Abstract
Aims
This study aimed to investigate how dark septate endophytes (DSE) from arid habitats affect host growth and their application to crops and medicinal plants in drought-prone soils.
Methods
First, the osmotic-stress tolerance of Paraphoma sp., Embellisia chlamydospora, and Cladosporium oxysporum, isolated from Hedysarum scoparium, was tested using osmotically adjusted pure culture. Second, we examined the performance of host (H. scoparium) and non-host (Glycyrrhiza uralensis and Zea mays) plants inoculated with these fungi under mild (MD) and extreme drought (ED) conditions in a growth chamber.
Results
All the DSE showed high tolerance to osmotic stress in vitro and could colonise the roots of all the plants. For H. scoparium, DSE improved the root biomass and length depending on DSE species, with Paraphoma sp. and C. oxysporum exhibiting positive effects under all the drought treatments. For G. uralensis and Z. mays, DSE inoculation enhanced the root development of plants under MD condition and was dependent on the plant–fungus species. However, this positive effect was weakened under extreme drought stress.
Conclusions
DSE isolated from H. scoparium enhanced the root growth of the host plant under drought conditions and may also be used to promote the cultivation of agricultural and medicinal plants.
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References
Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470. https://doi.org/10.1007/s11104-009-0125-8
Alvarez-Flores R, Winkel T, Nguyen-Thi-Truc A, Joffre R (2014) Root foraging capacity depends on root system architecture and ontogeny in seedlings of three Andean Chenopodium species. Plant Soil 380:415–428. https://doi.org/10.1007/s11104-014-2105-x
Andrade-Linares DR, Grosch R, Restrepo S, Krumbein A, Franken P (2011) Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21:413–422. https://doi.org/10.1007/s00572-010-0351-1
Ashrafi S, Knapp DG, Blaudez D, Chalot M, Maciá-Vicente JG, Zagyva I, Dababat AA, Maier W, Kovács GM (2018) Inhabiting plant roots, nematodes, and truffles- Polyphilus, a new helotialean genus with two globally distributed species. Mycologia 110:286–299. https://doi.org/10.1080/00275514.2018.1448167
Awad W, Byrne PF, Reid SD, Comas LH, Haley SD (2018) Great plains winter wheat varies for root length and diameter under drought stress. Agron J 110:226–235. https://doi.org/10.2134/agronj2017.07.0377
Azcón-Aguilar C, Palenzuela J, Roldán A, Bautista S, Vallejo R, Barea JM (2003) Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertification-threatened Mediterranean shrublands. Appl Soil Ecol 22:29–37. https://doi.org/10.1016/S0929-1393(02)00107-5
Bai X, Zhu J, Zhao A, Su P, Bu Q, Zhao X (2008) Comparison of physiological adaptabilities of several desert plants to drying stress. Chin J Appl Environ Biol 14(6):763–768. (In Chinese)
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. https://doi.org/10.1371/journal.pone.0047968
Ban Y, Xu Z, Yang Y, Zhang H, Chen H, Tang M (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
Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247. https://doi.org/10.1007/s00572-003-0222-0
Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol Ecol 92:fiw144. https://doi.org/10.1093/femsec/fiw144
Berthelot C, Perrin Y, Leyval C, Blaudez D (2017a) Melanization and ageing are not drawbacks for successful agro-transformation of dark septate endophytes. Fungal Biol 121:652–663. https://doi.org/10.1016/j.funbio.2017.04.004
Berthelot C, Blaudez D, Leyval C (2017b) Differential growth promotion of poplar and birch inoculated with three dark septate endophytes in two trace element-contaminated soils. Int J Phytoremediat 19:1118–1125. https://doi.org/10.1080/15226514.2017.1328392.
