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RESEARCH ARTICLE (Open Access)

Plant species, nitrogen status and endophytes are drivers of soil microbial communities in grasslands

Susanne Rasmussen A , Anthony J. Parsons A , Julia Russell B , Daniel A. Bastías https://orcid.org/0000-0002-0522-5538 C and Qianhe Liu https://orcid.org/0000-0002-2791-2187 C *
+ Author Affiliations
- Author Affiliations

A Institute of Agriculture and Environment, Massey University, Palmerston North, New Zealand.

B John Innes Centre, Norwich Research Park, Norwich, UK.

C AgResearch Limited, Grasslands Research Centre, Palmerston North, New Zealand.

* Correspondence to: qianhe.liu@agresearch.co.nz

Handling Editor: Megan Ryan

Crop & Pasture Science 75, CP23149 https://doi.org/10.1071/CP23149
Submitted: 29 May 2023  Accepted: 12 September 2023  Published: 28 September 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

There is concern that the introduction of ‘novel’ plant germplasm/traits could outpace our capacity to measure and so assess their impacts on soil microbial communities and function.

Aim

This study aimed to investigate the effects of plant species/functional traits, nitrogen (N) fertilisation and endophyte infection on grassland soil microbial communities within a short time span of 2 years.

Methods

Two field experiments with monoculture plots were conducted in a common soil. Experiment 1 compared grasses and legumes, using two cultivars of perennial ryegrass (Lolium perenne) that varied in fructan content, along with the legumes white clover (Trifolium repens) and bird’s-foot trefoil (Lotus pedunculatus) that varied in tannin content. Grass treatments received high and low N application levels. Experiment 2 compared the presence/absence of Epichloë strains in ryegrass, tall fescue (Schedonorus phoenix) and meadow fescue (Schedonorus pratensis). Soil microbial communities were analysed by using high-throughput sequencing of DNA isolated from bulk soil cores.

Key results

Higher abundance of ligninolytic fungi was found in grass soils and pectinolytic fungi in legume soils. Levels of N fertilisation and fructan in ryegrass had only minor effects on soil fungal communities. By contrast, N fertilisation or fixation had a strong effect on bacterial communities, with higher abundance of nitrifiers and denitrifiers in high-N grass soils and in legume soils than in low-N grass soils. Epichloë affected soil microbiota by reducing the abundance of certain fungal phytopathogens, increasing mycorrhizal fungi and reducing N-fixing bacteria.

Conclusions

Chemical composition of plant cell walls, which differs between grasses and legumes, and presence of Epichloë in grasses were the main drivers of shifts in soil microbial communities.

Implications

Impacts of farming practices such as mono- or poly-culture, N fertilisation and presence of Epichloë in grasses on soil microbial communities should be considered in pasture management.

Keywords: bulk soil, Epichloë, legumes, microbiota, nitrogen, pastures, soil microbial community, temperate grasslands.

References

Atiwesh G, Parrish CC, Banoub J, Le T-AT (2022) Lignin degradation by microorganisms: a review. Biotechnology Progress 38(2), e3226.
| Crossref | Google Scholar | PubMed |

Barrasa JM, Blanco MN, Esteve-Raventós F, Altés A, Checa J, Martinez AT, et al. (2014) Wood and humus decay strategies by white-rot basidiomycetes correlate with two different dye decolorization and enzyme secretion patterns on agar plates. Fungal Genetics and Biology 72(11), 106-114.
| Crossref | Google Scholar |

Bastías DA, Gundel PE (2023) Plant stress responses compromise mutualisms with Epichloë endophytes. Journal of Experimental Botany 74(1), 19-23.
| Crossref | Google Scholar | PubMed |

Bastías DA, Balestrini R, Pollmann S, Gundel PE (2022) Environmental interference of plant−microbe interactions. Plant, Cell & Environment 45(12), 3387-3398.
| Crossref | Google Scholar | PubMed |

Benitez M-S, Taheri WI, Lehman RM (2016) Selection of fungi by candidate cover crops. Applied Soil Ecology 103(7), 72-82.
| Crossref | Google Scholar |

Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, et al. (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. Journal of Ecology 94(5), 893-904.
| Crossref | Google Scholar |

Bisaria VS, Ghose TK (1981) Biodegradation of cellulosic materials: substrates, microorganisms, enzymes and products. Enzyme and Microbial Technology 3(2), 90-104.
| Crossref | Google Scholar |

Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL, Seabloom EW, et al. (2014) Finding generality in ecology: a model for globally distributed experiments. Methods in Ecology and Evolution 5(1), 65-73.
| Crossref | Google Scholar |

Brisson N, Gate P, Gouache D, Charmet G, Oury F-X, Huard F (2010) Why are wheat yields stagnating in Europe? A comprehensive data analysis for France. Field Crops Research 119(1), 201-212.
| Crossref | Google Scholar |

Brown AE, Finlay R, Ward JS (1987) Antifungal compounds produced by Epicoccum purpurascens against soil-borne plant pathogenic fungi. Soil Biology and Biochemistry 19(6), 657-664.
| Crossref | Google Scholar |

Cai Y, Sun Y (2011) ESPRIT-Tree: hierarchical clustering analysis of millions of 16S rRNA pyrosequences in quasilinear computational time. Nucleic Acids Research 39(14), e95.
| Crossref | Google Scholar | PubMed |

Card SD, Bastías DA, Caradus JR (2021) Antagonism to plant pathogens by Epichloë fungal endophytes – a review. Plants 10(10), 1997.
| Crossref | Google Scholar | PubMed |

Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annual Review of Plant Physiology and Plant Molecular Biology 47, 445-476.
| Crossref | Google Scholar | PubMed |

Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant and Soil 340, 347-355.
| Crossref | Google Scholar |

Chen YP, Rekha PD, Arun AB, Shen FT, Lai W-A, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Applied Soil Ecology 34(1), 33-41.
| Crossref | Google Scholar |

Chen Z, White JF, Malik K, Chen H, Jin Y, Yao X, Wei X, Li C, Nan Z (2022) Soil nutrient dynamics relate to Epichloë endophyte mutualism and nitrogen turnover in a low nitrogen environment. Soil Biology and Biochemistry 174, 108832.
| Crossref | Google Scholar |

Cripps MG, Edwards GR, McKenzie SL (2013) Grass species and their fungal symbionts affect subsequent forage growth. Basic and Applied Ecology 14(3), 225-234.
| Crossref | Google Scholar |

De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters 11(5), 516-531.
| Crossref | Google Scholar | PubMed |

DeBoy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H, Emerson JB, et al. (2008) Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicas. Journal of Bacteriology 190(15), 5455-5463.
| Crossref | Google Scholar | PubMed |

Domsch KH, Gams W (1969) Variability and potential of a soil fungus population to decompose pectin, xylan and carboxymethyl-cellulose. Soil Biology and Biochemistry 1(1), 29-36.
| Crossref | Google Scholar |

Dudeja SS, Giri R (2014) Beneficial properties, colonization, establishment and molecular diversity of endophytic bacteria in legumes and non legumes. African Journal of Microbiology Research 8(15), 1562-1572.
| Crossref | Google Scholar |

Dunfield PF, Tamas I, Lee KC, Morgan XC, McDonald IR, Stott MB (2012) Electing a candidate: a speculative history of the bacterial phylum OP10. Environmental Microbiology 14(12), 3069-3080.
| Crossref | Google Scholar | PubMed |

Dungait JAJ, Hopkins DW, Gregory AS, Whitmore AP (2012) Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biology 18(6), 1781-1796.
| Crossref | Google Scholar |

Dzoyem JP, Melong R, Tsamo AT, Maffo T, Kapche DGWF, Ngadjui BT, et al. (2017) Cytotoxicity, antioxidant and antibacterial activity of four compounds produced by an endophytic fungus Epicoccum nigrum associated with Entada abyssinica. Revista Brasileira de Farmacognosia 27(2), 251-253.
| Crossref | Google Scholar |

Eady C (2021) The impact of alkaloid-producing Epichloë endophyte on forage ryegrass breeding: a New Zealand perspective. Toxins 13(2), 158.
| Crossref | Google Scholar | PubMed |

