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A foliar Epichloë endophyte and soil moisture modified belowground arbuscular mycorrhizal fungal biodiversity associated with Achnatherum inebrians

  • Rui Zhong
  • Chao Xia
  • Yawen Ju
  • Xingxu ZhangEmail author
  • Tingyu Duan
  • Zhibiao NanEmail author
  • Chunjie Li
Regular Article
  • 72 Downloads

Abstract

Background and aims

Fungal symbionts, present in above and in belowground tissues, such as that of Epichloë endophytes and arbuscular mycorrhizal (AM) fungi, respectively, can modify the responses of host plants to environmental changes. Individual grass plants of the subfamily Pooideae can be host to both a foliar Epichloë endophytic fungus and root-associated AM fungi. Understanding the multiple interactions among above- and belowground symbionts and their host is an important step in understanding terrestrial ecosystems.

Methods

A field experiment was conducted to study the effects of E. gansusensis endophyte and soil moisture on the belowground AM fungal biodiversity associated with Achnatherum inebrians, through amplicon sequencing technology. Soil properties were compared among stands using standard techniques.

Results

Our results show that E. gansusensis increased root-associated AM fungal diversity under drought conditions, while decreasing diversity under the water addition treatment. Water addition and water stress treatments decreased the diversity and richness of the AM fungal community in rhizosphere soil compared to the normal treatment. The E. gansusensis altered the composition of the root-associated AM fungal community. Aboveground biomass was closely positively related to the abundance of Funneliformis in the root and the diversity of the rhizosphere soil AM fungal community was positively related to the soil total nitrogen and phosphorus.

Conclusion

This study suggested that soil moisture regimes shifted the effects of E. gansuensis on the diversity of the root-associated AM fungal community from positive to negative; moreover, soil moisture and foliar E. gansusensis altered soil properties, thereby affecting belowground AM fungi.

Keywords

Foliar Epichloë endophyte Root-associated Rhizosphere soil AM fungi Soil moisture Biodiversity Achnatherum inebrians 

Notes

Acknowledgements

We wish to thank the editor and anonymous reviewers for their valuable comments, Michael Christensen retired from AgResearch, Grasslands Research Centre, New Zealand, for polishing the English and his beneficial suggestions. This work was financially supported by the National Nature Science Foundation of China (31772665), Program for Changjiang Scholars and Innovative Research Team in University of China (IRT17R50), and the Open Foundation of Research Institute of Qilian Mountains (504000-87080305), Lanzhou University.

Supplementary material

11104_2019_4365_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1565 kb)

