Abstract
Epichloë endophytes can not only affect the growth and resistance of the host plant but also change the biotic and abiotic properties of the soil where the host is situated. Here, we used endophyte-infected (EI) and endophyte-free (EF) Leymus chinensis as plant materials, to study the microbial diversity and composition in the host root endosphere and rhizosphere soil under both pot and field conditions. The results showed that endophyte infection did not affect the diversity of either bacteria or fungi in the root zone. There were significant differences in both bacterial and fungal communities between the root endosphere and the rhizosphere, and between the field and the pot, while endophytes only affected root endosphere microbial communities. The bacterial families affected by endophyte infection changed from 29.07% under field conditions to 40% under pot conditions. In contrast, the fungal families affected by endophyte infection were maintained at nearly 50% under both field and pot conditions. That is to say, bacterial communities in the root endosphere were more strongly affected by environmental conditions, and in comparison, the fungal communities were more strongly affected by species specificity. Endophytes significantly affected the fungal community composition of the host root endosphere in both potted and field plants, only the effect was more obvious in potted plants. Endophyte infection increased the abundance of three fungal families (Thelebolaceae, Herpotrichiellaceae and Trimorphomycetaceae) under both field and potted conditions. In potted plants, endophytes also altered the dominant fungi from pathogenic Pleosporales to saprophytic Chaetomiaceae. Endophyte infection increased the relative abundance of arbuscular mycorrhizal fungi and saprophytic fungi, especially under potted conditions.
Overall, endophytes significantly affected the fungal community composition of the host root endosphere in both potted and field plants. Endophytes had a greater impact on root endosphere microorganisms than the rhizosphere, a greater impact on fungal communities than bacteria, and a greater impact on root endosphere microorganisms under potted conditions than at field sites.
Similar content being viewed by others
Data availability
Data will be provided upon acceptance of manuscript.
References
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Chen W, Zhou H, Wu Y, Li Y, Xue S (2021) Plant-mediated effects of long-term warming on soil microorganisms on the Qinghai-Tibet Plateau. Catena 204:105391
Qiao YJ, Gu CZ, Zhu HT, Wang D, Zhang MY, Zhang YX, Yang CR, Zhang YJ (2020) Allelochemicals of Panax notoginseng and their effects on various plants and rhizosphere microorganisms. Plant Divers 42:11
Lapkina EZ, Saveleva EE, Tyrranen LS, Bulgakova NA (2021) The study of population dynamics of ecological groups of microorganisms epiphytic microbiota stellaria media and urtica dioica. Экосистемы 25:22–29. https://doi.org/10.37279/2414-4738-2021-25-22-29
Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse. Ecol Lett 3:267–274
Clay K (1989) Clavicipitaceolls endophytes of grasses: their potential as biocontrol agents. Mycol Res 92:1–12
Muller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456. https://doi.org/10.1016/j.pbi.2005.05.007
Chen X, Luo X, Fan M, Zeng W, Yang C, Wu J, Zhao C, Zhang Y, Zhao P (2019) Endophytic fungi from the branches of Camellia taliensis (W. W. Smith) Melchior, a widely distributed wild tea plant. World J Microbiol Biotechnol 35:113
Shan L, Shakoor A, Wubet T, Zhang N, Liang Y, Ma K (2018) Fine-scale variations of fungal community in a heterogeneous grassland in Inner Mongolia: Effects of the plant community and edaphic parameters. Soil Biol Biochem 122:104–110. https://doi.org/10.1016/j.soilbio.2018.04.007
