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.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
All data generated or analyzed were included in this manuscript and the supporting information.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hou Y (2015) Study on the quality evaluation of Radix pseudostellariae by plant metabolomics. Dissertation, Nanjing University of Chinese Medicine
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
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
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
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
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
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
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
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
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
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
Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal, Complex Systems 1695:1–9
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
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
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
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
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
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
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
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
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
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
Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330
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
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.
This work was supported by National Science Foundation of China (U1205021, 82003884, 81573530), and the Project Funded by China Postdoctoral Science Foundation (No. 2019M650150).
Consent for Publication
All authors agreed with the publication of this manuscript.
The authors declare no competing interests.
Below is the link to the electronic supplementary material.
About this article
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
- Soil sickness
- Crop microbiome
- Sustainable agriculture