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16), 2194-2200.
| Crossref | Google Scholar | PubMed |

Elderiny N, Lee J-J, Lee Y-H, Park S-J, Lee S-Y, Park S, et al. (2017) Adhaeribacter terrae sp. nov., a novel bacterium isolated from soil. International Journal of Systematic and Evolutionary Microbiology 67(8), 2922-2927.
| Crossref | Google Scholar | PubMed |

Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends in Ecology & Evolution 17(4), 177-183.
| Crossref | Google Scholar |

Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecology Letters 12(11), 1238-1249.
| Crossref | Google Scholar | PubMed |

Filip Z, Haider K, Martin JP (1972) Influence of clay minerals on the formation of humic substances by Epicoccum nigrum and Stachybotrys chartarum. Soil Biology and Biochemistry 4(2), 147-154.
| Crossref | Google Scholar |

Filip Z, Haider K, Beutelspacher H, Martin JP (1974) Comparisons of IR-spectra from melanins of microscopic soil fungi, humic acids and model phenol polymers. Geoderma 11(1), 37-52.
| Crossref | Google Scholar |

Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, et al. (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089), 1715-1719.
| Crossref | Google Scholar | PubMed |

García-Parisi PA, Lattanzi FA, Grimoldi AA, Druille M, Omacini M (2017) Three symbionts involved in interspecific plant-soil feedback: epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis. Plant and Soil 412, 151-162.
| Crossref | Google Scholar |

Ghahramani A, Howden SM, del Prado A, Thomas DT, Moore AD, Ji B, Ates S (2019) Climate change impact, adaptation, and mitigation in temperate grazing systems: a review. Sustainability 11(24), 7224.
| Crossref | Google Scholar |

Ghimire SR, Craven KD (2011) Enhancement of switchgrass (Panicum virgatum L.) biomass production under drought conditions by the ectomycorrhizal fungus Sebacina vermifera. Applied and Environmental Microbiology 77(19), 7063-7067.
| Crossref | Google Scholar | PubMed |

Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspective and future prospects. American Journal of Alternative Agriculture 1(2), 51-57.
| Crossref | Google Scholar |

Grabber JH, Ralph J, Lapierre C, Barrière Y (2004) Genetic and molecular basis of grass cell-wall degradability. I. Lignin-cell wall matrix interactions. Comptes Rendus Biologies 327(5), 455-465.
| Crossref | Google Scholar | PubMed |

Hancock KR, Collette V, Fraser K, Greig M, Xue H, Richardson K, et al. (2012) Expression of the R2R3-MYB transcription factor TaMYB14 from Trifolium arvense activates proanthocyanidin biosynthesis in the legumes Trifolium repens and Medicago sativa. Plant Physiology 159(3), 1204-1220.
| Crossref | Google Scholar | PubMed |

Harris JR (1986) The association of Phoma sclerotioides with root diseases of cereals, legumes and weeds. Australasian Plant Pathology 15, 14-17.
| Crossref | Google Scholar |

Harris PJ, Smith BG (2006) Plant cell walls and cell-wall polysaccharides: structures, properties and uses in food products. International Journal of Food Science and Technology 41(s2), 129-143.
| Crossref | Google Scholar |

Hartmann M, Lee S, Hallam SJ, Mohn WW (2009) Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environmental Microbiology 11(12), 3045-3062.
| Crossref | Google Scholar | PubMed |

Jones MB, Donnelly A (2004) Carbon sequestration in temperate grassland ecosystems and the influence of management, climate and elevated CO2. New Phytologist 164(3), 423-439.
| Crossref | Google Scholar |

Kelliher FM, Parfitt RL, van Koten C, Schipper LA, Rys G (2013) Use of shallow samples to estimate the total carbon storage in pastoral soils. New Zealand Journal of Agricultural Research 56(1), 86-90.
| Crossref | Google Scholar |