References

  1. Almeida-Rodríguez AM, Gómes MP, Loubert-Hudon A, Joly S, Labrecque M (2015) Symbiotic association between Salix purpurea L. and Rhizophagus irregularis: modulation of plant responses under copper stress. Tree Physiol 36:407–420PubMedCrossRefPubMedCentralGoogle Scholar
  2. 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 22:912–918CrossRefGoogle Scholar
  3. Arrieta A, Iannone L, Scervino J, Vignale M, Novas M (2015) A foliar endophyte increases the diversity of phosphorus-solubilizing rhizospheric fungi and mycorrhizal colonization in the wild grass Bromus auleticus. Fungal Ecol 17:146–154CrossRefGoogle Scholar
  4. Becker M, Becker Y, Green K, Scott B (2016) The endophytic symbiont Epichloë festucae establishes an epiphyllous net on the surface of Lolium perenne leaves by development of an expressorium, an appressoriumdophytic syexit structure. New Phytol 211:240–254PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bell-Dereske L, Takacs-Vesbach C, Kivlin SN, Emery SM, Rudgers JA (2017) Leaf endophytic fungus interacts with precipitation to alter belowground microbial communities in primary successional dunes. FEMS Microbiol Ecol 93:fix036PubMedCentralCrossRefGoogle Scholar
  6. Bhadalung NN, Rungchuang J (2005) Effects of long-term NP-fertilization on abundance and diversity of arbuscular mycorrhizal fungi under a maize cropping system. Plant Soil 270:371–382CrossRefGoogle Scholar
  7. Borriello R, Lumini E, Girlanda M, Bonfante P, Bianciotto V (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48:911–922CrossRefGoogle Scholar
  8. Buyer JS, Zuberer DA, Nichols KA, Franzluebbers AJ (2011) Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant Soil 339:401–412CrossRefGoogle Scholar
  9. Chen YL, Zhang X, Ye JS, Han HY, Wan SQ, Chen BD (2014) Six-year fertilization modifies the biodiversity of arbuscular mycorrhizal fungi in a temperate steppe in inner Mongolia. Soil Biol Biochem 69:371–381CrossRefGoogle Scholar
  10. Chen L, Li XZ, Li CJ, Swoboda GA, Young CA, Sugawara K, Leuchtmann A, Schardl CL (2015a) Two distinct Epichloë species symbiotic with Achnatherum inebrians, drunken horse grass. Mycologia 107:863–873PubMedCrossRefGoogle Scholar
  11. Chen D, Mi J, Chu PF, Cheng JH, Zhang LX, Pan QM, Xie YC, Bai YF (2015b) Patterns and drivers of soil microbial communities along a precipitation gradient on the Mongolian plateau. Landsc Ecol 30:1669–1682CrossRefGoogle Scholar
  12. Chen C, Zhang JN, Lu M, Qin C, Chen YH, Li Y, Huang QW, Wang JC, Shen ZG, Shen QR (2016a) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fertil Soils 52:1–13CrossRefGoogle Scholar
  13. Chen N, He RL, Chai Q, Li CJ, Nan ZB (2016b) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80:367–375CrossRefGoogle Scholar
  14. Chen ML, Yang G, Ye S, Li PY, Qiu HY, Zhou XT, Huang LQ, Cao Z (2017) Glomus mosseae inoculation improves the root system architecture, photosynthetic efficiency and flavonoids accumulation of liquorice under nutrient stress. Front Plant Sci 8:931PubMedPubMedCentralCrossRefGoogle Scholar
  15. Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolarrd J, Nickless E, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongation grass leaves. Fungal Genet Biol 45:84–93PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chu-Chou 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 24:633–637CrossRefGoogle Scholar
  17. Clark JS, Campbell JH, Grizzle H, Acostamartìnez V, Zak JC (2009) Soil microbial community response to drought and precipitation variability in the Chihuahuan Desert. Microb Ecol 57:248–260PubMedCrossRefPubMedCentralGoogle Scholar
  18. Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier Ü, Saks Ü, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973PubMedCrossRefPubMedCentralGoogle Scholar
  19. Deepika S, Kothamasi D (2015) Soil moisture-a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25:67–75PubMedCrossRefPubMedCentralGoogle Scholar
  20. Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804PubMedCrossRefGoogle Scholar
  21. Erica L, Alberto O, Roberto B, Paola B, Valeria B (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179Google Scholar
  22. Franzluebbers AJ, Hill NS (2005) Soil carbon, nitrogen, and ergot alkaloids with short- and long-term exposure to endophyte-infected and endophyte-free tall fescue. Soil Sci Soc Am J 69:404–412CrossRefGoogle Scholar
  23. Gai JP, Tian H, Yang FY, Christie P, Li XL, Klironomos JN (2012) Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia 55:145–151CrossRefGoogle Scholar
