Skip to main content

Advertisement

Log in

The relationship between root endophytic microbial of plant species and soil properties in different patches of alpine meadow

  • Ecology & Biogeography - Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Plants do not live alone as single entities but are closely associated with an incredible diversity of bacteria, fungi and other organisms. To explore the advantages of endophytes in controlling ecosystem responses to plant community succession, in this study, the Illumina MiSeq high-throughput sequencing technology was applied to characterize root endophytic microbials community structure composition and diversity variation in different patches of degraded alpine meadow. The relationship between root endophytic microbials of plant species and soil properties was analyzed. The results showed that the soil property values all decreased after K. humilis dominated alpine meadow community was replaced by A. tenuifolia, L. virgaurea and P. kansuensis dominated patches. Root endophytic fungi were little affected by soil pH and soil properties. Unlike the fungi, the plant species of root endophytic bacteria have been affected by different dominant plants or soil properties availability. Root endophytic bacteria were species richness, greater diversity and well correlated with soil pH and soil properties in phyla level. Positive and negative associations in the root endophytic microbiome were observed. Exploring and finding the method of plant–microbial joint restoration in the ecological restoration, so as to provide reference for the further study of plant endophytic microbial resources in alpine meadow.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The authors confirm that the data supporting the findings of this study are available within the article or some have been submitted to the NCBI BioProject.

References

  • Bao SD (2008) Soil agrochemical analysis (Third edition). China Agricultural Press, Beijing, pp 25–100

    Google Scholar 

  • Baxendale C, Orwin KH, Poly F, Pommier T, Bardgett RD (2014) Are plant–soil feedback responses explained by plant traits? New Phytol 204:408–423

    Article  PubMed  Google Scholar 

  • Burns RG, Pukite A, McLaren A (1972) Concerning the location and persistence of soil urease. Soil Sci Soc Am J 36:308–311

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175

    Article  Google Scholar 

  • Che RX, Wang F, Wang WJ, Zhang J, Zhao X, Rui YC, Xu ZH, Wang YF, Hao YB, Cui XY (2017) Increase in ammonia-oxidizing microbe abundance during degradation of alpine meadows may lead to greater soil nitrogen loss. Biogeochemistry 136:341–352

    Article  CAS  Google Scholar 

  • Che RX, Wang YF, Li KX, Xu ZH, Hu JM, Wang F, Rui YC, Li LF, Zhe P, Cui XY (2019) Degraded patch formation significantly changed microbial community composition in alpine meadow soils. Soil till Res 195:104426

    Article  Google Scholar 

  • Chen J, Yamamura Y, Hori Y, Shiyomi M, Yasuda T, Zhou HK, Li YN, Tang YH (2008) Small-scale species richness and its spatial variation in an alpine meadow on the Qinghai-Tibet Plateau. Ecol Res 23:657–663

    Article  Google Scholar 

  • Chen L, Brookes PC, Xu J, Zhang J, Zhang C, Zhou X, Luo Y (2016) Structural and functional differentiation of the root-associated bacterial microbiomes of perennial ryegrass. Soil Biol Biochem 98:1–10

    Article  CAS  Google Scholar 

  • Compant S, Saikkonen K, Mitter B, Campisano A, Mercado-Blanco J (2016) Editorial special issue: soil, plants and endophytes. Plant Soil 405:1–11

    Article  CAS  Google Scholar 

  • Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249

    Article  CAS  PubMed  Google Scholar 

  • Curd EE, Martiny JBH, Li H, Smith TB (2018) Bacterial diversity is positively correlated with soil heterogeneity. Ecosphere 9:e02079

    Article  Google Scholar 

  • Das SK, Varma A (2010) Role of enzymes in maintaining soil health. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 25–42

    Chapter  Google Scholar 

  • Deng SP, Tabatabai MA (1996a) Effect of tillage and residue management on enzyme activities in soils: I. Amidohydrolases. Biol Fertil Soils 22:202–207

    Article  CAS  Google Scholar 

  • Deng SP, Tabatabai MA (1996b) Effect of tillage and residue management on enzyme activities in soils: II. Glycosidases. Biol Fertil Soils 22:208–213

    Article  CAS  Google Scholar 

  • Deng SP, Tabatabai MA (1997) Effect of tillage and residue management on enzyme activities in soils: III. Phosphatases and arylsulfatase. Biol Fertil Soils 24:141–146

    Article  CAS  Google Scholar 

  • Ding T, Melcher U (2016) Influences of plant species, season and location on leaf endophytic bacterial communities of non-cultivated plants. PLoS ONE 11:e0150895

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong SK, Zhang J, Li YY, Liu SL, Dong QM, Zhou HK, Yeomans J, Li Y, Li S, Gao XX (2020) Effect of grassland degradation on aggregate-associated soil organic carbon of alpine grassland ecosystems in the Qinghai-Tibetan Plateau. Eur J Soil Sci 71:69–79

    CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci 112:E911–E920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadiji AE, Babalola OO (2020) Metagenomics methods for the study of plant-associated microbial communities: a review. J Microbiol Meth 170:105860