Khan ST, Horiba Y, Yamamoto M, Hiraishi A (2002) Members of the family Comamonadaceae as primary poly(3-hydroxybutyrate-co-3-hydroxyvalerate)-degrading denitrifiers in activated sludge as revealed by a polyphasic approach. Applied and Environmental Microbiology 68(7), 3206-3214.
| Crossref | Google Scholar | PubMed |

Klejdus B, Vacek J, Lojková L, Benešová L, Kubáñ V (2008) Ultrahigh-pressure liquid chromatography of isoflavones and phenolic acids on different stationary phases. Journal of Chromatography A 1195(1–2), 52-59.
| Crossref | Google Scholar | PubMed |

Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annual Review of Phytopathology 47, 39-62.
| Crossref | Google Scholar | PubMed |

Knowles R (1982) Denitrification. Microbiological Reviews 46(1), 43-70.
| Crossref | Google Scholar | PubMed |

Kolton M, Erlacher A, Berg G, Cytryn E (2016) The Flavobacterium genus in the plant Holobiont: ecological, physiological, and applicative insights. In ‘Microbial models: from environmental to industrial sustainability. Vol. 1. Microorganisms for sustainability’. (Ed. S Castro-Sowinski) pp. 189–207. (Springer: Singapore) doi:10.1007/978-981-10-2555-6_9

Kou M-Z, Bastías DA, Christensen MJ, Zhong R, Nan Z-B, Zhang X-X (2021) The plant salicylic acid signalling pathway regulates the infection of a biotrophic pathogen in grasses associated with an Epichloë endophyte. Journal of Fungi 7(8), 633.
| Crossref | Google Scholar | PubMed |

Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Review of Microbiology 55, 485-529.
| Crossref | Google Scholar | PubMed |

Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104), 806-809.
| Crossref | Google Scholar | PubMed |

Mahmud K, Lee K, Hill NS, Mergoum A, Missaoui A (2021) Influence of tall fescue Epichloë endophytes on rhizosphere soil microbiome. Microorganisms 9(9), 1843.
| Crossref | Google Scholar |

Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology 5, 28.
| Crossref | Google Scholar | PubMed |

McGee DC, Kellock AW (1974) Fusarium avenaceum, a seed-borne pathogen of subterranean clover roots. Australian Journal of Agricultural Research 25, 549-557.
| Crossref | Google Scholar |

McSherry ME, Ritchie ME (2013) Effects of grazing on grassland soil carbon: a global review. Global Change Biology 19(5), 1347-1357.
| Crossref | Google Scholar | PubMed |

Morgenstern I, Klopman S, Hibbett DS (2008) Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. Journal of Molecular Evolution 66(3), 243-257.
| Crossref | Google Scholar | PubMed |

Mudge PL, Kelliher FM, Knight TL, O’Connell D, Fraser S, Schipper LA (2017) Irrigating grazed pasture decreases soil carbon and nitrogen stocks. Global Change Biology 23(2), 945-954.
| Crossref | Google Scholar | PubMed |

Murphy WM, Gotlieb AR, Dugdale DT (1985) The effects of Fusarium wilt and weed control on survival of birdsfoot trefoil. Canadian Journal of Plant Science 65(2), 329-334.
| Crossref | Google Scholar |

Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. The Plant Cell 7(7), 869-885.
| Crossref | Google Scholar | PubMed |

Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, et al. (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS ONE 6(2), e17000.
| Crossref | Google Scholar | PubMed |

Nemergut DR, Townsend AR, Sattin SR, Freeman KR, Fierer N, Neff JC, et al. (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environmental Microbiology 10(11), 3093-3105.
| Crossref | Google Scholar | PubMed |

Nuchdang S, Vatanyoopaisarn S, Phalakornkule C (2015) Effectiveness of fungal treatment by Coprinopsis cinerea and Polyporus tricholoma on degradation and methane yields of lignocellulosic grass. International Biodeterioration & Biodegradation 104, 38-45.
| Crossref | Google Scholar |

Oenema O, Wrage N, Velthof GL, van Groenigen JW, Dolfing J, Kuikman PJ (2005) Trends in global nitrous oxide emissions from animal production systems. Nutrient Cycling in Agroecosystems 72, 51-65.
| Crossref | Google Scholar |

