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Tripartite Interactions Between Endophytic Fungi, Arbuscular Mycorrhizal Fungi, and Leymus chinensis

  • Plant Microbe Interactions
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Abstract

Grasses often establish multiple simultaneous symbiotic associations with endophytic fungi and arbuscular mycorrhizal fungi (AMF). Many studies have examined pair-wise interactions between plants and endophytic fungi or between plants and AMF, overlooking the interplays among multiple endosymbionts and their combined impacts on hosts. Here, we examined both the way in which each symbiont affects the other symbionts and the tripartite interactions between leaf endophytic fungi, AMF, and Leymus chinensis. As for AMF, different species (Glomus etunicatum, GE; Glomus mosseae, GM; Glomus claroideum, GC; and Glomus intraradices, GI) and AMF richness (no AMF, single AMF taxa, double AMF mixtures, triple AMF mixtures, and all four together) were considered. Our results showed that significant interactions were observed between endophytes and AMF, with endophytes interacting antagonistically with GM but synergistically with GI. No definitive interactions were observed between the endophytes and GE or GC. Additionally, the concentration of endophytes in the leaf sheath was positively correlated with the concentration of AMF in the roots under low AMF richness. The shoot biomass of L. chinensis was positively related to both endophyte concentration and AMF concentration, with only endophytes contributing to shoot biomass more than AMF. Endophytes and AMF increased shoot growth by contributing to phosphorus uptake. The interactive effects of endophytes and AMF on host growth were affected by the identity of AMF species. The beneficial effect of the endophytes decreased in response to GM but increased in response to GI. However, no influences were observed with other GC and GE. In addition, endophyte presence can alter the response of host plants to AMF richness. When leaf endophytes were absent, shoot biomass increased with higher AMF richness, only the influence of AMF species identity outweighed that of AMF richness. However, when leaf endophytes were present, no significant association was observed between AMF richness and shoot biomass. AMF species identity rather than AMF richness promoted shoot growth. The results of this study demonstrate that the outcomes of interspecific symbiotic interactions are very complex and vary with partner identity such that the effects of simultaneous symbioses cannot be generalized and highlight the need for studies to evaluate fitness response of all three species, as the interactive effects may not be the same for each partner.

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References

  1. Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite-what decides? Curr Opin Plant Biol 9:358–363

    PubMed  Google Scholar 

  2. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    CAS  Google Scholar 

  3. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342

    PubMed  CAS  Google Scholar 

  4. Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    PubMed  CAS  Google Scholar 

  5. Omacini M, Semmartin M, Perez LI, Gundel PE (2012) Grass–endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279

    Google Scholar 

  6. Zaidi A, Khan MS (2007) Stimulatory effects of dual inoculation with phosphate solubilizing microorganisms and arbuscular mycorrhizal fungus on chickpea. Anim Prod Sci 47:1016–1022

    CAS  Google Scholar 

  7. Arrieta A, Iannones LJ, 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 17:146–154

    Google Scholar 

  8. Berthelot C, Blaudez D, Beguiristain T, Chalot M, Leyval C (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

    PubMed  CAS  Google Scholar 

  9. 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

    PubMed  Google Scholar 

  10. Smith SE, Read DJ (2008) Mycorrhizal Symbiosisthird edn. Academic press, Oxford

    Google Scholar 

  11. Lee BR, Muneer S, Jung WJ, Avice JC, Ourry 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 145:440–449

    PubMed  CAS  Google Scholar 

  12. Zhang YF, Wang P, Yang YF, Bi Q, Tian SY, Shi XW (2011) Arbuscular mycorrhizal fungi improve reestablishment of Leymus chinensis in bare saline-alkaline soil: implication on vegetation restoration of extremely degraded land. J Arid Environ 75:773–778