  24. Grümberg BC, Urcelay C, Shroeder MA, Vargas-Gil S, Luna SM (2015) The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol Fertil Soils 51:1–10CrossRefGoogle Scholar
  25. Guo JQ, McCulley RL, McNear DH (2015) Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition. Front Plant Sci 6:183PubMedPubMedCentralGoogle Scholar
  26. Guo JQ, McCulley RL, Phillips TD, McNear DH (2016) Fungal endophyte and tall fescue cultivar interact to differentially affect bulk and rhizosphere soil processes governing C and N cycling. Soil Biol Biochem 101:165–174CrossRefGoogle Scholar
  27. Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508PubMedCrossRefGoogle Scholar
  28. Helmke PA, Sparks DL (1996) Lithium, sodium, potassium, rubidium and cesium. In: Sparks DL (Ed) Methods of soil analysis part 3: chemical methods. Soil Sci Soc Am J 551–574Google Scholar
  29. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT (2011) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407CrossRefGoogle Scholar
  30. Hosseini F, Mosaddeghi MR, Hajabbasi MA, Sabzalian MR (2016) Role of fungal endophyte of tall fescue (Epichloë coenophiala) on water availability, wilting point and integral energy in texturally-different soils. Agric Water Manag 163:197–211CrossRefGoogle Scholar
  31. Iqbal J, Siegrist JA, Nelson JA, McCulley RL (2012) Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biol Biochem 44:81–92CrossRefGoogle Scholar
  32. Johnson LJ, Briggs LR, Caradus JR, Finch SC, Fleetwood DJ, Fletcher LR, Hume DE, Johnson RD, Popay AJ, Tapper BA (2013) The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers 60(1):171–188CrossRefGoogle Scholar
  33. Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121(12):2090–2096CrossRefGoogle Scholar
  34. Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105CrossRefGoogle Scholar
  35. Li CJ, Nan ZB, Paul VH, Dapprich PD, Liu Y (2004) A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon 90:141–147Google Scholar
  36. Li XL, Gai JP, Cai XB, Li XL, Christie P, Zhang FS, Zhang JL (2014) Molecular diversity of arbuscular mycorrhizal fungi associated with two co-occurring perennial plant species on a Tibetan altitudinal gradient. Mycorrhiza 24:95–107PubMedCrossRefPubMedCentralGoogle Scholar
  37. Li LF, Li T, Zhang Y, Zhao ZW (2010) Molecular diversity of arbuscular mycorrhizal fungi and their distribution patterns related to host-plants and habitats in a hot and arid ecosystem, southwest China. FEMS Microbiol Ecol 71:418-427PubMedCrossRefPubMedCentralGoogle Scholar
  38. Li XL, Zhu TY, Peng F, Chen Q, Lin S, Christle P, Zhang JL (2015) Inner Mongolian steppe arbuscular mycorrhizal fungal communities respond more strongly to water availability than to nitrogen fertilization. Environ Microbiol 17:3051–3068PubMedCrossRefPubMedCentralGoogle Scholar
  39. Li NN, Zhao YF, Xia C, Zhong R, Zhang XX (2016) Effects of thiophanate methyl on seed borne Epichloë fungal endophyte of Achnatherum inebrians. Pratacultural Sci 33(7):1306–1314 (in Chinese with English abstract)Google Scholar
  40. Liang Y, Wang HC, Li CJ, Nan Z, Li FD (2017) Effects of feeding drunken horse grass infected with Epichloë gansuensis endophyte on animal performance, clinical symptoms and physiological parameters in sheep. BMC Vet Res 13(1):223PubMedPubMedCentralCrossRefGoogle Scholar
  41. Lin XG, Feng YZ, Zhang HY, Chen RR, Wang JH, Zhang JB, Chu HY (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771PubMedCrossRefPubMedCentralGoogle Scholar
  42. Liu QH, Parsons AJ, Xue H, Fraser K, Ryan D, 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 25:910–920CrossRefGoogle Scholar
  43. Liu YJ, Shi GX, Mao L, Cheng G, Jiang SJ, Ma XJ, An LZ, Du GZ, Collins JN, Feng HY (2012) Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523–535PubMedCrossRefPubMedCentralGoogle Scholar
  44. Liu YJ, Mao L, Li JY, Shi GX, Jiang SJ, Ma XJ, An LZ, Du GZ, Feng HY (2015) Resource availability differentially drives community assemblages of plants and their root-associated arbuscular mycorrhizal fungi. Plant Soil 386:341–355CrossRefGoogle Scholar
  45. Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320CrossRefGoogle Scholar
  46. Malik RJ, Dixon MH, Bever JD (2016) Mycorrhizal composition can predict foliar pathogen colonization in soybean. Biol Control 103:46–53CrossRefGoogle Scholar
  47. Mirshad PP, Puthur JT (2016) Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum retz.). Environ Monit Assess 188:425PubMedCrossRefPubMedCentralGoogle Scholar