Biemann B, Linderman RG (1981) Quantifying vesicular arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87(1):63–67. https://doi.org/10.1111/j.1469-8137.1981.tb01690.x
Bloomfield BJ, Alexander M (1967) Melanins and resistance of fungi to lysis. J Bacteriol 93:1276–1280
Butler M, Day A (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136. https://doi.org/10.1139/w98-119
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30(3):239–264. https://doi.org/10.1071/FP02076
Chen DM, Khalili K, Cairney JWG (2003) Influence of water stress on biomass production by isolates of an ericoid mycorrhizal endophyte of Woollsia pungens and Epacris microphylla (Ericaceae). Mycorrhiza 13:173–176. https://doi.org/10.1007/s00572-003-0228-7
Chen YL, Dunbabin VM, Diggle AJ, Siddique KHM, Rengel Z (2012) Assessing variability in root traits of wild Lupinus angustifolius germplasm: basis for modelling root system structure. Plant Soil 354:141–155. https://doi.org/10.1007/s11104-011-1050-1
Collin-Hansen C, Andersen RA, Steinnes E (2005) Molecular defense systems are expressed in the king bolete (Boletus edulis) growing near metal smelters. Mycologia 97:973–983. https://doi.org/10.1080/15572536.2006.11832747
Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442. https://doi.org/10.3389/fpls.2013.00442
Della Monica IF, Saparrat MCN, Godeas AM, Scervino JM (2015) The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes. Fungal Ecol 17:10–17. https://doi.org/10.1016/j.funeco.2015.04.004
Deng J, Ding G, Gao G, Wu B, Zhang Y, Qin S, Fan W (2015) The sap flow dynamics and response of Hedysarum scoparium to environmental factors in semiarid northwestern China. PLoS One 10:e0131683. https://doi.org/10.1371/journal.pone.0131683
Diene O, Sakagami N, Narisawa K (2014) The role of dark septate endophytic fungal isolates in the accumulation of cesium by Chinese cabbage and tomato plants under contaminated environments. PLoS One 9:e109233. https://doi.org/10.1371/journal.pone.0109233
Elavarthi S, Martin B (2010) Spectrophotometric assays for antioxidant enzymes in plants. In: Sunkar R. (eds) plant stress tolerance. Methods in molecular biology (methods and protocols), 639. Humana Press
Ellis DH, Griffiths DA (1974) The location and analysis of melanins in the cell walls of some soil fungi. Can J Microbiol 20(10):1379–1386. https://doi.org/10.1139/m74-212
Fernandez CW, Koide RT (2013) The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecol 6:479–486. https://doi.org/10.1016/j.funeco.2013.08.004
Gong C, Wang J, Hu C, Wang J, Ning P, Bai J (2015) Interactive response of photosynthetic characteristics in Haloxylon ammodendron and Hedysarum scoparium exposed to soil water and air vapor pressure deficits. J Environ Sci 34:184–196. https://doi.org/10.1016/j.jes.2015.03.012
González-Teuber M, Urzúa A, Plaza P, Bascuñán-Godoy L (2018) Effects of root endophytic fungi on response of Chenopodium quinoa to drought stress. Plant Ecol 219:231–240. https://doi.org/10.1007/s11258-017-0791-1
Hund A, Ruta N, Liedgens M (2009) Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance. Plant Soil 318:311–325. https://doi.org/10.1007/s11104-008-9843-6
Jin HQ, Liu HB, Xie YY, Zhang YG, Xu QQ, Mao LJ, Li XJ, Chen J, Lin FC, Zhang CL (2018) Effect of the dark septate endophytic fungus Acrocalymma vagum on heavy metal content in tobacco leaves. Symbiosis 74:89–95. https://doi.org/10.1007/s13199-017-0485-4
Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310. https://doi.org/10.1046/j.1469-8137.1998.00265.x
Junges E, Muniz MFB, Bastos BO, Oruoski P (2016) Biopriming in bean seeds. Acta Agr Scand, B-SP 66:207–214. https://doi.org/10.1080/09064710.2015.1087585
Kannadan S, Rudgers JA (2008) Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol 22:706–713. https://doi.org/10.1111/j.1365-2435.2008.01395.x