Swamy N, Sandhu SS (2021) Fungal endophytes: Entry, establishment, diversity, future prospects in agriculture. Fungi Bio-Prospects in Sustainable Agriculture, Environment and Nano-Technology 1:97–105. https://doi.org/10.1016/B978-0-12-821394-0.00004-4
Vázquez-de-Aldana BR, Zabalgogeazcoa I, García-Ciudad A, García-Criado B (2013) An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil 362:201–213. https://doi.org/10.1007/s11104-012-1283-7
Zhang M, Wang H, Hussain M, Qi J, Wu G (2020) Identification and functional assessment of endophytic bacterial diversity in Ageratina adenophora (Sprengel) and their interactions with the host plant. South Afr J Bot 134:99–108. https://doi.org/10.1016/j.sajb.2020.07.038
Ganie SA, Bhat JA, Devoto A (2021) The influence of endophytes on rice fitness under environmental stresses. Plant Molecular Biology. https://doi.org/10.1007/s11103-021-01219-8
Fuchs B, Krischke M, Mueller MJ, Krauss J (2016) Herbivore-specific induction of defence metabolites in a grass–endophyte association. Funct Ecol 31:318–324. https://doi.org/10.1111/1365-2435.12755
Li F, Guo Y, Christensen MJ, Gao P, Li Y, Duan T (2018) An arbuscular mycorrhizal fungus and Epichloe festucae var. lolii reduce Bipolaris sorokiniana disease incidence and improve perennial ryegrass growth. Mycorrhiza 28:159–169. https://doi.org/10.1007/s00572-017-0813-9
Zhang Y, Yu X, Zhang W, Lang D, Zhang X, Cui G, Zhang X (2019) Interactions between endophytes and plants: beneficial effect of endophytes to ameliorate biotic and abiotic stresses in plants. J Plant Biol 62:1–13
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 25:910–920. https://doi.org/10.1111/j.1365-2435.2011.01853.x
Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320. https://doi.org/10.1111/j.2007.0030-1299.15973.x
Müller J (2003) Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Funct Plant Biol 30:419–424
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
Zhou Y, Li X, Gao Y, Liu H, Gao YB, van der Heijden MGA, Ren AZ, Bennett A (2018) Plant endophytes and arbuscular mycorrhizal fungi alter plant competition. Funct Ecol 32:1168–1179. https://doi.org/10.1111/1365-2435.13084
Zhou Y, Li X, Qin J, Liu H, Chen W, Niu Y, Ren A, Gao Y (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. https://doi.org/10.1016/j.funeco.2015.11.004
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. https://doi.org/10.1111/j.1600-0706.2012.20153.x
Yan ZC, Ying-De LI, Cheng WJ, Gao P, Guo YE, Duan TY (2018) Effects of AM fungi and grass endophyte on the growth of ryegrass under different salt concentrations. Grassl Turf 38:63–70. https://doi.org/10.13817/j.cnki.cyycp.2018.01.010
Arrieta AM, Iannone LJ, Scervino JM, Vignale MV, Novas MV (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. https://doi.org/10.1016/j.funeco.2015.07.001
Vignale MV, Iannone LJ, Pinget AD, De Battista JP, Novas MV (2015) Effect of epichloid endophytes and soil fertilization on arbuscular mycorrhizal colonization of a wild grass. Plant Soil 405:279–287. https://doi.org/10.1007/s11104-015-2522-5
Slaughter LC, Nelson JA, Carlisle AE, Bourguignon M, Dinkins RD, Phillips TD, McCulley RL (2019) Tall fescue and E. coenophiala genetics influence root-associated soil fungi in a temperate grassland. Front Microbiol 10:2380. https://doi.org/10.3389/fmicb.2019.02380
Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355. https://doi.org/10.1007/s11104-010-0607-8
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 339:401–412. https://doi.org/10.1007/s11104-010-0592-y
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 44:81–92. https://doi.org/10.1016/j.soilbio.2011.09.010
Mahmud K, Lee K, Hill N, Missaoui A (2021) Influence of tall fescue Epichloë endophytes on rhizosphere soil microbiome. Microorganisms 9:1–22. https://doi.org/10.21203/rs.3.rs-614409/v1
