Abstract
Leaf spot of perennial ryegrass (Lolium perenne) caused by Bipolaris sorokiniana is an important disease in temperate regions of the world. We designed this experiment to test for the combined effects of the arbuscular mycorrhizal (AM) fungus Claroideoglomus etunicatum and the grass endophyte fungus Epichloë festucae var. lolii on growth and disease occurrence in perennial ryegrass. The results show that C. etunicatum increased plant P uptake and total dry weight and that this beneficial effect was slightly enhanced when in association with the grass endophyte. The presence in plants of both the endophyte and B. sorokiniana decreased AM fungal colonization. Plants inoculated with B. sorokiniana showed the typical leaf spot symptoms 2 weeks after inoculation and the lowest disease incidence was with plants that were host to both C. etunicatum and E. festucae var. lolii. Plants with these two fungi had much higher activity of peroxidases (POD), superoxide dismutase (SOD) and catalase (CAT) and lower values of malondialdehyde (MDA) and hydrogen peroxide (H2O2). The AM fungus C. etunicatum and the grass endophyte fungus E. festucae var. lolii have the potential to promote perennial ryegrass growth and resistance to B. sorokiniana leaf spot.
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References
Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol 22(5):912–918. https://doi.org/10.1111/j.1365-2435.2008.01432.x
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180(2):501–510. https://doi.org/10.1111/j.1469-8137.2008.02583.x
Barker GM (1987) Mycorrhizal infection influences Acremonium-induced resistance to argentine stem weevil inryegrass. In: New Zealand weed and pest control Conference, Wellington, pp 199–203
Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140
Bolwell GP, Daudi A (2009) Reactive oxygen species in plant pathogen interactions. In: Reactive oxygen species in plant signaling. Springer Berlin, Heidelberg, pp 113–133. https://doi.org/10.1007/978-3-642-00390-5_7
Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal genet bio l45:84-93
Chu-Chao M, Guo B, An ZQ, Hendrix JW, Ferriss RS, Siegel MR, Dougherty CT, Burrus PB (1992) Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol Biochem 24(7):633–637. https://doi.org/10.1016/0038-0717(92)90041-U
Chung KR, Schardl LC (1997) Sexual cycle and horizontal transmission of the grass symbiont, Epichloë typhina. Mycol Res 101(3):295–301. https://doi.org/10.1017/S0953756296002602
Duan TY, Facelli E, Smith SE, Smith FA, Nan ZB (2011) Differential effects of soil disturbance and plant residue retention on function of arbuscular mycorrhizal (AM) symbiosis are not reflected in colonization of roots or hyphal development in soil. Soil Biol Biochem 43(3):571–578. https://doi.org/10.1016/j.soilbio.2010.11.024
Elsharkawy MM, Shimizu M, Takahashi H, Hyakumachi M (2012) The plant growth-promoting fungus Fusarium equiseti, and the arbuscular mycorrhizal fungus Glomus mosseae, induce systemic resistance against cucumber mosaic virus in cucumber plants. Plant Soil 361(1-2):397–409. https://doi.org/10.1007/s11104-012-1255-y
Facelli E, Duan T, Smith SE, Christophersen HM, Facelli JM, Smith FA (2014) Opening the black box: outcomes of interactions between arbuscular mycorrhizal (AM) and non-host genotypes of Medicago depend on fungal identity, interplay between P uptake pathways and external P supply. Plant Cell Environ 37(6):1382–1392. https://doi.org/10.1111/pce.12237
Florea S, Schardl CL, Hollin W (2015) Detection and isolation of Epichloë species, fungal endophytes of grasses. Curr Protoc Microbiol 38:19A.1.1–19A.1.24
Gallagher RT, Hawkes AD, Steyn PS, Vleggaar R (1984) Tremorgenic neurotoxins from perennial ryegrass causing ryegrass staggers disorder of livestock: structure elucidation of lolitrem B. J Chem Soc Chem Commun 9:614–616
Gavito ME, Bruhn D, Jakobsen I (2002) Phosphorus uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment. New Phytol 154(3):751–760. https://doi.org/10.1046/j.1469-8137.2002.00404.x
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Gu YX, Wang DJ, Hu YG (2007) The effect of endophytic fungus on curvularia lunate in Festuca arundinacea. Chin J Grassl 29:112–115
