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RESEARCH ARTICLE (Open Access)

Effect of Epichloë gansuensis endophyte on rhizosphere bacterial communities and nutrient concentrations and ratios in the perennial grass species Achnatherum inebrians during three growth seasons

Wenpeng Hou https://orcid.org/0000-0003-0335-7796 A , Chao Xia A , Michael J. Christensen B , Jianfeng Wang A D , Xiuzhang Li A C , Tao Chen A and Zhibiao Nan A
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Grassland Agro-ecosystems Lanzhou University; Center for Grassland Microbiome; Key Laboratory of Grassland Livestock Industry Innovation (Ministry of Agriculture and Rural Affairs); Engineering Research Center of Grassland Industry (Ministry of Education); College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, Gansu 730000, PR China.

B Retired from AgResearch, Grasslands Research Centre, Private Bag 11-008, Palmerston North 4442, New Zealand.

C State Key Laboratory of Plateau Ecology and Agriculture, Qinghai Academy of Animal and Veterinary Sciences, Qinghai University, Xining, Qinghai 810016, PR China.

D Corresponding author. Email: wangjf12@lzu.edu.cn

Crop and Pasture Science 71(12) 1050-1066 https://doi.org/10.1071/CP20145
Submitted: 4 May 2020  Accepted: 29 October 2020   Published: 7 December 2020

Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND

Abstract

Achnatherum inebrians is an invasive perennial grass widespread in natural grasslands of north-west China and plays an important role in grassland ecological restoration. The presence of the seed-borne endophytic fungus Epichloë gansuensis in A. inebrians promotes grass growth, increases resistance to abiotic stress, and affects the rhizosphere microbial community of host plants. However, the relationships among E. gansuensis, rhizosphere bacteria and plant contents of carbon (C), nitrogen (N), phosphorus (P) and potassium (K) during different growing seasons are not clear. We examined changes in the rhizosphere bacterial community and in nutrient contents and ratios in A. inebrians with (E+) and without (E−) E. gansuensis in May, August and December. The Shannon diversity index was higher for rhizosphere bacteria of E+ than E− plants in the three different seasons. Leaf C, N and P contents and root P and K contents were higher in E+ than E− plants in May, and leaf K and root C were higher in E+ than E− plants in August. Leaf C : N ratios were lower in E+ than E− plants in December, and leaf C : K ratios were lower in E+ than E− plants in August and December. In addition, our results indicate significant interactions among rhizosphere bacteria, C, N, P and K contents, and endophyte treatment in three different seasons. In conclusion, E. gansuensis enhanced the C, N, P and K contents of host plants, and affected nutrient ratios of A. inebrians probably by increasing rhizosphere bacterial diversity and altering rhizosphere bacterial community structure. This study provides new findings on the ecological function of the endophyte E. gansuensis, including its potential role in enhancing soil fertility. The improvements in soil fertility were utilised in extrapolating to forage grass–endophyte associations.

Keywords: different growth phase, endophyte, rhizosphere bacterial diversity, stoichiometry.


References

Abbasi MK, Sharif S, Kazmi M, Sultan T, Aslam M (2011) Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants. Plant Biosystems 145, 159–168.
Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants.Crossref | GoogleScholarGoogle Scholar |

Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annual Review of Ecology, Evolution, and Systematics 39, 153–170.
Stoichiometry and nutrition of plant growth in natural communities.Crossref | GoogleScholarGoogle Scholar |

Bansal OP, Singh G, Katiyar P (2014) Effect of untreated sewage effluent irrigation on heavy metal content, microbial population and enzymatic activities of soils in Aligarh. Journal of Environmental Biology 35, 641–647.

Bao AK, Du BQ, Touil L, Kang P, Wang QL, Wang SM (2016) Co-expression of tonoplast Cation/H+ antiporter and H+-pyrophosphatase from xerophyte Zygophyllum xanthoxylum improves alfalfa plant growth under salinity, drought and field conditions. Plant Biotechnology Journal 14, 964–975.
Co-expression of tonoplast Cation/H+ antiporter and H+-pyrophosphatase from xerophyte Zygophyllum xanthoxylum improves alfalfa plant growth under salinity, drought and field conditions.Crossref | GoogleScholarGoogle Scholar | 26268400PubMed |