  48. Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL (2013) Tall fescue endophyte effects on tolerance to water deficit stress. BMC Plant Biol 13:127PubMedPubMedCentralCrossRefGoogle Scholar
  49. Naylor D, Degraaf S, Purdom E, Coleman-Derr D (2017) Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J 11:2691–2704PubMedPubMedCentralCrossRefGoogle Scholar
  50. Nelson DV, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Sparks DL (Ed) Methods of soil analysis part 2: chemical and microbiological properties. Soil Sci Soc Am J 961–1010Google Scholar
  51. 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 55:19–28CrossRefGoogle Scholar
  52. Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin P, Simpson G, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. J Stat Soft 48:1–21Google Scholar
  53. Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232CrossRefGoogle Scholar
  54. Patchett B, Chapman R, Fletcher L, Gooneratne S (2008) Root loline concentration in endophyte infected meadow fescue (Festuca pratensis) is increased by grass grub (Costelytra zealandica) attack. N Z Plant Prot 61:210–214Google Scholar
  55. Pellegrino E, Öpik M, Bonari E, Ercoli L (2015) Responses of wheat to arbuscular mycorrhizal fungi: a meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217CrossRefGoogle Scholar
  56. Robertson G, Coleman D, Bledsoe C, Sollins P (1999) Standard soil methods for long-term ecological research. Oxford University Press, New YorkGoogle Scholar
  57. Rojas X, Guo JQ, Leff JW, McNear DH, Fierer N, McCulley RL (2016) Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microb Ecol 72:197–206PubMedCrossRefGoogle Scholar
  58. Rostas M, Cripps MG, Silcock P (2015) Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 177:487–497PubMedCrossRefGoogle Scholar
  59. Santos-Medellín C, Edwards J, Liechty Z, Bao N, Sundaresan V (2017) Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8:e00764–e0071717PubMedPubMedCentralCrossRefGoogle Scholar
  60. Schardl CL, Leuchtmann A, Spiering MJ (2005) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340CrossRefGoogle Scholar
  61. Schloss D, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedPubMedCentralCrossRefGoogle Scholar
  62. Schmidt PA, Schmitt I, Otte J, Bandow C, Römbke J, Bálint M, Rolshausen G (2017) Season-long experimental drought alters fungal community composition but not diversity in a grassland soil. Microb Ecol 75:1–11Google Scholar
  63. Shi ZC (1997) Important poisonous plants of China grassland. China Agriculture Press, BeijingGoogle Scholar
  64. Sikes B, Cottenie K, Klironomos J (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280CrossRefGoogle Scholar
  65. Slaughter LC, McCulley RL (2016) Aboveground Epichloë coenophiala–grass associations do not affect belowground fungal symbionts or associated plant, soil parameters. Microb Ecol 72:682–691PubMedCrossRefGoogle Scholar
  66. Slaughter LC, Nelson JA, Carlisle E, Bourguignon M, Dinkins RD, Phillips TD, McCulley RL (2018) Climate change and Epichloë coenophiala association modify belowground fungal symbioses of tall fescue host. Fungal Ecol 31:37–46CrossRefGoogle Scholar
  67. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press, New YorkGoogle Scholar
  68. Soto-Barajas MC, Zabalgogeazcoa I, Gómez-Fuertes J, González-Blanco V, Vázquez-De-Aldana BR (2016) Epichloë endophytes affect the nutrient and fiber content of Lolium perenne, regardless of plant genotype. Plant Soil 405:65–277CrossRefGoogle Scholar
  69. Souza T (2015) Handbook of Arbuscular Mycorrhizal Fungi. Springer International PublishingGoogle Scholar
  70. Sun XF, Su YY, Zhang Y, Wu MY, Zhang Z, Pei KQ, Sun LF, Wan SQ, Liang Y (2013) Diversity of arbuscular mycorrhizal fungal spore communities and its relations to plants under increased temperature and precipitation in a natural grassland. Chin Sci Bull 58:4109–4119CrossRefGoogle Scholar
  71. Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch P, Põldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pärtel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson K-H, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo L-d, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, De Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346(6213):1256688PubMedPubMedCentralCrossRefGoogle Scholar
  72. Turrini A, Sbrana C, Avio L, Njeru EM, Bocci G, Bàrberi P, Giovannetti M (2016) Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession. Biol Fertil Soils 52:643–653CrossRefGoogle Scholar