Hanson WC (1950) The photometric determination of phosphorus in fertilizers using the phosphovanado-molybdate complex. J Sci Food Agric 1(6):172–173. https://doi.org/10.1002/jsfa.2740010604
Johnson LJ, Bonth ACMD, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA, Simpson WR, Voisey CR, Card SD (2013) The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers 60(1):171–188. https://doi.org/10.1007/s13225-013-0239-4
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecol 84(9):2292–2301. https://doi.org/10.1890/02-0413
Kumar KB, Khan P (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine corocana) leaves during senescence. Indian J Expe Biol 20:412–416
Larimer AL, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121(12):2090–2096. https://doi.org/10.1111/j.1600-0706.2012.20153.x
Lee BR, Muneer S, Jung WJ, Aviced JC, Ourryd A, Kim TH (2012) Mycorrhizal colonization alleviates drought- induced oxidative damage and lignification in the leaves of drought-stressed perennial ryegrass (Lolium perenne). Physiol Plant 145(3):440–449. https://doi.org/10.1111/j.1399-3054.2012.01586.x
Lenoir I, Fontaine J, Tisserant B, Laruelle F, Lounèshadj SA (2017) Beneficial contribution of the arbuscular mycorrhizal fungus, Rhizophagus irregularis, in the protection of Medicago truncatula roots against benzo[a]pyrene toxicity. Mycorrhiza 27(5):465–476. https://doi.org/10.1007/s00572-017-0764-1
Li HS, Sun Q, Zhao SJ, Zhang WH (2000) Principle and techniques of botanic, chemical and physiological experiments, 1st edn. Senior Education Press, Beijing
Li CJ, Nan ZB, Paul VH, Liu Y (2004) A new Neotyphodiums pecies symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon 90:141–147
Li HY, Smith FA, Dickson S, Holloway RE, Smith SE (2008) Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain? New Phytol 178(4):852–862. https://doi.org/10.1111/j.1469-8137.2008.02410.x
Liu Q, Parsons AJ, Xue H, Fraser K, Ryan GD, Newman JA, Rasmussen S (2011) Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Funct Ecol 25(4):910–920. https://doi.org/10.1111/j.1365-2435.2011.01853.x
López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61(10):2589–2601. https://doi.org/10.1093/jxb/erq089
Ma MZ, Nan ZB (2011) Effect of fungal endophytes against rust disease of perennial ryegrass (Lolium perenne) on growth and physiological indices. Acta Pratacult Sin 20:150–156
Ma MZ, Christensen MJ, Nan ZB (2015) Effects of the endophyte Epichloë festucae var. lolii of perennial ryegrass (Lolium perenne) on indicators of oxidative stress from pathogenic fungi during seed germination and seedling growth. Eur J Plant Pathol 141(3):571–583. https://doi.org/10.1007/s10658-014-0563-x
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159(1):89–102. https://doi.org/10.1007/BF00000098
Martínez-Medina A, Pascual JA, Lloret E, Roldán A (2009) Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum, and their effects on Fusarium wilt in melon plants grown in seedling nurseries. J Sci Food Agr 89(11):1843–1850. https://doi.org/10.1002/jsfa.3660
Maya MA, Matsubara Y (2013) Tolerance to Fusarium wilt and anthracnose diseases and changes of antioxidative activity in mycorrhizal cyclamen. Crop Prot 47:41–48. https://doi.org/10.1016/j.cropro.2013.01.007
McLaughlin MJ, Lancaster PA, Sale PG, Uren NC, Peverill KI (1994) Comparison of cation/anion exchange resin methods for multi-element testing of acidic soils. Soil Res 32(2):229–240. https://doi.org/10.1071/SR9940229
Müller J (2003) Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct Plant Biol 30(4):419–424. https://doi.org/10.1071/FP02189
Nan ZB (1995) Fungicide seed treatments of sainfoil control seed-borne and root-invading fungi. New Zeal J Agr Res 38(3):413–420. https://doi.org/10.1080/00288233.1995.9513144
Novas MV, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30
Novas MV, Iannone LJ, Godeas AM, Scervino JM (2011) Evidence for leaf endophyte regulation of root symbionts: effect of Neotyphodium, endophytes on the pre-infective state of mycorrhizal fungi. Symbiosis 55(1):19–28. https://doi.org/10.1007/s13199-011-0140-4
Omacini M, Eggers T, Bonkowski M, Gang AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20(2):226–232. https://doi.org/10.1111/j.1365-2435.2006.01099.x
Parsaeian M, Mirlouhi AF, Almajid RA, Baradaran M (2006) The morphological changes affected by endophytes on induction of cold tolerance in two species of festuca. Iranian J Crop Sci. 8:139–152
