Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Plant pathogen resistance is mediated by recruitment of specific rhizosphere fungi

Abstract

Beneficial interactions between plants and rhizosphere microorganisms are key determinants of plant health with the potential to enhance the sustainability of agricultural practices. However, pinpointing the mechanisms that determine plant disease protection is often difficult due to the complexity of microbial and plant-microbe interactions and their links with the plant’s own defense systems. Here, we found that the resistance level of different banana varieties was correlated with the plant’s ability to stimulate specific fungal taxa in the rhizosphere that are able to inhibit the Foc TR4 pathogen. These fungal taxa included members of the genera Trichoderma and Penicillium, and their growth was stimulated by plant exudates such as shikimic acid, D-(-)-ribofuranose, and propylene glycol. Furthermore, amending soils with these metabolites enhanced the resistance of a susceptible variety to Foc TR4, with no effect observed for the resistant variety. In total, our findings suggest that the ability to recruit pathogen-suppressive fungal taxa may be an important component in determining the level of pathogen resistance exhibited by plant varieties. This perspective opens up new avenues for improving plant health, in which both plant and associated microbial properties are considered.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Disease incidence and relative abundance of Foc TR4 in rhizosphere soils of different banana varieties.
Fig. 2: Properties of the rhizosphere fungal communities associated different banana varieties.
Fig. 3: Identification of fungal isolates and pathogen suppression effects of selected fungal isolates.
Fig. 4: Metabolite analysis of rhizosphere soils of different banana varieties.
Fig. 5: Effects of pure metabolites on the growth of putative key fungal taxa in vitro.
Fig. 6: Effects of the exogenous metabolites on the susceptibility of different varieties to Foc TR4.
Fig. 7: Conceptual model for the interaction mechanisms among plant, pathogen and beneficial fungal key taxa derived by rhizosphere metabolites.

Similar content being viewed by others

Data availability

Raw amplicon sequencing data was deposited at the National Center for Biotechnology Information (NCBI) under the accession number PRJNA830664.

References

  1. Strange RN, Scott PR. Plant Disease: a threat to global food security. Annu Rev Phytopathol. 2005;43:83–116.

    Article  CAS  PubMed  Google Scholar 

  2. Jones JDG, Dangl JL. The plant immune system. Nature 2006;444:323–9.

    Article  CAS  PubMed  Google Scholar 

  3. Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P. Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol. 2017;55:565–89.

    Article  CAS  PubMed  Google Scholar 

  4. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science. 2015;349:860–4.

    Article  CAS  PubMed  Google Scholar 

  5. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol. 2014;52:347–75.

    Article  CAS  PubMed  Google Scholar 

  6. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.

    Article  CAS  PubMed  Google Scholar 

  7. Blundell R, Schmidt JE, Igwe A, Cheung AL, Vannette RL, Gaudin ACM, et al. Organic management promotes natural pest control through altered plant resistance to insects. Nat Plants. 2020;6:483–91.

    Article  CAS  PubMed  Google Scholar 

  8. Lee S-M, Kong HG, Song GC, Ryu C-M. Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME J. 2021;15:330–47.

    Article  CAS  PubMed  Google Scholar 

  9. Li H, La S, Zhang X, Gao L, Tian Y. Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress. ISME J. 2021;15:2865–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Xu L, Dong Z, Chiniquy D, Pierroz G, Deng S, Gao C, et al. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nat Commun. 2021;12:3209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wei Z, Gu Y, Friman V-P, Kowalchuk GA, Xu Y, Shen Q, et al. Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv. 2019;5:eaaw0759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME. Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol. 2019;19:201.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013;11:789–99.

    Article  CAS  PubMed  Google Scholar 

  14. Yin C, Casa Vargas JM, Schlatter DC, Hagerty CH, Hulbert SH, Paulitz TC. Rhizosphere community selection reveals bacteria associated with reduced root disease. Microbiome 2021;9:86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun. 2018;9:2738.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chen S, Waghmode TR, Sun R, Kuramae EE, Hu C, Liu B. Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome 2019;7:136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Butler D. Fungus threatens top banana. Nature 2013;504:195–6.