Basak BB, Biswas DR (2009) Influence of potassium solubilizing microorganism (Bacillus mucilaginosus) and waste mica on potassium uptake dynamics by sudan grass (Sorghum vulgare Pers.) grown under two Alfisols. Plant and Soil 317, 235–255.
Influence of potassium solubilizing microorganism (Bacillus mucilaginosus) and waste mica on potassium uptake dynamics by sudan grass (Sorghum vulgare Pers.) grown under two Alfisols.Crossref | GoogleScholarGoogle Scholar |

Bell CW, Asao S, Calderon F, Wolk B, Wallenstein MD (2015) Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth. Soil Biology & Biochemistry 85, 170–182.
Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth.Crossref | GoogleScholarGoogle Scholar |

Burke IC, Lauenroth WK, Vinton MA, Hook PB, Kelly RH, Epstein HE, Aguiar MR, Robles MD, Aguilera MO, Murphy KL (1998) Plant–soil interactions in temperate grasslands. Biogeochemistry 42, 121–143.
Plant–soil interactions in temperate grasslands.Crossref | GoogleScholarGoogle Scholar |

Calvo P, Watts DB, Kloepper JW, Torbert HA (2017) Effect of microbial-based inoculants on nutrient concentrations and early root morphology of corn (Zea mays). Journal of Plant Nutrition and Soil Science 180, 56–70.
Effect of microbial-based inoculants on nutrient concentrations and early root morphology of corn (Zea mays).Crossref | GoogleScholarGoogle Scholar |

Canbolat MY, Bilen S, Çakmakçı R, Şahin F, Aydın A (2006) Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biology and Fertility of Soils 42, 350–357.
Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora.Crossref | GoogleScholarGoogle Scholar |

Cassman KG (1999) Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. Proceedings of the National Academy of Sciences of the United States of America 96, 5952–5959.
Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture.Crossref | GoogleScholarGoogle Scholar | 10339523PubMed |

Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytologist 169, 27–34.
Plants actively control nitrogen cycling: uncorking the microbial bottleneck.Crossref | GoogleScholarGoogle Scholar | 16390416PubMed |

Chen L, Li X, Swoboda GA, Young CA, Sugawara K, Leuchtmann A, Schardl CL (2015) Two distinct Epichloë species symbiotic with Achnatherum inebrians, drunken horse grass. Mycologia 107, 863–873.

Chen N, He RL, Chai Q, Li CJ, Nan ZB (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regulation 80, 367–375.
Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians.Crossref | GoogleScholarGoogle Scholar |

Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics and Biology 45, 84–93.
Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves.Crossref | GoogleScholarGoogle Scholar | 17919950PubMed |

De Deyn GB, Raaijmakers CE, Ruijven JV, Berendse F, Putten WHVD (2004) Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106, 576–586.
Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web.Crossref | GoogleScholarGoogle Scholar |

De Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biology and Fertility of Soils 24, 358–364.
Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |

Dotaniya ML, Meena VD (2015) Rhizosphere effect on nutrient availability in soil and its uptake by plants: a review. Proceedings of the National Academy of Sciences. India. Section B, Biological Sciences 85, 1–12.
Rhizosphere effect on nutrient availability in soil and its uptake by plants: a review.Crossref | GoogleScholarGoogle Scholar |

Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Applied Soil Ecology 36, 184–189.
The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils.Crossref | GoogleScholarGoogle Scholar |

Egamberdiyeva D, Höflich G (2004) Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. Journal of Arid Environments 56, 293–301.
Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan.Crossref | GoogleScholarGoogle Scholar |

Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant–soil system. Annual Review of Environment and Resources 30, 75–115.
Feedback in the plant–soil system.Crossref | GoogleScholarGoogle Scholar |

Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N: P stoichiometry: toward a unified view of cellular and ecosystem processes. Bioscience 46, 674–684.
Organism size, life history, and N: P stoichiometry: toward a unified view of cellular and ecosystem processes.Crossref | GoogleScholarGoogle Scholar |

Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist 186, 593–608.
Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change.Crossref | GoogleScholarGoogle Scholar | 20298486PubMed |

Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, Knight R, Gilbert JA, McCulley RL (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the united states. Science 342, 621–624.
Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the united states.Crossref | GoogleScholarGoogle Scholar | 24179225PubMed |

Franzluebbers AJ, Nazih N, Stuedemann JA, Fuhrmann JJ, Schomberg HH, Hartel PG (1999) Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue. Soil Science Society of America Journal 63, 1687–1694.
Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue.Crossref | GoogleScholarGoogle Scholar |

Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012, 1–15.
Plant growth-promoting bacteria: mechanisms and applications.Crossref | GoogleScholarGoogle Scholar |

Gong X, Liu C, Li J, Luo Y, Yang Q, Zhang W, Yang P, Feng B (2019) Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China. Soil & Tillage Research 195, 104355
Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China.Crossref | GoogleScholarGoogle Scholar |

Govindasamy V, Senthilkumar M, Mageshwaran V, Annapurna K (2009) Detection and characterization of ACC deaminase in plant growth promoting rhizobacteria. Journal of Plant Biochemistry and Biotechnology 18, 71–76.
Detection and characterization of ACC deaminase in plant growth promoting rhizobacteria.Crossref | GoogleScholarGoogle Scholar |

Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biology & Biochemistry 30, 369–378.
Selective influence of plant species on microbial diversity in the rhizosphere.Crossref | GoogleScholarGoogle Scholar |

Guo JQ (2014) The influence of tall fescue cultivar and endophyte status on root exudate chemistry and rhizosphere processes. PhD Thesis, University of Kentucky, Lexington, KY, USA.

Höflich G, Wiehe W, Hecht-Buchholz C (1995) Rhizosphere colonization of different crops with growth promoting Pseudomonas and Rhizobium bacteria. Microbiological Research 150, 139–147.
Rhizosphere colonization of different crops with growth promoting Pseudomonas and Rhizobium bacteria.Crossref | GoogleScholarGoogle Scholar |

Horwath WR, Elliott LF, Lynch JM (1998) Influence of soil quality on the function of inhibitory rhizobacteria. Letters in Applied Microbiology 26, 87–92.
Influence of soil quality on the function of inhibitory rhizobacteria.Crossref | GoogleScholarGoogle Scholar |

Hou WP, Wang JF, Nan ZB, Christensen MJ, Xia C, Chen T, Zhang ZX, Niu XL (2020) Epichloë gansuensis endophyte-infection alters soil enzymes activity and soil nutrients at different growth stages of Achnatherum inebrians. Plant and Soil
Epichloë gansuensis endophyte-infection alters soil enzymes activity and soil nutrients at different growth stages of Achnatherum inebrians.Crossref | GoogleScholarGoogle Scholar |

Houlden A, Timmswilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiology Ecology 65, 193–201.
Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops.Crossref | GoogleScholarGoogle Scholar | 18616582PubMed |

Huitu O, Forbes KM, Helander M, Julkunen-Tiitto R, Lambin X, Saikkonen K, Stuart P, Sulkama S, Hartley S (2014) Silicon, endophytes and secondary metabolites as grass defenses against mammalian herbivores. Frontiers in Plant Science 5, 478
Silicon, endophytes and secondary metabolites as grass defenses against mammalian herbivores.Crossref | GoogleScholarGoogle Scholar | 25278951PubMed |

Ibekwe AM, Kennedy AC (1998) Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions. FEMS Microbiology Ecology 26, 151–163.
Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions.Crossref | GoogleScholarGoogle Scholar |

Inceoglu O, Salles JF, van Overbeek L, van Elsas JD (2010) Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Applied and Environmental Microbiology 76, 3675–3684.
Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields.Crossref | GoogleScholarGoogle Scholar | 20363788PubMed |

Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biology and Fertility of Soils 40, 7–13.
The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility.Crossref | GoogleScholarGoogle Scholar |

Ju YW, Zhong R, Christensen MJ, Zhang XX (2020) Effects of Epichloë gansuensis endophyte on the root and rhizosphere soil bacteria of Achnatherum inebrians under different moisture conditions. Frontiers in Microbiology 11,
Effects of Epichloë gansuensis endophyte on the root and rhizosphere soil bacteria of Achnatherum inebrians under different moisture conditions.Crossref | GoogleScholarGoogle Scholar |

Kennedy N, Connolly J, Clipson N (2005) Impact of lime, nitrogen and plant species on fungal community structure in grassland microcosms. Environmental Microbiology 7, 780–788.
Impact of lime, nitrogen and plant species on fungal community structure in grassland microcosms.Crossref | GoogleScholarGoogle Scholar | 15892697PubMed |

Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70.
Feedback with soil biota contributes to plant rarity and invasiveness in communities.Crossref | GoogleScholarGoogle Scholar | 11986666PubMed |

Koerselman W, Meuleman AF (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33, 1441–1450.
The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation.Crossref | GoogleScholarGoogle Scholar |

Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152–3166.
Exotic plant species alter the microbial community structure and function in the soil.Crossref | GoogleScholarGoogle Scholar |

Latour X, Philippot L, Corberand T, Lemanceau P (1999) The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. FEMS Microbiology Ecology 30, 163–170.
The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type.Crossref | GoogleScholarGoogle Scholar | 10508941PubMed |

Li X (2017) Study on the evolution and interactions of Epichloë gansuensis with host seed-borne fungi and rhizospheric microorganism. PhD Thesis, Lanzhou University, Lanzhou, Gansu, China.