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T British Mycol Soc 55(1):158–IN118. https://doi.org/10.1016/S0007-1536(70)80110-3
Pineda A, Zheng SJ, van Loon JJ, Pieterse CM, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15(9):507–514. https://doi.org/10.1016/j.tplants.2010.05.007
Popay AJ, Hume DE (2011) Endophytes improve ryegrass persistence by controlling insects. Pasture Persistence-Grassl Res PractSer 15:149–156
Sabzalian MR, Mirlohi A, Sharifnabi B (2012). Reaction to powdery mildew fungus, Blumeria graminis, in Endophyte-infected and endophyte-free tall and meadow fescues. Australas plant path 41:565–572
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(1):28–40. https://doi.org/10.1111/j.1744-7348.2011.00471.x
Schroeder MS, Janos DP (2005) Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15(3):203–216. https://doi.org/10.1007/s00572-004-0324-3
Smith SE, Read DJ (1996) Mycorrhizal symbiosis, 3rd edn. Academic, London
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046. https://doi.org/10.3852/16-042
Strickland JR, Bailey EM, Abney LK, Oliver JW (1996) Assessment of the mitogenic potential of the alkaloids produced by endophyte (Acremonium coenophialum)-infected tall fescue (Festuca arundinacea) on bovine vascular smooth muscle in vitro. J Anim Sci 74(7):1664–1671. https://doi.org/10.2527/1996.7471664x
Tapper BA, Latch GCM (1999) Selection against toxin production in endophyte-infected perennial ryegrass. Grassl Res Pract. Ser 7:107–111
Tian P, Nan ZB, Li CJ German(2008) Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur J Plant Pathol 122(4):593–602. https://doi.org/10.1007/s10658-008-9329-7
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Vicari M, Hatcher PE, Ayres PG (2002) Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecol 83(9):2452–2464. https://doi.org/10.1890/0012-9658(2002)083[2452:CEOFAM]2.0.CO;2
Wang JT, Zhao EZ (2014) The grass planting situation in 2013 in China. China Anim Ind 24:33–34
Wang XY, Zhou Y, Ren AZ, Gao YB (2014) Effect of endophyte infection on fungal disease resistance of Leymus chinensis. Acta Ecol Sin 34:6789–6796
West CP, Izekor E, Turner KE, Elmi AA (1993) Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agron J 85(2):264–270. https://doi.org/10.2134/agronj1993.00021962008500020019x
Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82(8):1198–1227. https://doi.org/10.1139/b04-082
XL W, XP G, MY S, Yue JJ (2008) Study on contents of cellulose, lignin and activities of POD, PAL in excised bamboo shoots of phyllostachysedulis. Forest Res 21:697–701
Zaefarian F, Rezvani M, Ardakani MR, Rejali F, Miransari M (2013) Impact of mycorrhizae formation on the phosphorus and heavy metal uptake of alfalfa. Commun Soil Sci Plan 44(8):1340–1352. https://doi.org/10.1080/00103624.2012.756505
Zambolim L, Schenck NC (1983) Reduction of the effects of pathogenic, root-infecting fungi on soybean by the mycorrhizal fungus, Glomus mosseae. Phytopathology 73(10):1402–1405. https://doi.org/10.1094/Phyto-73-1402
Zhang GL, Dai QG, Zhang HC, Ling L, Diao SY (2006) Influences of silicon and inoculation with Rhizoctonia solanion membrane lipid peroxidation and defense enzyme activities in rice leaves. J Yangzhou Univ 27:49–53
Zhang XX, Li CJ, Nan ZB (2009) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709
Zhang W, Card SD, Mace WJ, Christensen MJ, Mcgill CR, Matthew C (2017) Defining the pathways of symbiotic Epichloë colonization in grass embryos with confocal microscopy. Mycologia 109(1):153–161. https://doi.org/10.1080/00275514.2016.1277469
Zheng Y, Liu YH, Ge JY, Wang XY, Liu LJ, ZB B, Liu P (2010) Resveratrol protects human lens epithelial cells against H2O2 induced oxidative stress by increasing catalase, SOD-1, and HO-1 expression. Mol Vis 16:1467–1474
Zhu YG, Laidlaw AS, Christie P, Hammond MER (2000) The specificity of arbuscular mycorrhizal fungi in perennial ryegrass-white clover pasture. Agric Ecosyst Environ 77(3):211–218. https://doi.org/10.1016/S0167-8809(99)00087-0
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This research was financially supported by the National Natural Science Foundation of China (31100368), China Agriculture Research System (CARS-22 Green manure), and the National Basic Research Program of China (973) (2014CB138702).