Jain A, Chakraborty J, Das S (2020) Underlying mechanism of plant–microbe crosstalk in shaping microbial ecology of the rhizosphere. Acta Physiol Plant 42:8
Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. https://doi.org/10.1016/j.tim.2008.07.008
Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, North G, Visel A, Partida-Martinez LP, Tringe SG (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol 209:798–811. https://doi.org/10.1111/nph.13697
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. https://doi.org/10.1038/nature11237
Fang M, Xu X, Tang M, Tang J (2019) Structure and composition variation of the root-microbiota of Rhododendron delavayi. Acta Microbiol Sin (in Chinese) 59:1522–1534. https://doi.org/10.13343/j.cnki.wsxb.20180449
Zhong R, Xia C, Ju Y, Li N, Zhang X, Nan Z, Christensen MJ (2018) Effects of Epichloë gansuensis on root-associated fungal communities of Achnatherum inebrians under different growth conditions. Funct Ecol 31:29–36. https://doi.org/10.1016/j.funeco.2017.10.005
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. https://doi.org/10.1111/1574-6968.12083
Tao J, Yayu W, Yueying H, Jin X, Pengfan Z, Nian W, Xin L, Haiyan C, Guang L, Honggang J (2017) Taxonomic structure and functional association of foxtail millet root microbiome. Gigascience 6:10. https://doi.org/10.1093/gigascience/giy099
Bram B, Michiel O, Sofie T, Sascha T, Nele W, Wout B, Jaco V (2016) Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in metabarcoding studies. Front Microbiol 7:650. https://doi.org/10.3389/fmicb.2016.00650
Lu K (1999) Analytical methods of soil and agricultural chemistry. China Agricultural Science and Technology Press, Beijing
Anderson JM, Ingram J (1994) Tropical soil biology and fertility: a handbook of methods. Soil Sci 157:265
Bulgarelli D, Garrido-Oter R, Münch P, Weiman A, DröGe J, Pan Y, Mchardy A, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403
Chen B, Kaiqian, Chao S, Arunprasanna A, Xili L, Yong (2018) Gut bacterial and fungal communities of the domesticated silkworm (Bombyx mori) and wild mulberry-feeding relatives. ISME J Emultidiscip J Microb Ecol 12:2252–2262
Roberts EL, Ferraro A (2015) Rhizosphere microbiome selection by Epichloë endophytes of Festuca arundinacea. Plant Soil 396:229–239. https://doi.org/10.1007/s11104-015-2585-3
Rojas X, Guo J, Leff JW, McNear DH Jr, Fierer N, McCulley RL (2016) Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microb Ecol 72:197–206. https://doi.org/10.1007/s00248-016-0750-8
Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: Implications for sustainable agriculture. Fungal Biol Rev 25:68–72. https://doi.org/10.1016/j.fbr.2011.01.002
Alzahrani A (2017) Communities of arbuscular mycorrhizal fungi in salt marsh habitats: diversity, structure, and ecosystem function. Dissertation, University of Essex
Heijden MGAVD, Horton TR (2010) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150. https://doi.org/10.1111/j.1365-2745.2009.01570.x
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620. https://doi.org/10.1111/j.1469-8137.2006.01936.x
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.https://doi.org/10.1093/femsec/fix036
Zhong R, Xia C, Ju Y, Zhang X, Duan T, Nan Z, Li C (2019) A foliar Epichloë endophyte and soil moisture modified belowground arbuscular mycorrhizal fungal biodiversity associated with Achnatherum inebrians. Plant Soil. https://doi.org/10.1007/s11104-019-04365-7
Al-Hatmi AM, Meis JF, de Hoog GS (2016) Fusarium: Molecular diversity and intrinsic drug resistance. PLoS Pathog 12:e1005464. https://doi.org/10.1371/journal.ppat.1005464
Azegami K, Nishiyama K, Watanabe Y, Kadota I, Fukazawa C (1987) Pseudomonas plantarii sp. nov., the causal agent of rice seedling blight. Int J Syst Bacteriol 37:144–152. https://doi.org/10.1099/00207713-37-2-144