Li CJ, Nan ZB, Paul VH, Dapprich PD, Liu Y (2004a) A new Neotyphodium species symbiotic with drunken horse grass (Achnatherum inebrians) in China. Mycotaxon 90, 141–147.

Li CJ, Nan ZB, Gao JH, Tian P (2004b) Detection and distribution of NeotyphodiumAchnatherum inebrians association in China. In ‘Proceedings of 5th International Neotyphodium/Grass Interactions Symposium’. 23–26 May, 2004 Fayetteville, AR, USA. (Eds R Kallenbach, C Rosenkrans, T Ryan Loch)

Li CJ, Zhang XX, Li F, Nan ZB, Schardl CL (2007) Disease and pests resistance of endophyte infected and non-infected drunken horse grass. In ‘Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses’. 25–28 March 2007, Christchurch, New Zealand, (Eds AJ Popay, ER Thom) (New Zealand Grassland Association: Dunedin, New Zealand)

Li X, Ren A, Han R, Yin LJ, Wei MY, Gao YB (2012) Endophyte-mediated effects on the growth and physiology of Achnatherum sibiricum are conditional on both N and P availability. PLoS One 7, e48010
Endophyte-mediated effects on the growth and physiology of Achnatherum sibiricum are conditional on both N and P availability.Crossref | GoogleScholarGoogle Scholar | 23300928PubMed |

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 Science 33, 1306–1314.

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. Functional Ecology 25, 910–920.
Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content.Crossref | GoogleScholarGoogle Scholar |

Lupwayi NZ, Rice WA, Clayton GW (1998) Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation. Soil Biology & Biochemistry 30, 1733–1741.
Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation.Crossref | GoogleScholarGoogle Scholar |

Lyons PC, Evans JJ, Bacon CW (1990) Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue. Plant Physiology 92, 726–732.
Effects of the fungal endophyte Acremonium coenophialum on nitrogen accumulation and metabolism in tall fescue.Crossref | GoogleScholarGoogle Scholar | 16667341PubMed |

Maarastawi SA, Frindte K, Linnartz M, Knief C (2018) Crop rotation and straw application impact microbial communities in Italian and Philippine soils and the rhizosphere of Zea mays. Frontiers in Microbiology 9, 1295
Crop rotation and straw application impact microbial communities in Italian and Philippine soils and the rhizosphere of Zea mays.Crossref | GoogleScholarGoogle Scholar | 29963033PubMed |

Main TM, Dobberfuhl DR, Elser JJ (1997) N:P stoichiometry and ontogeny of crustacean zooplankton: a test of the growth rate hypothesis. Limnology and Oceanography 42, 1474–1478.
N:P stoichiometry and ontogeny of crustacean zooplankton: a test of the growth rate hypothesis.Crossref | GoogleScholarGoogle Scholar |

Malinowski D, Brauer D, Belesky D (1999) The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency. Journal Agronomy & Crop Science 183, 53–60.
The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar |

Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant and Soil 227, 115–126.
Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue.Crossref | GoogleScholarGoogle Scholar |

Man Y, Wang JX, Tam NF, Wan X, Huang WD, Zheng Y, Tang JP, Tao R, Yang Y (2020) Responses of rhizosphere and bulk substrate microbiome to wastewater-borne sulfonamides in constructed wetlands with different plant species. The Science of the Total Environment 706, 135955
Responses of rhizosphere and bulk substrate microbiome to wastewater-borne sulfonamides in constructed wetlands with different plant species.Crossref | GoogleScholarGoogle Scholar | 31855648PubMed |

Marschner P (2012) ‘Marschner’s mineral nutrition of higher plants.’ 2nd edn. (Academic Press: Cambridge, MA, USA)

Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant and Soil 261, 199–208.
Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type.Crossref | GoogleScholarGoogle Scholar |