    Article  CAS  Google Scholar 

  • Fadiji AE, Ayangbenro AS, Babalola OO (2021) Unveiling the putative functional genes present in root-associated endophytic microbiome from maize plant using the shotgun approach. J Appl Genet 62:339–351

    Article  CAS  PubMed  Google Scholar 

  • Fan KK, Weisenhorn P, Gilbert JA, Shi Y, Bai Y, Chu HY (2018) Soil pH correlates with the co-occurrence and assemblage process of diazotrophic communities in rhizosphere and bulk soils of wheat fields. Soil Biol Biochem 121:185–192

    Article  CAS  Google Scholar 

  • Feng MM, Tripathi BM, Shi Y, Adams JM, Zhu YG, Chu HY (2019) Interpreting distance-decay pattern of soil bacteria via quantifying the assembly processes at multiple spatial scales. Microbiolgy Open 8:e00851

    Google Scholar 

  • Frouz J, Prach K, Pižl V, Háněl L, Starý J, Tajovský K, Materna J, Balik V, Kalčík J, Řehounková K (2008) Interactions between soil development, vegetation and soil fauna during spontaneous succession in post mining sites. Eur J Soil Biol 44:109–121

    Article  Google Scholar 

  • Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750

    Article  PubMed  Google Scholar 

  • Garbeva P, Van Elsas JD, Van Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32

    Article  CAS  Google Scholar 

  • Guo JX, Bowatte S, Hou FJ (2021) Diversity of endophytic bacteria and fungi in seeds of Elymus nutans growing in four locations of Qinghai Tibet Plateau, China. Plant Soil 459:49–63

    Article  CAS  Google Scholar 

  • Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The Hidden World within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 25:9106395

    Google Scholar 

  • Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14

    Article  CAS  Google Scholar 

  • Kjøller AH, Struwe S (2002) Fungal communities, succession, enzymes, and decomposition. Enzymes Environ: Activity, Ecol Appl 1:267–284

    Google Scholar 

  • Lanzén A, Epelde L, Blanco F, Martín I, Artetxe U, Garbisu C (2016) Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci Rep 6:28257

    Article  PubMed  PubMed Central  Google Scholar 

  • Li YY, Dong SK, Wen L, Wang XX, Wu Y (2014) Soil carbon and nitrogen pools and their relationship to plant and soil dynamics of degraded and artificially restored grasslands of the Qinghai-Tibetan Plateau. Geoderma 213:178–184

    Article  CAS  Google Scholar 

  • Li YM, Wang SP, Jiang LL, Zhang LR, Cui SJ, Meng FD, Wang Q, Li XN, Zhou Y (2016) Changes of soil microbial community under different degraded gradients of alpine meadow. Agric Ecosyst Environ 222:213–222

    Article  Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2:18–22

    Google Scholar 

  • Lin L, Li YK, Xu XL, Zhang FW, Du YG, Liu SL, Guo XW, Cao GM (2015) Predicting parameters of degradation succession processes of Tibetan Kobresia grasslands. Solid Earth 6:1237–1246

    Article  Google Scholar 

  • Liu Y, Wang RH, Li YH et al (2017) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of “Beijing” hybrid maize planted in China. Plant Growth Regul 81:317–324

    Article  CAS  Google Scholar 

  • Liu SB, Zamanian K, Schleuss PM, Zarebanadkouki M, Kuzyakov Y (2018) Degradation of Tibetan grasslands: consequences for carbon and nutrient cycles. Agric Ecosyst Environ 252:93–104

    Article  CAS  Google Scholar 

  • Liu Y, Li YM, Luo W, Liu S, Chen WM, Chen C, Jiao S, Wei GH (2020) Soil potassium is correlated with root secondary metabolites and root-associated core bacteria in licorice of different ages. Plant Soil 456:61–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YX, QinY CT et al (2021) A practical guide to amplicon and metagenomic analysis of microbiome data. Protein Cell 12:315–330

    Article  PubMed  Google Scholar 

  • Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  PubMed  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Nelson EB, Simoneau P, Barret M, Mitter B, Compant S (2018) Editorial special issue: The soil, the seed, the microbes and the plant. Plant Soil 422:1–5

    Article  CAS  Google Scholar 

  • Nicksy J, Entz MH (2021) Recycled nutrients as a phosphorus source for Canadian organic agriculture: a perspective. Can J Soil Sci 101:571–580

    Article  Google Scholar 

  • Omomowo OI, Babalola OO (2019) Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms 7:7110481

    Article  Google Scholar 

  • Philippot L, Raaijmakers JM, Lemanceau P, Van Der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  CAS  PubMed  Google Scholar 

  • Proença DN, Schwab S, Baldani JI, Morais PV (2017) Diversity and function of endophytic microbial community of plants with economical potential (Chapter10). Diversity and benefits of microorganisms from the tropics. Springer, Cham pp 209–243

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Shang ZH, Ma YS, Long RJ, Ding LM (2008) Effect of fencing, artificial seeding and abandonment on vegetation composition and dynamics of ‘black soil land’ in the headwaters of the Yangtze and the Yellow Rivers of the Qinghai-Tibetan Plateau. Land Degrad Dev 19:554–563

