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Bio-fertilizer Amendment Alleviates the Replanting Disease under Consecutive Monoculture Regimes by Reshaping Leaf and Root Microbiome

Abstract

Replanting disease is a growing problem in intensive agricultural systems. Application of bio-fertilizer containing beneficial microbes contributes to disease suppression and is a promising strategy to control replanting disease. However, the effect of both replanting disease and bio-fertilizer amendment on the assembly of crop microbiota in leaves and roots and their relationships to crop yield and quality remains elusive. In these experiments, roots and leaves of Radix pseudostellariae were collected from different consecutive monoculture and bio-fertilizer amended fields, and the associated microbiota were characterized by bacterial 16S rRNA gene sequencing and quantitative PCR. Consecutive monoculture altered the bacterial community structure and composition and significantly increased the abundance of potential pathogenic Ralstonia and Fusarium oxysporum in leaves and roots. Furthermore, bio-fertilizer application alleviated replanting disease by decreasing the pathogen load, increasing the potential beneficial genera Pseudomonas, Streptomyces, Paenibacillus, and Bradyrhizobium. The proportion of positive correlations in the co-occurrence network of bio-fertilizer application was the highest, implying that bio-fertilizer potentially enhanced ecological commensalism or mutualism of the bacterial community across the two compartments. Structural equation models indicated that bio-fertilizer had a positive and indirect effect on both yield and quality by shaping the leaf microbiota and the root microbiota. Our findings highlight the role of leaf and root microbiota on replanting disease, showing that bio-fertilizer contributes to alleviating replanting disease by improving microbe–microbe interactions.

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Data Availability

All data generated or analyzed were included in this manuscript and the supporting information.

References

  1. 1.

    Altieri MA, Nicholls CI (2020) Agroecology and the reconstruction of a post-COVID-19 agriculture. J Peasant Stud 47:881–898. https://doi.org/10.1080/03066150.2020.1782891

    Article  Google Scholar 

  2. 2.

    Wu H, Wu H, Qin X, Lin M, Zhao Y, Rensing C, Lin W (2021) Replanting disease alters the faunal community composition and diversity in the rhizosphere soil of Radix pseudostellariae. Agr Ecosyst Environ 310:1–7

    Article  Google Scholar 

  3. 3.

    Wu H, Qin X, Wang J, Wu L, Chen J, Fan J, Zheng L, Tangtai H, Arafat Y, Lin W (2019) Rhizosphere responses to environmental conditions in Radix pseudostellariae under continuous monoculture regimes. Agr Ecosyst Environ 270:19–31

    Article  Google Scholar 

  4. 4.

    Li Y, Dai S, Wang B, Jiang Y, Ma Y, Pan L, Wu K, Huang X, Zhang J, Cai Z, Zhao J (2020) Autotoxic ginsenoside disrupts soil fungal microbiomes by stimulating potentially pathogenic microbes. Appl Environ Microbiol 86(9):e00130-20. https://doi.org/10.1128/aem.00130-20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Wu L, Yang B, Li M, Chen J, Xiao Z, Wu H, Tong Q, Luo X, Lin W (2019) Modification of rhizosphere bacterial community structure and functional potentials to control Pseudostellaria heterophylla replant disease. Plant Dis 104:25–24

    Article  Google Scholar 

  6. 6.

    Xiong W, Guo S, Jousset A, Zhao Q, Wu H, Li R, Kowalchuk GA, Shen Q (2017) Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem 114:238–247. https://doi.org/10.1016/j.soilbio.2017.07.016

    CAS  Article  Google Scholar 

  7. 7.

    Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, Ruan Y, Geisen S, Shen Q, Kowalchuk GA (2020) Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 8:137. https://doi.org/10.1186/s40168-020-00892-z

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, Shen Q (2017) Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem 104:39–48

    CAS  Article  Google Scholar 

  9. 9.

    Compant S, Mitter B, GualbertoColli-Mull J, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197. https://doi.org/10.1007/s00248-011-9883-y

    Article  PubMed  Google Scholar 

  10. 10.

    Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. In: Merchant, SS (ed.). Annual Review of Plant Biology 64:807–838

    CAS  Article  Google Scholar 

  11. 11.