Ohta Y, Nishi S, Kobayashi K, Tsubouchi T, Iida K, Tanizaki A, et al. (2015) Draft genome sequence of Novosphingobium sp. strain MBES04, isolated from sunken wood from Suruga Bay, Japan. Genome Announcements 3(1), e01373–14.
| Crossref | Google Scholar | PubMed |

Oliveira DM, Mota TR, Grandis A, de Morais GR, de Lucas RC, Polizeli MLTM, et al. (2020) Lignin plays a key role in determining biomass recalcitrance in forage grasses. Renewable Energy 147(1), 2206-2217.
| Crossref | Google Scholar |

Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecological Research 22(6), 955-974.
| Crossref | Google Scholar |

Osono T (2010) Decomposition of grass leaves by ligninolytic litter-decomposing fungi. Grassland Science 56(1), 31-36.
| Crossref | Google Scholar |

Parsons AJ, Rowarth JS, Rasmussen S (2011) High sugar grasses. In ‘Plant sciences reviews 2011’. (Ed. D Hemming) pp.187–195. (CABI Reviews: Wallingford, UK) doi:10.1079/PAVSNNR20116046

Parsons AJ, Thornley JHM, Newton PCD, Rasmussen S, Rowarth JS (2013) Soil carbon dynamics: the effects of nitrogen input, intake demand and off-take by animals. Science of The Total Environment 465, 205-215.
| Crossref | Google Scholar | PubMed |

Parsons AJ, Thornley JHM, Rasmussen S, Rowarth JS (2016) Some clarification of the impacts of grassland intensification on food production, nitrogen release, greenhouse gas emissions and carbon sequestration: using the example of New Zealand. CAB Reviews 11(54), 1-19.
| Crossref | Google Scholar |

Patchett A, Newman JA (2021) Comparison of plant metabolites in root exudates of Lolium perenne infected with different strains of the fungal endophyte Epichloë festucae var. lolii. Journal of Fungi 7(2), 148.
| Crossref | Google Scholar | PubMed |

Patureau D, Bernet N, Moletta R (1996) Study of the denitrifying enzymatic system of Comamonas sp. strain SGLY2 under various aeration conditions with a particular view on nitrate and nitrite reductases. Current Microbiology 32, 25-32.
| Crossref | Google Scholar |

Pellissier L, Niculta-Hirzel H, Dubuis A, Pagni M, Guex N, Ndiribe C, et al. (2014) Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps. Molecular Ecology 23, 4274-4290.
| Crossref | Google Scholar | PubMed |

Piechulla B, Lemfack MC, Kai M (2017) Effects of discrete bioactive microbial volatiles on plants and fungi. Plant, Cell & Environment 40, 2042-2067.
| Crossref | Google Scholar | PubMed |

Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, et al. (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters 18(1), 85-95.
| Crossref | Google Scholar | PubMed |

Qu T-B, Du W-C, Yuan X, Yang Z-M, Liu D-B, Wang D-L, Yu L-J (2016) Impacts of grazing intensity and plant community composition on soil bacterial community diversity in a steppe grassland. PLoS ONE 11(7), e0159680.
| Crossref | Google Scholar |

Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12(1), 38.
| Crossref | Google Scholar |

Reichenbach H, Lang E, Schumann P, Spröer C (2006) Byssovorax cruenta gen. nov., sp. nov., nom. Rev., a cellulose-degrading myxobacterium: rediscovery of ‘Myxococcus cruentus’ Thaxter 1897. International Journal of Systematic and Evolutionary Microbiology 56(10), 2357-2363.
| Crossref | Google Scholar |

Reisinger A, Ledgard S (2013) Impact of greenhouse gas metrics on the quantification of agricultural emissions and farm-scale mitigation strategies: a New Zealand case study. Environmental Research Letters 8, 025019.
| Crossref | Google Scholar |

Rochon DA, Kakani K, Robbins M, Reade R (2004) Molecular aspects of plant virus transmission by Olpidium and plasmodiophorid vectors. Annual Review of Phytopathology 42, 211-241.
| Crossref | Google Scholar | PubMed |

