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7 - From Darkness to Light: Emergence of the Mysterious Dark Septate Endophytes in Plant Growth Promotion and Stress Alleviation

from Part II - Role of Endophytes in Growth and Biotic and Abiotic Stress Resistance

Published online by Cambridge University Press:  01 April 2019

By
Charlotte Berthelot ,
Michel Chalot ,
Corinne Leyval  and
Damien Blaudez
Edited by
Trevor R. Hodkinson ,
Fiona M. Doohan ,
Matthew J. Saunders  and
Brian R. Murphy
Trevor R. Hodkinson
Affiliation:
Trinity College Dublin
Fiona M. Doohan
Affiliation:
University College Dublin
Matthew J. Saunders
Affiliation:
Trinity College Dublin
Brian R. Murphy
Affiliation:
Trinity College Dublin
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Summary

Dark septate endophytes (DSEs) are ascomycetous fungi whose structure is characterised by dark melanised hyphae and microsclerotia located in plant roots. Associations with DSEs are commonly found in various biomes and plant taxa. Although DSEs are commonly recorded, the effects of their colonisation on plant growth and fitness are unclear. This chapter summarises the state of knowledge about DSEs from the literature and personal data. The effects of DSEs on plant growth range from parasitism to mutualism. They can promote plant growth by improving nutrition (e.g. solubilisation of minerals, degradation of complex carbon compounds), producing secondary metabolites (e.g. phytohormones, volatile organic compounds) and protecting against phytopathogens. More particularly, the high tolerance of DSEs to abiotic stress and their relatively high abundance in trace element-contaminated and other stressful habitats suggest that they may have an important function for host survival under these conditions. Finally, this chapter outlines why additional research is required in the emerging field of plant–DSE interactions to address future challenges.

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Endophytes for a Growing World , pp. 143 - 164
Publisher: Cambridge University Press
Print publication year: 2019