    Zhang J, Zhang N, Liu Y-X, Zhang X, Hu B, Qin Y, Xu H, Wang H, Guo X, Qian J, Wang W, Zhang P, Jin T, Chu C, Bai Y (2018) Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61:613–621. https://doi.org/10.1007/s11427-018-9284-4

    Article  PubMed  Google Scholar 

  12. 12.

    Gong T, Xin X-F (2021) Phyllosphere microbiota: community dynamics and its interaction with plant hosts. J Integr Plant Biol 63:297–304. https://doi.org/10.1111/jipb.13060

    Article  PubMed  Google Scholar 

  13. 13.

    Chen T, Nomura K, Wang X, Sohrabi R, Xu J, Yao L, Paasch BC, Ma L, Kremer J, Cheng Y, Zhang L, Wang N, Wang E, Xin X-F, He SY (2020) A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580:653. https://doi.org/10.1038/s41586-020-2185-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Chaudhry V, Runge P, Sengupta P, Doehlemann G, Parker JE, Kemen E (2021) Shaping the leaf microbiota: plant-microbe-microbe interactions. J Exp Bot 72:36–56. https://doi.org/10.1093/jxb/eraa417

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Chen Q-L, An X-L, Zheng B-X, Ma Y-B, Su J-Q (2018) Long-term organic fertilization increased antibiotic resistome in phyllosphere of maize. Sci Total Environ 645:1230–1237. https://doi.org/10.1016/j.scitotenv.2018.07.260

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Sun A, Jiao X-Y, Chen Q, Wu A-L, Zheng Y, Lin Y-X, He J-Z, Hu H-W (2021) Microbial communities in crop phyllosphere and root endosphere are more resistant than soil microbiota to fertilization. Soil Biol Biochem 153(107):2411–2502. https://doi.org/10.1016/j.soilbio.2020.108113

    CAS  Article  Google Scholar 

  17. 17.

    Hou Y (2015) Study on the quality evaluation of Radix pseudostellariae by plant metabolomics. Dissertation, Nanjing University of Chinese Medicine

  18. 18.

    Wu H, Qin X, Wu H, Li F, Wu J, Zheng L, Wang J, Chen J, Zhao Y, Lin S (2020) Biochar mediates microbial communities and their metabolic characteristics under continuous monoculture. Chemosphere 246:125835. https://doi.org/10.1016/j.chemosphere.2020.125835

  19. 19.

    Wu H, Wu L, Wang J, Zhu Q, Lin S, Xu J, Zheng C, Chen J, Qin X, Fang C (2016) Mixed phenolic acids mediated proliferation of pathogens Talaromyces helicus and Kosakonia sacchari in continuously monocultured Radix pseudostellariae rhizosphere soil. Front Microbiol 7:335

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Wu H, Xu J, Wang J, Qin X, Wu L, Li Z, Lin S, Lin W, Zhu Q, Khan M, Lin W (2017) Insights into the mechanism of proliferation on the special microbes mediated by phenolic acids in the Radix pseudostellariae rhizosphere under continuous monoculture regimes. Front Plant Sci 8:659. https://doi.org/10.3389/fpls.2017.00659

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Chen J, Wu L, Xiao Z, Wu Y, Wu H, Qin X, Wang J, Wei X, Khan MU, Lin S, Lin W (2017) Assessment of the Diversity of Pseudomonas spp. and Fusarium spp. in Radix pseudostellariae rhizosphere under monoculture by combining DGGE and quantitative PCR. Front Microbiol 8:1748. https://doi.org/10.3389/fmicb.2017.01748

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Wu L, Chen J, Wu H, Qin X, Wang J, Wu Y, Khan MU, Lin S, Xiao Z, Luo X (2016) Insights into the regulation of rhizosphere bacterial communities by application of bio-organic fertilizer in Pseudostellaria heterophylla monoculture regime. Front Microbiol 7:1788

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Wang M, Song J, Han L, Liu X, Wang L, Zou L, Fu X (2010) Content analysis and dynamic research of heterophyllin B in the R. pseudostellariae. J Chinese Med Mater 33:1225–1227

    CAS  Google Scholar 

  24. 24.

    Wu H, Wang X, Wang L, Xiang Y, Shi J (2012) The antibiotic activity of polysaccharide from Houttuynia cordata thunb. Chinese Wild Plant Res 31:24–26

    Google Scholar 

  25. 25.