    Google Scholar 

  13. Pebriansyah A, Karti PDMH, Permana (2012) Role of arbuscular mycorrhizal fungi (AMF) in overcoming drought stress of several tropical grasses. Proceeding of the 2nd International Seminar on Animal Industry Jakarta:5–6

  14. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940

    CAS  Google Scholar 

  15. Zhang YP, Nan ZB (2007) Growth and anti-oxidative systems changes in Elymus dahuricus is affected by Neotyphodium endophyte under contrasting water availability. J Agron Crop Sci 193:377–386

    CAS  Google Scholar 

  16. Kannadan S, Rudgers JA (2008) Endophyte symbiosis benefits a rare grass under low water availability. Funct Ecol 22:706–713

    Google Scholar 

  17. Zai XM, Zhang HS, Hao ZP (2017) Effects of arbuscular mycorrhizal fungi and phosphate-solubilizing fungus on the rooting, growth and rhizosphere niche of beach plum (Prunus maritima) cuttings in a phosphorus-deficient soil. J Am Pomol Soc 71:226–235

    Google Scholar 

  18. Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:10–23

    Google Scholar 

  19. Rudgers JA, Clay K (2005) Fungal endophytes in terrestrial communities and ecosystems. In: Dighton EJ, Oudemans P, White JFJ (eds) The fungal community. M. Dekker, New York, pp 423–444

  20. Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320

    Google Scholar 

  21. Schardl CL, Leuchtmann A, Chung K-R, Penny D, Siegel MR (1997) Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Mol Biol Evol 14:133–143

    CAS  Google Scholar 

  22. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyper-diverse? Ecol Lett 3:267–274

    Google Scholar 

  23. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297

    Google Scholar 

  24. Bush LP, Wilkinson HH, Schardl CL (1997) Bio-protective alkaloids of grass-fungal endophyte symbiosis. Plant Physiol 114:1–7

    PubMed  PubMed Central  CAS  Google Scholar 

  25. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340

    PubMed  CAS  Google Scholar 

  26. Popay AJ (2009) Insect herbivory and defensive mutualisms between plants and fungi. In: White Jr J, Torres M (eds) Defensive mutualism in microbial symbiosis. Boca Raton, pp 347–358

  27. Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, Calie PJ et al (2013) Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genet 9:1–26

    Google Scholar 

  28. Clay K (1987) Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 73:3583–3562

    Google Scholar 

  29. Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97

    Google Scholar 

  30. Marks S, Clay K, Cheplick GP (1991) Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca Arundinacea and Lolium Perenne. J Appl Ecol 28:194–204

    Google Scholar 

  31. Malinowski DP, Leuchtmann A, Schmidt D, Nösberger J (1997) Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agron J 89:673–678

    Google Scholar 

  32. Morse LJ, Day TA, Faeth SH (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability. Environ Exp Bot 48:257–268

    Google Scholar 

  33. Rudgers JA, Swafford AL (2009) Benefits of a fungal endophyte in Elymus virginicus decline under drought stress. Basic Appl Ecol 10:43–51

    Google Scholar 

  34. Liu H, Chen W, Wu M, Wu RH, Zhou Y, Gao YB, Ren AZ (2017) Arbuscular mycorrhizal fungus inoculation reduces the drought-resistance advantage of endophyte-infected versus endophyte-free Leymus chinensis. Mycorrhiza 27:791–799

    PubMed  CAS  Google Scholar 

  35. Malinowski DP, Alloush GA, Belesky DP (1998) Evidence for chemical changes on the roots surface of tall fescue in response to infection with fungal endophyte Neotyphodium coenophialum. Plant Soil 205:1–12

    CAS  Google Scholar 

  36. Malinowski DP, Belesky DP (1999) Neotyphodium coenophialum endophyte infection affects the ability of tall fescue to use sparingly available phosphorus. J Plant Nutr 22:835–853

    CAS  Google Scholar 

  37. Rahman MH, Saiga S (2005) Endophytic fungi (Neotyphodium coenophialum) affect the growth and mineral uptake, transport and efficiency ratios in tall fescue (Festuca arundinacea). Plant Soil 272:163–171