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References

Addy, H. D., Piercey, M. M. and Currah, R. S. (2005). Microfungal endophytes in roots. Canadian Journal of Botany-Revue Canadienne de Botanique, 83, 1–13.Google Scholar
Alberton, O., Kuyper, T. W. and Summerbell, R. C. (2009). Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil, 328, 459–470.CrossRefGoogle Scholar
Andrade-Linares, D. R., Grosh, R., Restrepo, S. et al. (2011). Effects of dark septate endophytes on tomato plant performance. Mycorrhiza, 21, 413–422.CrossRefGoogle ScholarPubMed
Ban, Y., Tang, M., Chen, H. et al. (2012). The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One, 7, e47968.CrossRefGoogle ScholarPubMed
Ban, Y., Xu, Z., Yang, Y. et al. (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.CrossRefGoogle Scholar
Bartholdy, B., Berreck, M. and Haselwandter, K. (2001). Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals, 14, 33–42.CrossRefGoogle ScholarPubMed
Berthelot, C., Leyval, C., Foulon, J. et al. (2016). Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiology Ecology, 92, fiw144.CrossRefGoogle ScholarPubMed
Berthelot, C., Blaudez, D. and Leyval, C. (2017). Differential growth promotion of poplar and birch inoculated with three dark septate endophytes in two trace element-contaminated soils. International Journal of Phytoremediation, 19,1118–1125.CrossRefGoogle ScholarPubMed
Berthelot, C., Blaudez, D., Beguiristain, T. et al. (2018). Co-inoculation of Lolium perenne with Funneliformis mosseae and the dark septate endophyte Cadophora sp. in a trace element-polluted soil. Mycorrhiza, 28 , 301–314.CrossRefGoogle Scholar
Bois, G., Bertrand, A., Piché, Y. et al. (2006). Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations. Mycorrhiza, 16, 99–109.CrossRefGoogle Scholar
Brundrett, M. C. (2006). Understanding the roles of multifunctional mycorrhizal and endophytic fungi. In Microbial Root Endophytes, ed. Schulz, B, Boyle, C. and Sieber, T. N. Berlin: Springer, pp. 281–298.CrossRefGoogle Scholar
Butler, M. and Day, A. (1998). Fungal melanins: a review. Canadian Journal of Microbiology, 44, 1115–1136.CrossRefGoogle Scholar
Caldwell, B. A., Jumpponen, A. and Trappe, J. M. (2000). Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia, 92, 230–232.CrossRefGoogle Scholar
Compant, S., Saikkonen, K., Mitter, B. et al. (2016). Editorial special issue: soil, plants and endophytes. Plant and Soil, 405, 1CrossRefGoogle Scholar
David, A. S., Haridas, S., LaButti, K. et al. (2016). Draft genome sequence of Microdochium bolleyi, a dark septate fungal endophyte of beach grass. Genome Announcements, 4, e00270–16.CrossRefGoogle ScholarPubMed
Della Monica, I. F., Saparrat, M. C. N., Godeas, A. M. et al. (2015). The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes. Fungal Ecology, 17, 10–17.CrossRefGoogle Scholar
De Maria, S. Rivelli, A. R., Kuffner, M. et al. (2011). Interactions between accumulation of trace elements and macronutrients in Salix caprea after inoculation with rhizosphere microorganisms. Chemosphere, 84, 1256–1261.CrossRefGoogle ScholarPubMed
Deram, A., Languereau, F. and Haluwyn, C. Van. (2011). Mycorrhizal and endophytic fungal colonization in Arrhenatherum elatius L. roots according to the soil contamination in heavy metals. Soil and Sediment Contamination, 20, 114–127.CrossRefGoogle Scholar
Grünig, C. R., Queloz, V. and Sieber, T. N. (2011). Structure of diversity in dark septate endophytes: from species to genes. In Endophytes of forest trees, ed. Pirtilla, A. M and Franck, A. C. London: Springer, pp. 3–30.CrossRefGoogle Scholar
Harman, G. E., Howell, C., Viterbo, A. et al. (2004). Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2, 43–56.CrossRefGoogle ScholarPubMed
Haselwandter, K. and Read, D. J. (1982). The significance of a root-fungus association in two Carex species of high-alpine plant communities. Oecologia, 53, 352–354.CrossRefGoogle ScholarPubMed
He, Y., Yang, Z., Li, M. et al. (2017). Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress. Environmental Science and Pollution Research International, 24. doi: 10.1007/s11356-017-9459-6.CrossRefGoogle ScholarPubMed
Hilbert, M., Voll, L. M., Ding, L. et al. (2012). Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytologist, 196, 520–534.CrossRefGoogle Scholar
Hung, R., Lee, S. and Bennett, J. W. (2013). Arabidopsis thaliana as a model system for testing the effect of Trichoderma volatile organic compounds. Fungal Ecology, 6, 19–26.CrossRefGoogle Scholar
Jumpponen, A. and Trappe, J. M. (1998a). Dark septate endophytes: a review with special reference to facultative biotrophic root-colonizing fungi. New Phytologist, 140, 295–310.CrossRefGoogle Scholar
Jumpponen, A. and Trappe, J. M. (1998b). Performance of Pinus contorta inoculated with two strains of root endophytic fungus, Phialocephala fortinii: effects of synthesis system and glucose concentration. Canadian Journal of Botany, 76, 1205–1213.CrossRefGoogle Scholar
Jumpponen, A., Trappe, J. M. and Mattson, K. (1998). Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza, 7, 261–265.CrossRefGoogle ScholarPubMed
Khan, A.L., Hamayun, M., Ahmad, N. et al. (2011). Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiologia Plantarum, 143, 329–43.CrossRefGoogle ScholarPubMed