    Zeng L, Lin M, Dai L, Li J, Li J, Zhang Z, Lin W (2012) Effects of continuous cropping on photosynthesis and medicinal quality of Pseudostellariae heterophylla. Acta Agron Sin 38:1522–1528

    CAS  Article  Google Scholar 

  26. 26.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Lievens B, Brouwer M, Vanachter A, Levesque CA, Cammue BPA, Thomma B (2005) Quantitative assessment of phytopathogenic fungi in various substrates using a DNA macroarray. Environ Microbiol 7:1698–1710. https://doi.org/10.1111/j.1462-2920.2005.00816.x

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695:1–9

    Google Scholar 

  29. 29.

    Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Venkatachalam S, Ranjan K, Prasanna R, Ramakrishnan B, Thapa S, Kanchan A (2016) Diversity and functional traits of culturable microbiome members, including cyanobacteria in the rice phyllosphere. Plant Biol 18:627–637. https://doi.org/10.1111/plb.12441

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Gu S, Wei Z, Shao Z, Friman V-P, Cao K, Yang T, Kramer J, Wang X, Li M, Mei X, Xu Y, Shen Q, Kuemmerli R, Jousset A (2020) Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol 5: 1002-+. doi: https://doi.org/10.1038/s41564-020-0719-8

  32. 32.

    Olishevska S, Nickzad A, Deziel E (2019) Bacillus and Paenibacillus secreted polyketides and peptides involved in controlling human and plant pathogens. Appl Microbiol Biotechnol 103:1189–1215. https://doi.org/10.1007/s00253-018-9541-0

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Terakado-Tonooka J, Fujihara S, Ohwaki Y (2013) Possible contribution of Bradyrhizobium on nitrogen fixation in sweet potatoes. Plant Soil 367:639–650. https://doi.org/10.1007/s11104-012-1495-x

    CAS  Article  Google Scholar 

  34. 34.

    Viaene T, Langendries S, Beirinckx S, Maes M, Goormachtig S (2016) Streptomyces as a plant’s best friend? FEMS Microbiol Ecol 92(8):fiw119. https://doi.org/10.1093/femsec/fiw119

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Xiang Q, Chen Q-L, Zhu D, Yang X-R, Qiao M, Hu H-W, Zhu Y-G (2020) Microbial functional traits in phyllosphere are more sensitive to anthropogenic disturbance than in soil. Environ Pollut 265(Pt A):114954. https://doi.org/10.1016/j.envpol.2020.114954

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Dini-Andreote F (2020) Endophytes: the second layer of plant defense. Trends Plant Sci 25:319–322. https://doi.org/10.1016/j.tplants.2020.01.007

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Tkacz A, Bestion E, Bo Z, Hortala M, Poole PS (2020) Influence of plant fraction, soil, and plant species on microbiota: a multikingdom comparison. MBio 11(1):e02785-19. https://doi.org/10.1128/mBio.02785-19

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Wu L, Yang Y, Chen S, Zhao M, Zhu Z, Yang S, Qu Y, Ma Q, He Z, Zhou J (2016) Long-term successional dynamics of microbial association networks in anaerobic digestion processes. Water Res 104:1–10

    Article  Google Scholar 

  39. 39.

    Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330

    CAS  Article  Google Scholar 

  40. 40.

    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621. https://doi.org/10.1038/s41579-020-0412-1

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the National Science Foundation of China and the Project Funded by China Postdoctoral Science Foundation for providing the funds used in this work.

Funding

This work was supported by National Science Foundation of China (U1205021, 82003884, 81573530), and the Project Funded by China Postdoctoral Science Foundation (No. 2019M650150).

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Authors

Contributions

WX Lin and HM Wu conceived the study; HM Wu wrote the paper. HM Wu, JY Wang, XJ Qin and J Chen performed experiments; HM Wu and Z Zhang performed the statistical analyses; LK Wu and S Lin were involved in soil sampling. C Rensing and WX Lin have revised the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Zhen Zhang, Christopher Rensing or Wenxiong Lin.

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Cite this article

Wu, H., Zhang, Z., Wang, J. et al. Bio-fertilizer Amendment Alleviates the Replanting Disease under Consecutive Monoculture Regimes by Reshaping Leaf and Root Microbiome. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01861-1

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Keywords

  • Soil sickness
  • Phyllosphere
  • Crop microbiome
  • Allelopathy
  • Sustainable agriculture