  73. Vandegrift R, Roy BA, Pfeifer-Meister L, Johnson BR, Bridgham SD (2015) The herbaceous landlord: integrating the effects of symbiont consortia within a single host. PeerJ 3:e1379PubMedPubMedCentralCrossRefGoogle Scholar
  74. van Aarle IMV, Olsson PA, Söderström B (2002) Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol 155:173–182CrossRefGoogle Scholar
  75. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998a) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  76. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998b) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091CrossRefGoogle Scholar
  77. van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423PubMedCrossRefGoogle Scholar
  78. van Geel M, Busschaert P, Honnay O, Lievens B (2014) Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106:93–100PubMedCrossRefPubMedCentralGoogle Scholar
  79. van Geel M, Beenhouwer MD, Ceulemans T, Caes K (2016) Application of slow-release phosphorus fertilizers increases arbuscular mycorrhizal fungal diversity in the roots of apple trees. Plant Soil 402:291–301CrossRefGoogle Scholar
  80. van Hecke MM, Treonis AM, Kaufman JR (2005) How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Festuca arundinacea) rhizodeposition and soil microorganisms? Plant Soil 275:101–109CrossRefGoogle Scholar
  81. Verbruggen E, van Heijden MGA, Weedon JT, Kowalchuk GA, Röling WF (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21:2341–2235PubMedCrossRefPubMedCentralGoogle Scholar
  82. Vignale MV, Iannone LJ, Scervino JM, Novas MV (2018) Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil 422:267–281CrossRefGoogle Scholar
  83. Wang JF, Tian P, Christensen M, Zhang XX, Li CJ, Nan ZB (2018) Effect of Epichloë gansuensis endophyte on the activity of enzymes of nitrogen metabolism, nitrogen use efficiency and photosynthetic ability of Achnatherum inebrians under various NaCl concentrations. Plant Soil 422:267–281CrossRefGoogle Scholar
  84. Xia C, Zhang XX, Christensen MJ, Nan ZB, Li CJ (2015) Epichloë endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunken horse grass (Achnatherum inebrians). Fungal Ecol 16:26–34CrossRefGoogle Scholar
  85. Xia C, Li NN, Zhang XX, Feng Y, Christensen MJ, Nan ZB (2016) An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol 22:26–33CrossRefGoogle Scholar
  86. Xia C, Christensen MJ, Zhang XX, Nan ZB (2018) Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant Soil 424:555–571CrossRefGoogle Scholar
  87. Xu L, Naylor D, Dong ZB, Simmons T, Pierroz G, Hixson KK, Kim YM, Zink EM, Engbrecht KM, Wang Y, Gao C, De Graaf S, Madera MA, Sievert JA, Hollingsworth J, Birdseye D, Scheller HV, Hutmacher R, Dahlberg J, Jansson C, Taylor JW, Lemaux PG, Coleman-Derr D (2018) Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci USA 115:4284–4293CrossRefGoogle Scholar
  88. Zhang XX, Li CJ, Nan ZB (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175(1):703–709PubMedCrossRefPubMedCentralGoogle Scholar
  89. Zhang XX, Li CJ, Nan ZB, Matthew C (2012) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Res 52:70–78CrossRefGoogle Scholar
  90. Zhang XM, Wei HW, Chen QS, Han XG (2014) The counteractive effects of nitrogen addition and watering on soil bacterial communities in a steppe ecosystem. Soil Biol Biochem 72:26–34CrossRefGoogle Scholar
  91. Zhao J, Zhang R, Xue C, Xun WB, Sun L, Xu YC, Shen QR (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443–453PubMedCrossRefGoogle Scholar
  92. Zhong R, Zhou XR, Zhang ZQ, Xia C, Li NN, Zhang XX (2017) Effect of Epichloë gansuensis on arbuscular mycorrhizal fungi spore diversity in rhizosphere soil of drunken horse grass under different growth conditions. Pratacultural Sci 34:1627–1634 (in Chinese with English abstract)Google Scholar
  93. Zhong R, Xia C, Ju YW, Li NN, Zhang XX, Nan ZB, Christensen MJ (2018) Effects of Epichloë gansuensis on root-associated fungal communities of Achnatherum inebrians under different growth conditions. Fungal Ecol 31:29–36CrossRefGoogle Scholar
  94. Zhou Y, Li X, Qin JH, Liu H, Chen W, Niu Y, Ren AZ, Gao YB (2016) Effects of simultaneous infections of endophytic fungi and arbuscular mycorrhizal fungi on the growth of their shared host grass Achnatherum sibiricum under varying N and P supply. Fungal Ecol 20:56–65CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.State key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Center for Grassland Microbiome, College of Pastoral Agricultural Science and TechnologyLanzhou UniversityLanzhouPeople’s Republic of China

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