Khastini, R. O., Ogawara, T., Sato, Y. et al. (2014). Control of Fusarium wilt in melon by the fungal endophyte, Cadophora sp. European Journal of Plant Pathology, 139, 333–342.CrossRefGoogle Scholar
Knapp, D. G. and Kovács, G. M. (2016). Interspecific metabolic diversity of root colonizind fungi reveals by enzyme activity tests. FEMS Microbiology Ecology, 92, p.fiw190.CrossRefGoogle ScholarPubMed
Knapp, D. G., Pintye, A. and Kovács, G. M. (2012). The dark side is not fastidious: dark septate endophytic fungi of native and invasive plants of semiarid sandy areas. PLoS One, 7, p.e32570.CrossRefGoogle Scholar
Kovàcs, G. M. and Szigetvari, C. (2002). Mycorrhizae and other root-associated fungal structures of the plants of a sandy grassland on the Great Hungarian Plain. Phyton – Annales Rei Botanicae, 42, 211–223.Google Scholar
Kramer, R. and Abraham, W. R. (2012). Volatile sesquiterpenes from fungi: what are they good for? Phytochemistry Reviews, 11, 15–37.CrossRefGoogle Scholar
Lacercat-Didier, L., Berthelot, C., Foulon, J. et al. (2016). New mutualistic fungal endophytes isolated from poplar roots display high metal tolerance. Mycorrhiza, 26, 1–15.CrossRefGoogle ScholarPubMed
Lemfack, M. C., Nickel, J., Dunkel, M. et al. (2014). MVOC: a database of microbial volatiles. Nucleic Acids Research, 42, 744–748.CrossRefGoogle ScholarPubMed
Li, T., Liu, M. J., Zhang, X. T. et al. (2011). Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. The Science of the Total Environment, 409, 1069–1074.CrossRefGoogle ScholarPubMed
Likar, M. and Regvar, M. (2009). Application of temporal temperature gradient gel electrophoresis for characterisation of fungal endophyte communities of Salix caprea L. in a heavy metal polluted soil. The Science of the Total Environment, 407, 6179–6187.CrossRefGoogle Scholar
Likar, M. and Regvar, M. (2013). Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant and Soil, 370, 593–604.CrossRefGoogle Scholar
Mahmoud, R. S. and Narisawa, K. (2013). A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS One, 8, e78746.CrossRefGoogle ScholarPubMed
Mandyam, K. G. and Jumpponen, A. (2005). Seeking the elusive function of the root-colonising dark septate endophytic fungi. Studies in Mycology, 53, 173–189.CrossRefGoogle Scholar
Mandyam, K. G. and Jumpponen, A. (2014). Unraveling the dark septate endophyte functions: insights from the Arabidospis model. In Advances in Endophytic Research, ed. Verma, V. C and Gange, A. C. India: Springer, pp. 115–141.CrossRefGoogle Scholar
Mandyam, K. G. and Jumpponen, A. (2015). Mutualism–parasitism paradigm synthesized from results of root-endophyte models. Frontiers in Microbiology, 5, 1–13.CrossRefGoogle ScholarPubMed
Mandyam, K. G., Roe, J. and Jumpponen, A. (2013). Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biology, 117, 250–260.CrossRefGoogle ScholarPubMed
Mayerhofer, M. S., Kernaghan, G. and Harper, K. A. (2013). The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza, 23, 119–128.CrossRefGoogle ScholarPubMed
Melin, E. (1921). Über die mykorrhizapilze von Pinus sylvestris L. und Picea abies (L.) Karst. (vorläufige mitteilungen). Svensk Botanisk Tidskrift, 15, 192–203.Google Scholar
Narisawa, K., Ohki, K. T. and Hashiba, T. (2000). Suppression of clubroot formation in Chinese cabbage by the root endophytic fungus, Heteroconium chaetospira. Plant Pathology, 49, 141–146.CrossRefGoogle Scholar
Narisawa, K., Kawamata, H., Currah, S. H. et al. (2002). Suppression of Verticillium wilt in eggplant by some fungal root endophytes. European Journal of Plant Pathology, 108, 103–109.CrossRefGoogle Scholar
Naznin, H. A., Kimura, N., Miyasawa, M. et al. (2013). Analysis of volatile organic compounds emitted by plant growth-promoting fungus Phoma sp. GS8-3 for growth promotion effects on tobacco. Microbes and Environments, 28, 42–49.CrossRefGoogle ScholarPubMed
Newsham, K. K. (2011). A meta-analysis of plant responses to dark septate root endophytes. New Phytologist, 190, 783–793.CrossRefGoogle ScholarPubMed
Op De Beeck, M., Lievens, B., Busschaert, P. et al. (2015). Impact of metal pollution on fungal diversity and community structures. Environmental Microbiology, 17, 2035–2047.CrossRefGoogle ScholarPubMed
Paul, D. and Park, K. (2013). Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors (Basel, Switzerland), 13, 13969–13977.CrossRefGoogle ScholarPubMed
Peterson, R. L., Wagg, C. and Pautler, M. (2008). Associations between microfungal endophytes and roots: do structural features indicate function? Botany, 86, 445–456.CrossRefGoogle Scholar
Peyronel, B. (1924). Prime ricerche sulla micorizae endotrofiche e sulla microflora radicola normalle della fanerograme. Revista Biologia, 6 , 463–485.Google Scholar
Porras-Alfaro, A. and Bayman, P. (2011). Hidden fungi, emergent properties: endophytes and microbiomes. Annual Review of Phytopathology, 49, 291–315.CrossRefGoogle ScholarPubMed
Read, D. J. and Haselwandter, K. (1981). Observations on the mycorrhizal status of some alpine plant communities. The New Phytologist, 88, 341–352.CrossRefGoogle Scholar