Urakami T, Ito-Yoshida C, Araki H, Kijima T, Suzuki KI, Komagata K (1994) Transfer of Pseudomonas plantarii and Pseudomonas glumae to Burkholderia as Burkholderia spp. and Description of Burkholderia vandii sp. nov. Int J Syst Bacteriol 44:235–245
Wang C, Zhang M, Huang N, Ma J (2017) Review on the application of Photosynthetic bacteria. Anhui AgriSci (in Chinese) 23. https://doi.org/10.16377/j.cnki.issn1007-7731.2017.10.012
Li XZ, Fang AG, Li CJ, Nan ZB (2015) Advances in the researches on the effects of grass endophytes on other microbes. Acta Ecol Sin 35:1660–1671
Tian P, Nan Z, Li C, Spangenberg G (2008) Effect of the endophyte Neotyphodium lolii on susceptibility and host physiological response of perennial ryegrass to fungal pathogens. Eur J Plant Pathol 122:593–602. https://doi.org/10.1007/s10658-008-9329-7
Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EH, Hyde KD, Jeewon R (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590. https://doi.org/10.1007/s00248-006-9117-x
Promputtha I, Hyde KD, McKenzie EHC, Peberdy JF, Lumyong S (2010) Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers 41:89–99. https://doi.org/10.1007/s13225-010-0024-6
Bell-Dereske L, Gao X, Masiello CA, Sinsabaugh RL, Rudgers JA (2016) Plant–fungal symbiosis affects litter decomposition during primary succession. Oikos 126:801–811. https://doi.org/10.5061/dryad.11nr8
Hannula SE, Kielak AM, Steinauer K, Huberty M, Heinen R, Bezemer TM (2019) Time after time temporal variation in the effects of grass and forb species on soil bacterial and fungal communities Ecological and Evolutionary. Science 10:e02635-e2719. https://doi.org/10.1128/mBio
Zhou Y, Zheng Y, Zhu J, Li X, Ren Z, Gao B (2014) Effects of fungal endophyte infection on soil properties and microbial communities in the host grass habitat. Chin J Plant Ecol 38:54–61
Zhong R, Zhou R, Zhang Q, Xia C, Li N (2017) Effect of Epichloe gansuensis on arbuscular mycorrhizal fungi spore diversity in rhizophere soil of drunken horse grass under different growth conditions. Pratacult Sci (in Chinese) 34:1627–1634. https://doi.org/10.11829/j.issn.1001-0629.2017-0067
Prestidge RA (1993) Causes and control of perennial ryegrass staggers in New Zealand. Ecosyst Environ 44:283–300
Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: Currencies of mutualism. Phytochemistry 68:980–996. https://doi.org/10.1016/j.phytochem.2007.01.010
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340. https://doi.org/10.1146/annurev.arplant.55.031903.141735
Acknowledgements
We greatly appreciate the support of Abaga banner grassland workstation for their invaluable assistance on this experiment.
Funding
This work was supported by the National Natural Science Foundation of China (31971425).
Author information
Authors and Affiliations
Contributions
Jing Chen was involved in investigation, visualization, writing—original draft. Yongkang Deng performed data curation. Xinhe Yu contributed to software. Guanghong Wu provided methodology, review & editing. Yubao Gao performed conceptualization. Anzhi Ren did conceptualization, funding acquisition, supervision, writing—review & editing.
Corresponding authors
Ethics declarations
Conflicts of interests
The authors declare that they have no known competing financial interests or personal relationships that could influence the work reported in this paper.
Ethics approval
Not applicable.
Rights and permissions
About this article
Cite this article
Chen, J., Deng, Y., Yu, X. et al. Epichloë Endophyte Infection Changes the Root Endosphere Microbial Community Composition of Leymus Chinensis Under Both Potted and Field Growth Conditions. Microb Ecol 85, 604–616 (2023). https://doi.org/10.1007/s00248-022-01983-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-022-01983-0