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. Microbial Ecology 72(1), 197-206.
| Crossref | Google Scholar | PubMed |

Schardl CL, Florea S, Pan J, Nagabhyru P, Bec S, Calie PJ (2013) The epichloae: alkaloid diversity and roles in symbiosis with grasses. Current Opinion in Plant Biology 16(4), 480-488.
| Crossref | Google Scholar | PubMed |

Schipper LA, Parfitt RL, Ross C, Baisden WT, Claydon JJ, Fraser S (2010) Gains and losses in C and N stocks of New Zealand pasture soils depend on land use. Agriculture, Ecosystems & Environment 139(4), 611-617.
| Crossref | Google Scholar |

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75(23), 7537-7541.
| Crossref | Google Scholar | PubMed |

Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences 109(16), 6241-6246.
| Crossref | Google Scholar |

Shirkavand E, Baroutian S, Gapes DJ, Young BR (2016) Combination of fungal and physicochemical processes for lignocellulosic biomass pretreatment – a review. Renewable and Sustainable Energy Reviews 54, 217-234.
| Crossref | Google Scholar |

Soussana J-F, Lemaire G (2014) Coupling carbon and nitrogen cycles for environmentally sustainable intensification of grasslands and crop-livestock systems. Agriculture, Ecosystems & Environment 190, 9-17.
| Crossref | Google Scholar |

Suhara H, Kodama S, Kamei I, Maekawa N, Meguro S (2012) Screening of selective lignin-degrading basidiomycetes and biological pretreatment for enzymatic hydrolysis of bamboo culms. International Biodeterioration & Biodegradation 75, 176-180.
| Crossref | Google Scholar |

Sánchez Márquez S, Bills GF, Dominguez Acuña L, Zabalgogeazcoa I (2010) Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Diversity 41(1), 115-123.
| Crossref | Google Scholar |

Takashima Y, Narisawa K, Hidayat I, Rahayu G (2014) First report on fungal symbionts of Lycopodiaceae root from Mount Gede Pangrango National Park Indonesia. Journal of Developments in Sustainable Agriculture 9, 81-88.
| Crossref | Google Scholar |

Tamaki H, Tanaka Y, Matsuzawa H, Muramatsu M, Meng X-Y, Hanada S, et al. (2011) Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10. International Journal of Systematic and Evolutionary Microbiology 61(6), 1442-1447.
| Crossref | Google Scholar |

Terrill TH, Rowan AM, Douglas GB, Barry TN (1992) Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. Journal of the Science of Food and Agriculture 58(3), 321-329.
| Crossref | Google Scholar |

Toda T, Hyakumachi M, Suga H, Kageyama K, Tanaka A, Tani T (1999) Differentiation of Rhizoctonia AG-D isolates from turfgrass into subgroups I and II based on rDNA and RAPD analyses. European Journal of Plant Pathology 105, 835-846.
| Crossref | Google Scholar |

Tomazelli D, Klauberg-Filho O, Mendes SDC, Baldissera TC, Garagorry FC, Tsai SM, Pinto CE, Mendes LW, Goss-Souza D (2023) Pasture management intensification shifts the soil microbiome composition and ecosystem functions. Agriculture, Ecosystems & Environment 346(11), 108355.
| Crossref | Google Scholar |

Tomme P, Driver DP, Amandoron EA, Miller RC, Jr, Antony R, Warren J, et al. (1995) Comparison of a fungal (family I) and bacterial (family II) cellulose-binding domain. Journal of Bacteriology 177(15), 4356-4363.
| Crossref | Google Scholar | PubMed |

Tuzimura K, Watanabe I (1962) The effect of rhizosphere of various plants on the growth of Rhizobium. Soil Science and Plant Nutrition 8(4), 13-17.
| Crossref | Google Scholar |

Uhde-Stone C, Zinn KE, Ramirez-Yañez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiology 131(3), 1064-1079.
| Crossref | Google Scholar | PubMed |

van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11(3), 296-310.
| Crossref | Google Scholar | PubMed |

van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews 37(4), 477-494.
| Crossref | Google Scholar | PubMed |