Reininger, V. and Schlegel, M. (2016). Analysis of the Phialocephala subalpina transcriptome during colonization of its host plant Picea abies. PLoS One, 11, 1–16.CrossRefGoogle ScholarPubMed
Ruotsalainen, A. L. and Kytöviita, M. M. (2004). Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. Oecologia, 140, 226–233.CrossRefGoogle Scholar
Ruotsalainen, A. L., Markkola, A. and Kozlov, M. V. (2007). Root fungal colonisation in Deschampsia flexuosa: Effects of pollution and neighbouring trees. Environmental Pollution, 147, 723–728.CrossRefGoogle ScholarPubMed
Schulz, B. and Boyle, C. (2005). The endophytic continuum. Mycological Research, 109, 661–686.CrossRefGoogle ScholarPubMed
Schulz, B., Boyle, C., Draeger, S. et al. (2002). Endophytic fungi: a source of novel biologically active secondary metabolites. Mycological Research, 106, 996–1004.CrossRefGoogle Scholar
Spagnoletti, F. N., Tobar, N., di Pardo, F. et al. (2017). Dark septate endophytes present different potential to solubilize calcium, iron and aluminum phosphates. Applied Soil Ecology, 111, 25–32.CrossRefGoogle Scholar
Strobel, G. A., Dirkse, E., Sears, J. et al. (2001). Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology, 147, 2943–2950.CrossRefGoogle ScholarPubMed
Su, Z. Z., Mao, L.-J., Li, N. et al. (2013). Evidence for biotrophic lifestyle and biocontrol potential of dark septate endophyte Harpophora oryzae to rice blast disease. PLoS One, 8, e61332.CrossRefGoogle ScholarPubMed
Sukumar, P., Legué, V., Vayssière, A. et al. (2013). Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant, Cell and Environment, 36, 909–919.CrossRefGoogle ScholarPubMed
Surono, and 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 Ecology, 28, 1–10.CrossRefGoogle Scholar
Tamura, K., Stecher, D., Perterson, D. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefGoogle ScholarPubMed
Tellenbach, C. and Sieber, T. N. (2012). Do colonization by dark septate endophytes and elevated temperature affect pathogenicity of oomycetes? FEMS Microbiology Ecology, 82, 157–168.CrossRefGoogle ScholarPubMed
Tellenbach, C., Sumarah, M. W., Grunig, C. R. et al. (2013). Inhibition of Phytophthora species by secondary metabolites produced by the dark septate endophyte Phialocephala europaea. Fungal Ecology, 6, 12–18.CrossRefGoogle Scholar
Terhonen, E., Kerio, S., Sun, H. et al. (2014). Endophytic fungi of Norway spruce roots in boreal pristine mire, drained peatland and mineral soil and their inhibitory effect on Heterobasidion parviporum in vitro. Fungal Ecology, 9, 17–26.CrossRefGoogle Scholar
Terhonen, E., Sipari, N. and Asiegbu, F. O. (2016). Inhibition of phytopathogens by fungal root endophytes of Norway spruce. Biological Control, 99, 53–63.CrossRefGoogle Scholar
Upson, R., Read, D. J. and Newsham, K. K. (2009). Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza, 20, 1–11.CrossRefGoogle ScholarPubMed
Usuki, F. and Narisawa, K. (2007). A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia, 99, 175–184.CrossRefGoogle Scholar
Utmazian, M. N. D. S., Sweiger, P., Sommer, P. et al. (2007). Influence of Cadophora finlandica and other microbial treatments on cadmium and zinc uptake in willows grown on polluted soil. Plant Soil and Environment, 53, 158–166.CrossRefGoogle Scholar
Vohník, M., Albrechtová, J. and Vosátka, M. (2005). The inoculation with Oidodendron maius and Phialocephala fortinii alters phosphorus and nitrogen uptake, foliar C:N ratio and root biomass distribution in Rhododendron cv. Azurro. Symbiosis, 40, 87–96.Google Scholar
Vrålstad, T., Myrhe, E. and Schumasher, T. (2002). Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytologist, 155, 131–148.CrossRefGoogle ScholarPubMed
Wang, J., Li, T., Liu, G.-Y. et al. (2016). Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Nature Scientific Reports, 6, 1–12.Google ScholarPubMed
Xu, R., Li, T., Cui, H. et al. (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. Applied Soil Ecology, 93, 11–18.CrossRefGoogle Scholar
Xu, X. H., Su, Z.-Z., Wang, C. et al. (2014). The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte. Scientific Reports, 4, 1–9.Google ScholarPubMed
Yu, T., Nassuth, A. and Peterson, R. L. (2001). Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Canadian Journal of Microbiology, 47, 741–753.CrossRefGoogle ScholarPubMed
Zhan, F., Li, T., Cui, H. et al. (2016). Effects of tricyclazole on cadmium tolerance and accumulation characteristics of a dark septate endophyte (DSE), Exophiala pisciphila. Bulletin of Environmental Contamination and Toxicology, 96, 235–241.CrossRefGoogle ScholarPubMed
Zhan, F., Li, T., Cui, H. et al. (2017). Effects of a dark septate endophyte (DSE) on the glutathione metabolism in maize plants under cadmium. Journal of Plant Interactions, 12, 421–428.CrossRefGoogle Scholar
Zhang, Q., Gong, M., Yuan, J. et al. (2017). Dark septate endophyte improves drought tolerance in sorghum. International Journal of Agriculture and Biology, 19, 53–60.CrossRefGoogle Scholar
Zhang, Y., Zhang, Y., Liu, M. et al. (2008). Dark septate endophyte (DSE) fungi isolated from metal polluted soils: their taxonomic position, tolerance, and accumulation of heavy metals in vitro. Journal of Microbiology, 46, 624–632.CrossRefGoogle ScholarPubMed

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