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. https://doi.org/10.1007/s12275-012-2105-6
Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457. https://doi.org/10.3732/ajb.1200558
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:e32570. https://doi.org/10.1371/journal.pone.0032570
Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia-Molecular Phylogeny and Evolution of Fungi 35:87–100. https://doi.org/10.3767/003158515X687669
Knapp DG, Németh JB, Barry K, Hainaut M, Henrissat B, Johnson J, Kuo A, Lim JHP, Lipzen A, Nolan M, Ohm RA, Tamás L, Grigoriev IV, Spatafora JW, Nagy LG, Kovács GM (2018) Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Sci Rep 8:6321. https://doi.org/10.1038/s41598-018-24686-4
Li WYF, Shao G, Lam HM (2008) Ectopic expression of GmPAP3 alleviates oxidative damage caused by salinity and osmotic stresses. New Phytol 178:80–91. https://doi.org/10.1111/j.1469-8137.2007.02356.x
Li T, Liu MJ, Zhang XT, Zhang HB, Sha T, Zhao ZW (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074. https://doi.org/10.1016/j.scitotenv.2010.12.012
Li BK, He XL, He C, Chen YY, Wang XQ (2015) Spatial dynamics of dark septate endophytes and soil factors in the rhizosphere of Ammopiptanthus mongolicus in Inner Mongolia, China. Symbiosis 65:75–84. https://doi.org/10.1007/s13199-015-0322-6
Likar M, Regvar M (2013) Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil 370:593–604. https://doi.org/10.1007/s11104-013-1656-6
Liu Y, Xu S, Ling T, Xu L, Shen W (2010) Heme oxygenase/carbon monoxide system participates in regulating wheat seed germination under osmotic stress involving the nitric oxide pathway. J Plant Physiol 167:1371–1379. https://doi.org/10.1111/j.1469-8137.2007.02356.x
López-Coria M, Hernández-Mendoza JL, Sánchez-Nieto S (2016) Trichoderma asperellum induces maize seedling growth by activating the plasma membrane H+-ATPase. MPMI 29:797–806. https://doi.org/10.1094/mpmi-07-16-0138-r
Lugo MA, Molina MG, Crespo EM (2009) Arbuscular mycorrhizas and dark septate endophytes in bromeliads from south American arid environment. Symbiosis 47:17–21. https://doi.org/10.1007/s11104-013-1656-6
Lugo MA, Reinhart KO, Menoyo E, Crespo EM, Urcelay C (2015) Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment. Mycorrhiza 25:85–95. https://doi.org/10.1007/s00572-014-0592-5
Lugo MA, Menoyo E, Allione LR, Negritto MA, Henning JA, Anton AM (2018) Arbuscular mycorrhizas and dark septate endophytes associated with grasses from the argentine Puna. Mycologia 110:654–665. https://doi.org/10.1080/00275514.2018.1492846
Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189. https://doi.org/10.3114/sim.53.1.173
Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128. https://doi.org/10.1007/s00572-012-0456-9
Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. https://doi.org/10.1111/j.1469-8137.2010.03611.x
Palta JA, Chen X, Milroy SP, Rebetzke GJ, Dreccer MF, Watt M (2011) Large root systems: are they useful in adapting wheat to dry environments? Funct Plant Biol 38:347–354. https://doi.org/10.1071/FP11031
Perez-Naranjo JC (2009) Dark septate and arbuscular mycorrhizal fungal endophytes in roots of prairie grasses. Dissertation. In: University of Saskatchewan
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Trans Br Mycol Soc 55:158–163. https://doi.org/10.1016/S0007-1536(70)80110-3
Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl Environ Microbiol 74:2805–2813. https://doi.org/10.1128/aem.02769-07
Santos SGD, Silva PRAD, Garcia AC, Zilli JÉ, Berbara RLL (2017) Dark septate endophyte decreases stress on rice plants. Braz J Microbiol 48:333–341. https://doi.org/10.1016/j.bjm.2016.09.018