Meena VS, Meena SK, Verma JP, Kumar A, Aeron A, Mishra PK, Bisht JK, Pattanayak A, Naveed M, Dotaniya ML (2017) Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecological Engineering 107, 8–32.
Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review.Crossref | GoogleScholarGoogle Scholar |

Miller HJ, Henken G, van Veen JA (1989) Variation and composition of bacterial populations in the rhizospheres of maize, wheat, and grass cultivars. Canadian Journal of Microbiology 35, 656–660.
Variation and composition of bacterial populations in the rhizospheres of maize, wheat, and grass cultivars.Crossref | GoogleScholarGoogle Scholar |

Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Archives of Microbiology 193, 77–81.
Arbuscular mycorrhizal fungi and nitrogen uptake.Crossref | GoogleScholarGoogle Scholar | 21136040PubMed |

Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Current Opinion in Plant Biology 8, 450–456.
Symbiosis between grasses and asexual fungal endophytes.Crossref | GoogleScholarGoogle Scholar | 15946893PubMed |

Nan ZB, Li CJ (2004) Roles of the grass–Neotyphodium association in pastoral agriculture systems. Acta Ecologica Sinica 24, 605–616.

Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnologie, Agronomie, Société et Environnement 15, 327–337.

Niklas KJ, Cobb ED (2006) Biomass partitioning and leaf N, P-stoichiometry: comparisons between tree and herbaceous current-year shoots. Plant, Cell & Environment 29, 2030–2042.
Biomass partitioning and leaf N, P-stoichiometry: comparisons between tree and herbaceous current-year shoots.Crossref | GoogleScholarGoogle Scholar |

Ollivier J, Töwe S, Bannert A, Hai B, Kastl EM, Meyer A, Su MX, Kleineidam K, Schloter M (2011) Nitrogen turnover in soil and global change. FEMS Microbiology Ecology 78, 3–16.
Nitrogen turnover in soil and global change.Crossref | GoogleScholarGoogle Scholar | 21707675PubMed |

Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biology and Fertility of Soils 51, 403–415.
Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review.Crossref | GoogleScholarGoogle Scholar |

Qiao QH, Wang FR, Zhang JX, Chen Y, Zhang CY, Liu GD, Zhang H, Ma CL, Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Scientific Reports 7, 3940
The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage.Crossref | GoogleScholarGoogle Scholar |

Reed SC, Townsend AR, Davidson EA, Cleveland CC (2012) Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytologist 196, 173–180.
Stoichiometric patterns in foliar nutrient resorption across multiple scales.Crossref | GoogleScholarGoogle Scholar | 22882279PubMed |

Reef R, Ball MC, Feller IC, Lovelock CE (2010) Relationships among RNA:DNA ratio, growth and elemental stoichiometry in mangrove trees. Functional Ecology 24, 1064–1072.
Relationships among RNA:DNA ratio, growth and elemental stoichiometry in mangrove trees.Crossref | GoogleScholarGoogle Scholar |

Reza SM, Mirlohi A (2010) Neotyphodium endophytes trigger salt resistance in tall and meadow fescues. Journal of Plant Nutrition and Soil Science 173, 952–957.
Neotyphodium endophytes trigger salt resistance in tall and meadow fescues.Crossref | GoogleScholarGoogle Scholar |

Richardson MD, Cabrera RI, Murphy JA, Zaurov DE (1999) Nitrogen‐form and endophyte‐infection effects on growth, nitrogen uptake, and alkaloid content of chewings fescue turf grass. Journal of Plant Nutrition 22, 67–79.
Nitrogen‐form and endophyte‐infection effects on growth, nitrogen uptake, and alkaloid content of chewings fescue turf grass.Crossref | GoogleScholarGoogle Scholar |

Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proceedings of the National Academy of Sciences of the United States of America 109, 4181–4186.
Strong relationship between elemental stoichiometry and metabolome in plants.Crossref | GoogleScholarGoogle Scholar | 22371578PubMed |

Roesti D, Gaur R, Johri BN, Imfeld G, Sharma S, Kawaljeet K, Aragno M (2006) Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields. Soil Biology & Biochemistry 38, 1111–1120.
Plant growth stage, fertiliser management and bio-inoculation of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields.Crossref | GoogleScholarGoogle Scholar |

Rojas X, Guo J, Leff JW, McNear DH, Fierer N, McCulley RL (2016) Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities. Microbial Ecology 72, 197–206.
Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities.Crossref | GoogleScholarGoogle Scholar | 26992401PubMed |

Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant and Soil 268, 285–292.
Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annual Review of Plant Biology 55, 315–340.
Symbioses of grasses with seedborne fungal endophytes.Crossref | GoogleScholarGoogle Scholar | 15377223PubMed |

Schlatter DC, Hansen JC, Schillinger WF, Sullivan TS, Paulitz TC (2019) Common and unique rhizosphere microbial communities of wheat and canola in a semiarid Mediterranean environment. Applied Soil Ecology 144, 170–181.
Common and unique rhizosphere microbial communities of wheat and canola in a semiarid Mediterranean environment.Crossref | GoogleScholarGoogle Scholar |

Song ML, Chai Q, Li XZ, Yao X, Li CJ, Christensen MJ, Nan ZB (2015a) An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant and Soil 387, 153–165.
An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress.Crossref | GoogleScholarGoogle Scholar |

Song ML, Li X, Saikkonen K, Li CJ, Nan ZB (2015b) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecology 13, 44–52.
An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum.Crossref | GoogleScholarGoogle Scholar |

Sparks D, Bartels J (1996) Chemical methods. In ‘Methods of soil analysis’. (Soil Science Society of America: Madison, WI, USA)

Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Journal of Plankton Research 9, 9

Su YY, Guo LD, Hyde KD (2010) Response of endophytic fungi of stipa grandis to experimental plant function group removal in Inner Mongolia steppe, China. Fungal Diversity 43, 93–101.
Response of endophytic fungi of stipa grandis to experimental plant function group removal in Inner Mongolia steppe, China.Crossref | GoogleScholarGoogle Scholar |

Tian ZP, Wang RY, Ambrose KV, Clarke BB, Belanger FC (2017) The Epichloë festucae antifungal protein has activity against the plant pathogen Sclerotinia homoeocarpa, the causal agent of dollar spot disease. Scientific Reports 7, 5643
The Epichloë festucae antifungal protein has activity against the plant pathogen Sclerotinia homoeocarpa, the causal agent of dollar spot disease.Crossref | GoogleScholarGoogle Scholar |

Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418, 671
Agricultural sustainability and intensive production practices.Crossref | GoogleScholarGoogle Scholar | 12167873PubMed |

Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JP (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Molecular Ecology 12, 3085–3095.
Co-existing grass species have distinctive arbuscular mycorrhizal communities.Crossref | GoogleScholarGoogle Scholar | 14629388PubMed |

Wang JF, Zhang YQ, Li Y, Wang XM, Nan WB, Hu YF, Zhang H, Zhao CZ, Wang F, Li P, Shi HY, Bi YR (2015) Endophytic microbes Bacillus sp. LZR216-regulated root development is dependent on polar auxin transport in Arabidopsis seedlings. Plant Cell Reports 34, 1075–1087.
Endophytic microbes Bacillus sp. LZR216-regulated root development is dependent on polar auxin transport in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |

Wang JF, Nan ZB, Christensen MJ, Li CJ (2018a) Glucose-6-phosphate dehydrogenase plays a vital role in Achnatherum inebrians plants host to Epichloë gansuensis by improving growth under nitrogen deficiency. Plant and Soil 430, 37–48.
Glucose-6-phosphate dehydrogenase plays a vital role in Achnatherum inebrians plants host to Epichloë gansuensis by improving growth under nitrogen deficiency.Crossref | GoogleScholarGoogle Scholar |

Wang JF, Nan ZB, Christensen MJ, Zhang XX, Tian P, Zhang ZX, Niu XL, Gao P, Chen T, Ma LX (2018b) Effect of Epichloë gansuensis endophyte on the nitrogen metabolism, nitrogen use efficiency, and stoichiometry of Achnatherum inebrians under nitrogen limitation. Journal of Agricultural and Food Chemistry 66, 4022–4031.
Effect of Epichloë gansuensis endophyte on the nitrogen metabolism, nitrogen use efficiency, and stoichiometry of Achnatherum inebrians under nitrogen limitation.Crossref | GoogleScholarGoogle Scholar |

Wang JF, Tian P, Christensen MJ, Zhang XX, Li CJ, Nan ZB (2019) 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 and Soil 435, 57–68.
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.Crossref | GoogleScholarGoogle Scholar |