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 and Soil 422(1-2), 267-281.
| Crossref | Google Scholar |

Vogel J (2008) Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11(3), 301-307.
| Crossref | Google Scholar | PubMed |

Wakelin S, Harrison S, Mander C, Dignam B, Rasmussen S, Monk S, Fraser K, O’Callaghan M (2015) Impacts of endophyte infection of ryegrass on rhizosphere metabolome and microbial community. Crop & Pasture Science 66(10), 1049-1057.
| Crossref | Google Scholar |

Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73(16), 5261-5267.
| Crossref | Google Scholar | PubMed |

Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304(5677), 1629-1633.
| Crossref | Google Scholar | PubMed |

Weiß M, Waller F, Zuccaro A, Selosse M-A (2016) Sebacinales – one thousand and one interactions with land plants. New Phytologist 211(1), 20-40.
| Crossref | Google Scholar | PubMed |

Wemheuer F, Kaiser K, Karlovsky P, Daniel R, Vidal S, Wemheuer B (2017) Bacterial endophyte communities of three agricultural important grass species differ in their response towards management regimes. Scientific Reports 7, 40914.
| Crossref | Google Scholar | PubMed |

Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biology and Biochemistry 33(12-13), 1723-1732.
| Crossref | Google Scholar |

Yang Z, Jin Y, Hou F, Bowatte S (2021) Soil microbial and chemical responses to foliar Epichloë fungal infection in Lolium perenne, Hordeum brevisubulatum and Achnatherum inebrians. Fungal Ecology 53, 101091.
| Crossref | Google Scholar |

Yeager CM, Gallegos-Graves LV, Dunbar J, Hesse CN, Daligault H, Kuske CR (2017) Polysaccharide degradation capability of Actinomycetales soil isolates from a semiarid grassland of the Colorado Plateau. Applied and Environmental Microbiology 83(6), e03020–16.
| Crossref | Google Scholar | PubMed |

Yoon J, Matsuo Y, Adachi K, Nozawa M, Matsuda S, Kasai H, et al. (2008) Description of Persicirhabdus sediminis gen. nov., sp. nov., Roseibacillus ishigakijimensis gen. nov., sp. nov., Roseibacillus ponti sp. nov., Roseibacillus persicicus sp. nov., Luteolibacter pohnpeiensis gen. nov., sp. nov. and Luteolibacter algae sp. nov., six marine members of the phylum ‘Verrucomicrobia’, and emended descriptions of the class Verrucomicrobiae, the order Verrucomicrobiales and the family Verrucomicrobiaceae. International Journal of Systematic and Evolutionary Microbiology 58(4), 998-1007.
| Crossref | Google Scholar |

Young IM, Crawford JW (2004) Interactions and self-organization in the soil-microbe complex. Science 304(5677), 1634-1637.
| Crossref | Google Scholar | PubMed |

Yu Y, Zheng L, Zhou Y, Sang W, Zhao J, Liu L, et al. (2021) Changes in soil microbial community structure and function following degradation in a temperate grassland. Journal of Plant Ecology 14(3), 384-397.
| Crossref | Google Scholar |

Zahid MI, Gurr GM, Nikandrow A, Fulkerson WJ, Nicol HI (2001) Pathogenicity of root and stolon-colonising fungi to white clover. Australian Journal of Experimental Agriculture 41(6), 763-771.
| Crossref | Google Scholar |

Zak DR, Pregitzer KS, Burton AJ, Edwards IP, Kellner H (2011) Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems. Fungal Ecology 4, 386-395.
| Crossref | Google Scholar |

Zhong R, Zhang L, Zhang X (2022) Allelopathic effects of foliar Epichloë endophytes on belowground arbuscular mycorrhizal fungi: a meta-analysis. Agriculture 12(11), 1768.
| Crossref | Google Scholar |

Zhou Y, Zhu H, Fu S, Yao Q (2017) Variation in soil microbial community structure associated with different legume species is greater than that associated with different grass species. Frontiers in Microbiology 8, 1007.
| Crossref | Google Scholar |