    CAS  Google Scholar 

  38. Ren AZ, Gao YB, Zhou F (2007) Response of Neotyphodium lolii-infected perennial ryegrass to phosphorus deficiency. Plant Soil Environ 53:113–119

    CAS  Google Scholar 

  39. Li X, Zhou Y, Mace W, Qin JH, Liu H, Chen W, Ren AZ, Gao YB (2016) Endophyte species influence the biomass production of the native grass Achnatherum sibiricum (L.) Keng under high nitrogen availability. Ecol Evol 6:8595–8606

    PubMed  PubMed Central  Google Scholar 

  40. Christensen MJ (1996) Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Australas Plant Path 25:186–191

    Google Scholar 

  41. Wang X, Qin JH, Chen W, Zhou Y, Ren AZ, Gao YB (2016) Pathogen resistant advantage of endophyte-infected over endophyte-free Leymus chinensis is strengthened by pre-drought treatment. Eur J Plant Pathol 144:477–486

    CAS  Google Scholar 

  42. Chen W, Liu H, Wurihan GYB, Card SD, Ren AZ (2017) The advantages of endophyte infected over uninfected tall fescue in the growth and pathogen resistance are counteracted by elevated CO2. Sci Rep 7:1–12

    Google Scholar 

  43. Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325

    PubMed  Google Scholar 

  44. Smith SE, Read DJ (1997) Mycorrhizal symbiosis2nd edn. Academic Press

  45. Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068

    Google Scholar 

  46. Marulanda A, Azcón R, Ruiz-Lozano MJ (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa L. plants under drought stress. Physiol Plant 119:526–533

    CAS  Google Scholar 

  47. Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik J (eds) Arbuscular mycorrhizas: physiology and function2nd edn. Springer, Heidelberg, pp 193–208

    Google Scholar 

  48. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism – parasitism continuum. New Phytol 135:575–586

    Google Scholar 

  49. Allen EB, Allen MF, Egerton-Warburton L, Corkidi L, Gómez-Pompa A (2003) Impacts of early – and late – seral mycorrhizae during restoration in seasonal tropical forest, Mexico. Ecol Appl 13:1701–1717

    Google Scholar 

  50. Novas MV, Cabral D, Godeas AM (2005) Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 40:23–30

    Google Scholar 

  51. Novas MV, Iannone LJ, Godeas AM, Cabral D (2009) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog 8:75–81

    Google Scholar 

  52. Liu QH, Parsons AJ, Xue H, Fraser K, Ryan G, 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 25:910–920

    Google Scholar 

  53. Vignale MV, Iannone LJ, Pinget AD, De Battista JP, Novas MV (2016) Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 405:279–287

    CAS  Google Scholar 

  54. 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 24:633–637

    Google Scholar 

  55. Guo B, Hendrix J, An ZQ, Ferriss R (1992) Role of Acremonium endophyte of fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 84:882–885

    Google Scholar 

  56. Müller J (2003) Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct Plant Biol 30:419–424

    Google Scholar 

  57. 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 20:226–232

    Google Scholar 

  58. Zhou Y, Li X, Gao Y, Liu H, Gao YB, van der Heijden MGA, Ren AZ (2018) Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct Ecol 32:1168–1179

    Google Scholar 

  59. 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 20:56–65

    Google Scholar 

  60. Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    PubMed  CAS  Google Scholar 

  61. Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313

    PubMed  Google Scholar 

  62. Wagg C, Barendregt C, Jansa J, van der Heijden MGA (2015) Complementarity in both plant and mycorrhizal fungal communities are not necessarily increased by diversity in the other. J Ecol 103:1233–1244

    Google Scholar 

  63. Zhu MJ, Ren AZ, Wen W, Gao YB (2013) Diversity and taxonomy of endophytes from Leymus chinensis in the Inner Mongolia steppe of China. FEMS Microbiol Lett 340:135–145