Sheffield J, Andreadis KM, Wood EF, Lettenmaier DP (2009) Global and continental drought in the second half of the twentieth century: severity–area–duration analysis and temporal variability of large-scale events. J Clim 22:1962–1981. https://doi.org/10.1175/2008JCLI2722.1
Shi Z, Mickan B, Feng G, Chen Y (2015) Arbuscular mycorrhizal fungi improved plant growth and nutrient acquisition of desert ephemeral Plantago minuta under variable soil water conditions. J Arid Land 7:414–420. https://doi.org/10.1007/s40333-014-0046-0
Su ZZ, Mao LJ, Li N, Feng XX, Yuan ZL, Wang LW, Lin FC, Zhang CL (2013) Evidence for biotrophic lifestyle and biocontrol potential of dark septate endophyte Harpophora oryzae to rice blast disease. PLoS One 8(4):e61332. https://doi.org/10.1371/journal.pone.0061332
Surono NK (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
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 8:2437. https://doi.org/10.3389/fmicb.2017.02437
Villarreal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192. https://doi.org/10.1111/j.1469-8137.2004.01167.x
Wang JL, Li T, Liu GY, Smith JM, Zhao ZW (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Rep 6:22028. https://doi.org/10.1038/srep22028
Wu LQ, Lv YL, Meng ZX, Chen J, Guo SX (2010) The promoting role of an isolate of dark-septate fungus on its host plant Saussurea involucrata Kar. Et Kir. Mycorrhiza 20:127–135. https://doi.org/10.1007/s00572-009-0268-8
Xie L (2017) Species diversity and salt tolerance of DSE in the roots of Hedysarum scoparium Fisch. Et Mey. In Northwest China. Dissertation. Hebei University
Xie L, He X, Wang K, Hou L, Sun Q (2017) Spatial dynamics of dark septate endophytes in the roots and rhizospheres of Hedysarum scoparium in Northwest China and the influence of edaphic variables. Fungal Ecol 26:135–143. https://doi.org/10.1016/j.funeco.2017.01.007
Xie W, Hao Z, Zhou X, Jiang X, Xu L, Wu S, Zhao A, Zhang X, Chen B (2018) Arbuscular mycorrhiza facilitates the accumulation of glycyrrhizin and liquiritin in Glycyrrhiza uralensis under drought stress. Mycorrhiza 28:285–300. https://doi.org/10.1007/s00572-018-0827-y
Zhan F, He Y, Zu Y, Li T, Zhao Z (2011) Characterization of melanin isolated from a dark septate endophyte (DSE), Exophiala pisciphila. World J Microbiol Biotechnol 27:2483–2489. https://doi.org/10.1007/s11274-011-0712-8
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. https://doi.org/10.1007/s12275-008-0163-6
Zhang H, Tang M, Chen H, Wang Y, Ban Y (2010) Arbuscular mycorrhizas and dark septate endophytes colonization status in medicinal plant Lycium barbarum L. in arid northwestern China. Afr J Microbiol Res 4:1914–1920
Zhang H, Tang M, Chen H, Wang Y (2012) Effects of a dark-septate endophytic isolate LBF-2 on the medicinal plant Lycium barbarum L. J Microbiol 50:91–96. https://doi.org/10.1007/s12275-012-1159-9
Zhang QM, Gong MG, Yuan JF, Hou Y, Zhang HM, Wang Y, Hou X (2017) Dark septate endophyte improves drought tolerance in Sorghum. Int J Agric Biol 19:53–60. https://doi.org/10.17957/ijab/15.0241
Zhu ZB, Fan JY, Guo QS, Liu ZY, Zhu GS (2015) The growth and medicinal quality of Epimedium wushanense are improved by an isolate of dark septate fungus. Pharm Biol 53:1344–1351. https://doi.org/10.3109/13880209.2014.982296
Acknowledgements
This study was financially supported by the National Natural Science Foundation of China (project no. 31470533, 31770561, 31800345). We greatly appreciate the support of Experimental Center of Desert Forestry, CAF for their invaluable assistance on this experiment.
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Li, X., He, C., He, X. et al. Dark septate endophytes improve the growth of host and non-host plants under drought stress through altered root development. Plant Soil 439, 259–272 (2019). https://doi.org/10.1007/s11104-019-04057-2
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DOI: https://doi.org/10.1007/s11104-019-04057-2