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Supplementary Fig S1
Shoot height of perennial ryegrass with (E+) and without (E−) grass endophyte and colonized by Claroideoglomus etunicatum (AM) or non-mycorrhizal (NM) before Bipolaris sorokiniana inoculation. Mean ± SEM of four replicates. Markers adjacent to the same lowercase letter do not differ significantly at the same day between treatments at P ≤ 0.05 by Tukey’s HSD (DOCX 60 kb)
Supplementary Fig S2
Root/shoot ratio of perennial ryegrass with (E+) and without (E−) grass endophyte and colonized by Claroideoglomus etunicatum (stippled bars) or non-mycorrhizal (open bars) at harvest. Mean ± SEM of four replicates. B = Bipolaris sorokiniana applied, NB = no B. sorokiniana. Bars topped by the same lowercase letter do not differ significantly between treatments at P ≤ 0.05 by Tukey’s HSD. See Table 1 for ANOVA results (DOCX 48 kb)
Supplementary Fig S3
Shoot dry weight (a), root dry weight (b), and root length (c) of perennial ryegrass with (E+) and without (E−) grass endophyte and colonized by Claroideoglomus etunicatum (stippled bars) or non-mycorrhizal (open bars) at harvest. Mean ± SEM of four replicates. B = Bipolaris sorokiniana applied, NB = no B. sorokiniana. Bars topped by the same lower case letter do not differ significantly between treatments at P ≤ 0.05 by Tukey’s HSD. See Table 1 for ANOVA results (DOCX 152 kb)
Supplementary Fig S4
Root P concentration of perennial ryegrass with (E+) and without (E−) grass endophyte and colonized by Claroideoglomus etunicatum (stippled bars) or non-mycorrhizal (open bars) at harvest. Mean ± SEM of four replicates. B = Bipolaris sorokiniana applied, NB = no B. sorokiniana. Bars topped by the same lowercase letter do not differ significantly between treatments at P ≤ 0.05 by Tukey’s HSD. See Table 1 for ANOVA results (DOCX 47 kb)
Supplementary Fig S5
Superoxide dismutase (SOD) (a), catalase (CAT) (b), and polyphenol oxidase (PPO) (c) enzyme activity of perennial ryegrass with (E+) and without (E−) grass endophyte and colonized by Claroideoglomus etunicatum (stippled bars) or non-mycorrhizal (open bars) at harvest. Mean ± SEM of four replicates. B = Bipolaris sorokiniana applied, NB = no B. sorokiniana. Bars topped by the same lowercase letter do not differ significantly between treatments at P ≤ 0.05 by Tukey’s HSD. See Table 1 for ANOVA results (DOCX 128 kb)
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Li, F., Guo, Y., Christensen, M.J. et al. An arbuscular mycorrhizal fungus and Epichloë festucae var. lolii reduce Bipolaris sorokiniana disease incidence and improve perennial ryegrass growth. Mycorrhiza 28, 159–169 (2018). https://doi.org/10.1007/s00572-017-0813-9
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DOI: https://doi.org/10.1007/s00572-017-0813-9