    PubMed  CAS  Google Scholar 

  64. Huang ZH, Zhu JM, Mu XJ, Lin JX (2004) Pollen dispersion, pollen viability and pistil receptivity in Leymus chinensis. Ann Bot 93:295–301

    PubMed  PubMed Central  Google Scholar 

  65. Wei MK, Gao YB, Xu H, Su D, Zhang X, Wang YH, Lin F, Chen L, Nie LY, Ren AZ (2006) Occurrence of endophytes in grasses native to northern China. Grass Forage Sci 61:422–429

    Google Scholar 

  66. Latch GCM, Christensen MJ, Samuels GJ (1984) Five endophytes of Lolium and Festuca in New Zealand. Mycotaxon 167:338–342

    Google Scholar 

  67. Liu H, Chen W, Zhou Y, Li X, Ren AZ, Gao YB (2015) Effects of endophyte and arbuscular mycorrhizal fungi on growth of Leymus chinensis. J Plant Ecol 39:477–485

    Google Scholar 

  68. Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562

    PubMed  Google Scholar 

  69. Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA (2011) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92:1303–1313

    PubMed  Google Scholar 

  70. Wurst S, Kaiser N, Nitzsche S, Haase J, Auge H, Rillig MC, Powell JR (2015) Tree diversity modifies distance-dependent effects on seedling emergence but not plant-soil feedbacks of temperate trees. Ecology 96:1529–1539

    Google Scholar 

  71. Bao S (2000) Agrochemical analysis of soil. Beijing. Chinese Agricultural Press, China

    Google Scholar 

  72. Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol 173:787–797

    PubMed  CAS  Google Scholar 

  73. Buyer JS, Sasser M (2012) High throughput phospholipid fatty acid analysis of soils. Appl Soil Ecol 61:127–130

    Google Scholar 

  74. Rojas X, Guo JQ, Leff JW, McNear JDH, Fierer N, McCulley RL (2016) Infection with a shoot-specifc fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microb Ecol 72:197–206

    PubMed  CAS  Google Scholar 

  75. Vignale MV, Iannone LJ, Scervino JM, Novas MV (2017) Epichloë exudates promote in vitro and in vivo arbuscular mycorrhizal fungi development and plant growth. Plant Soil 422:267–281

    Google Scholar 

  76. 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 22:912–918

    Google Scholar 

  77. Larimer AL, Bever JD, Clay K (2012) Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121:2090–2096

    Google Scholar 

  78. Thrower LB, Lewis DH (1973) Uptake of sugars by Epichloë typhina (Pers. ex Fr.) Tul. In culture and from its host, Agrostis stolonifera L. New Phytol 72:501–508

    CAS  Google Scholar 

  79. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Google Scholar 

  80. Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7

    PubMed  PubMed Central  CAS  Google Scholar 

  81. Schardl CL, Young CA, Faulkner JR, Florea S, Pan J (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol 5:331–344

    Google Scholar 

  82. Prestidge RA, Gallagher RT (1988) Endophyte fungus confers resistance to ryegrass: argentine stem weevil larval studies. Ecol Entomol 13:429–435

    Google Scholar 

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This work was supported by the National Key Research and Development Program (2016YFC0500702) and National Natural Science Foundation of China (31570433).

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  1. College of Life Sciences, Nankai University, Tianjin, 300071, People’s Republic of China

    Hui Liu, Man Wu, Jinming Liu, Yaobing Qu, Yubao Gao & Anzhi Ren

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  1. Hui Liu
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Liu, H., Wu, M., Liu, J. et al. Tripartite Interactions Between Endophytic Fungi, Arbuscular Mycorrhizal Fungi, and Leymus chinensis. Microb Ecol 79, 98–109 (2020). https://doi.org/10.1007/s00248-019-01394-8

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