (2017) A new method for evaluating the drought tolerance of upland rice cultivars. Crop J 5:488–498. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Iman Hidayat
    • 1
  1. 1.Microbiology Division, Research Center for BiologyIndonesian Institute of Sciences (LIPI)CibinongIndonesia

Personalised recommendations