Wang JF, Hou WP, Christensen MJ, Xia C, Chen T, Zhang ZX, Nan ZB (2020a) The fungal endophyte Epichloë gansuensis increases NaCl-tolerance in Achnatherum inebrians through enhancing the activity of plasma membrane H+-ATPase and glucose-6-phosphate dehydrogenase. Science China. Life Sciences
The fungal endophyte Epichloë gansuensis increases NaCl-tolerance in Achnatherum inebrians through enhancing the activity of plasma membrane H+-ATPase and glucose-6-phosphate dehydrogenase.Crossref | GoogleScholarGoogle Scholar |

Wang JJ, Li RC, Zhang H, Wei GH, Li ZF (2020b) Beneficial bacteria activate nutrients and promote wheat growth under conditions of reduced fertilizer application. BMC Microbiology 20, 38
Beneficial bacteria activate nutrients and promote wheat growth under conditions of reduced fertilizer application.Crossref | GoogleScholarGoogle Scholar |

Wang JF, Hou WP, Christensen MJ, Li XZ, Xia C, Li CJ, Nan ZB (2020c) Role of Epichloë endophytes in improving host grass resistance ability and soil properties. Journal of Agricultural and Food Chemistry 68, 6944–6955.
Role of Epichloë endophytes in improving host grass resistance ability and soil properties.Crossref | GoogleScholarGoogle Scholar |

Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecological Monographs 69, 535–568.
Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties.Crossref | GoogleScholarGoogle Scholar |

Westover KM, Kennedy AC, Kelley SE (1997) Patterns of rhizosphere microbial community structure associated with co-occurring plant species. Journal of Ecology 85, 863–873.
Patterns of rhizosphere microbial community structure associated with co-occurring plant species.Crossref | GoogleScholarGoogle Scholar |

White RH, Engelke MC, Morton SJ, Johnson-Cicalese JM, Ruemmele BA (1992) Acremonium endophyte effects on tall fescue drought tolerance. Crop Science 32, 1392–1396.
Acremonium endophyte effects on tall fescue drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Xia C (2018) Responses of Epichloë gansuensis-Achnatherum inebrians symbiont to drought stress. PhD thesis, Lanzhou University, Lanzhou, China.

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 and Soil 424, 555–571.
Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit.Crossref | GoogleScholarGoogle Scholar |

Yang JW (2012) Study on soil microbial quantity, soil enzyme activity and physicochemical factor in various saline-alkali soil in Hexi Corridor. Master’s thesis, Northwest Normal University, Lanzhou, China.

Yang YH, Luo YQ (2011) Carbon: nitrogen stoichiometry in forest ecosystems during stand development. Global Ecology and Biogeography 20, 354–361.
Carbon: nitrogen stoichiometry in forest ecosystems during stand development.Crossref | GoogleScholarGoogle Scholar |

Yildirim E, Karlidag H, Turan M, Dursun A, Goktepe F (2011) Growth, nutrient uptake, and yield promotion of broccoli by plant growth promoting rhizobacteria with manure. HortScience 46, 932–936.

Zhang XB (2008) Study on microflora and characteristics of plant growth promoting rhizobacteria (PGPR) in rhizosphere of Kentucky bluegrass. PhD thesis, Beijing Forestry University, Beijing.

Zhang FS, Shen JB, Zhang JY, Zuo N, Li L, Chen XP (2010a) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China. Advances in Agronomy 107, 1–32.
Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China.Crossref | GoogleScholarGoogle Scholar |

Zhang XX, Li CJ, Nan ZB (2010b) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. Journal of Hazardous Materials 175, 703–709.
Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense.Crossref | GoogleScholarGoogle Scholar |

Zhang XX, Li CJ, Nan ZB, Matthew C (2012) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Research 52, 70–78.
Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators.Crossref | GoogleScholarGoogle Scholar |

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 Ecology 31, 29–36.
Effects of Epichloë gansuensis on root-associated fungal communities of Achnatherum inebrians under different growth conditions.Crossref | GoogleScholarGoogle Scholar |

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 Ecology 20, 56–65.
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.Crossref | GoogleScholarGoogle Scholar |

Ziegler M, Engel M, Welzl G, Schloter M (2013) Development of a simple root model to study the effects of single exudates on the development of bacterial community structure. Journal of Microbiological Methods 94, 30–36.
Development of a simple root model to study the effects of single exudates on the development of bacterial community structure.Crossref | GoogleScholarGoogle Scholar | 23611840PubMed |