    Article  Google Scholar 

  • Shen CC, Shi Y, Fan KK, He JS, Adams JM, Ge Y, Chu HY (2019) Soil pH dominates elevational diversity pattern for bacteria in high elevation alkaline soils on the Tibetan Plateau. FEMS Microbiol Ecol 95:fiz003

    Article  CAS  Google Scholar 

  • Singh D, Shi LL, Adams JM (2013) Bacterial diversity in the mountains of south-west China: climate dominates over soil parameters. J Microbiol 51:439–447

    Article  CAS  PubMed  Google Scholar 

  • Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176

    Article  CAS  Google Scholar 

  • Tabatabai MA, Dick WA (2002) Enzymes in soil: research and developments in measuring activities. Enzymes Environ: Activity, Ecol Appl 567–596

  • Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459

    Article  CAS  PubMed  Google Scholar 

  • Teng YM, Zhan JY, Agyemang FB, Sun YX (2020) The effects of degradation on alpine grassland resilience: a study based on meta-analysis data. Glob Ecol Conserv 24:e01336

    Article  Google Scholar 

  • Thomas RL, Sheard RW, Moyer JR (1967) Comparison of conventional and automated procedures for nitrogen, phosphorus, and potassium analysis of plant material using a single digestion1. Agron J 59:240–243

    Article  CAS  Google Scholar 

  • 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. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Vincent RC, Meguro M (2008) Influence of soil properties on the abundance of plant species in ferruginous rocky soils vegetation, southeastern Brazil. Braz J Bot 31:377–388

    Article  Google Scholar 

  • Wang Q (2013) Effects of bamboo vinegar foliar fertilizer and soil conditioner on tomato yield and quality and soil nutrients. Anhui Agric Univ 54:336–345

    Google Scholar 

  • Wang Y, Dong JX, Zheng XB, Zhang JG, Zhou PL, Song XP, Song WJ, Wang SS (2021) Wheat straw and biochar effect on soil carbon fractions, enzyme activities, and nutrients in a tobacco field. Can J Soil Sci 101:353–364

    Article  CAS  Google Scholar 

  • Xia Q, Rufty T, Shi W (2020) Soil microbial diversity and composition: Links to soil texture and associated properties. Soil Biol Biochem 149:107953

    Article  CAS  Google Scholar 

  • Xiao X, Chen WM, Zong L, Yang J, Jiao S, Lin YB, Wang ET, Wei GH (2017) Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Mol Ecol 26:1641–1651

    Article  CAS  PubMed  Google Scholar 

  • Xie HH, Wu QG, Hu JY, Yu LF, Bie PF, Wang H, Deng DZ (2018) Changes in soil physical and chemical properties during the process of alpine meadow degradation along the eastern Qinghai-Tibet Plateau. Eurasian Soil Sci 51:1440–1446

    Article  CAS  Google Scholar 

  • Xu J, Zhang YZ, Zhang PF et al (2018a) The structure and function of the global citrus rhizosphere microbiome. Nat Commun 9:4894

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu S, Li P, Sayer EJ et al (2018b) Initial soil organic matter content influences the storage and turnover of litter, root and soil carbon in grasslands. J Ecosystems 21:1377–1389

    Article  CAS  Google Scholar 

  • Yan Y, Lu XY (2015) Is grazing exclusion effective in restoring vegetation in degraded alpine grasslands in Tibet, China? PeerJ 3:1020

    Article  Google Scholar 

  • Yi XS, Li GS, Yin YY (2012) The impacts of grassland vegetation degradation on soil hydrological and ecological effects in the source region of the Yellow River–A case study in Junmuchang region of Maqin country. Procedia Environ Sci 13:967–981

    Article  CAS  Google Scholar 

  • Zhou H, Zhang DG, Jiang ZH, Sun P, Xiao HL, Wu YX, Chen JG (2019) Changes in the soil microbial communities of alpine steppe at Qinghai-Tibetan Plateau under different degradation levels. Sci Total Environ 651:2281–2291

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant no. 31760691), the National Key Research and Development Program of China (grant no. 2017YFC05048003) and the Programme of Introducing Talents of Discipline to Universities (D18013). We are also thankful to our all laboratory colleagues and research staff members for their constructive advice and help.

Author information

Authors and Affiliations

Authors

Contributions

The manuscript was written through contributions of all authors. WZQ analyzed and interpreted data, designed the work and drafted the manuscript with input from all authors. CSL and BHX collected the field data and assisted in the interpretation it. CKX and WWZ helped in the interpretation of the data and assisted in the submission. MZ has participated in the manuscript revision. The last manuscript versions were reviewed and adjusted by QYM. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Youming Qiao.

Ethics declarations

Conflicts of interest

The authors declare that have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Chen, S., Ben, H. et al. The relationship between root endophytic microbial of plant species and soil properties in different patches of alpine meadow. Braz. J. Bot 46, 681–693 (2023). https://doi.org/10.1007/s40415-023-00907-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-023-00907-7

Keywords

Navigation