    Article  CAS  PubMed  Google Scholar 

  18. Chen A, Sun J, Matthews A, Armas-Egas L, Chen N, Hamill S, et al. Assessing variations in host resistance to Fusarium oxysporum f sp. cubense Race 4 in Musa species, with a focus on the subtropical Race 4. Front Microbiol. 2019;10:1062.

    Article  PubMed  PubMed Central  Google Scholar 

  19. García-Bastidas FA, Van der Veen AJT, Nakasato-Tagami G, Meijer HJG, Arango-Isaza RE, Kema GHJ. An improved phenotyping protocol for Panama disease in banana. Front Plant Sci. 2019;10:1006.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sun J, Zhang J, Fang H, Peng L, Wei S, Li C, et al. Comparative transcriptome analysis reveals resistance-related genes and pathways in Musa acuminata banana “Guijiao 9” in response to Fusarium wilt. Plant Physiol Biochem. 2019;141:83–94.

    Article  CAS  PubMed  Google Scholar 

  21. Kwak M-J, Kong HG, Choi K, Kwon S-K, Song JY, Lee J, et al. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol. 2018;36:1100–9.

    Article  CAS  Google Scholar 

  22. Mendes LW, de Chaves MG, de Cassia Fonseca M, Mendes R, Raaijmakers JM, Tsai SM. Resistance breeding of common bean shapes the physiology of the rhizosphere microbiome. Front Microbiol. 2019;10:2252.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Haney CH, Samuel BS, Bush J, Ausubel FM. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nat Plants. 2015;1:15051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mendes LW, Raaijmakers JM, de Hollander M, Mendes R, Tsai SM. Influence of resistance breeding in common bean on rhizosphere microbiome composition and function. ISME J. 2018;12:212–24.

    Article  PubMed  Google Scholar 

  25. Teixeira PJPL, Colaianni NR, Law TF, Conway JM, Gilbert S, Li H, et al. Specific modulation of the root immune system by a community of commensal bacteria. Proc Natl Acad Sci USA. 2021;118:e2100678118.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Bhalla K, Qu X, Kretschmer M, Kronstad JW. The phosphate language of fungi. Trends Microbiol. 2022;30:338–49.

    Article  CAS  PubMed  Google Scholar 

  27. Cai F, Gao R, Zhao Z, Ding M, Jiang S, Yagtu C, et al. Evolutionary compromises in fungal fitness: hydrophobins can hinder the adverse dispersal of conidiospores and challenge their survival. ISME J. 2020;14:2610–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yuan X, Hong S, Xiong W, Raza W, Shen Z, Wang B, et al. Development of fungal-mediated soil suppressiveness against Fusarium wilt disease via plant residue manipulation. Microbiome 2021;9:200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yuan MM, Kakouridis A, Starr E, Nguyen N, Shi S, Pett-Ridge J, et al. Fungal-bacterial cooccurrence patterns differ between arbuscular mycorrhizal fungi and nonmycorrhizal fungi across soil niches. mBio 2021;12:e03509–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3:470–80.

    Article  CAS  PubMed  Google Scholar 

  31. Guo S, Tao C, Jousset A, Xiong W, Wang Z, Shen Z, et al. Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. ISME J. 2022;16:1932–43.

    Article  CAS  PubMed  Google Scholar 

  32. Dangl JL, Horvath DM, Staskawicz BJ. Pivoting the plant immune system from dissection to deployment. Science 2013;341:746–51.

    Article  CAS  PubMed  Google Scholar 

  33. De Coninck B, Timmermans P, Vos C, Cammue BPA, Kazan K. What lies beneath: belowground defense strategies in plants. Trends Plant Sci. 2015;20:91–101.

    Article  PubMed  Google Scholar 

  34. Li M, Ma G, Lian H, Su X, Tian Y, Huang W, et al. The effects of Trichoderma on preventing cucumber Fusarium wilt and regulating cucumber physiology. J Integr Agric. 2019;18:607–17.

    Article  Google Scholar 

  35. Zhao X, Liu X, Zhao H, Ni Y, Lian Q, Qian H, et al. Biological control of Fusarium wilt of sesame by Penicillium bilaiae 47M-1. Biol Control. 2021;158:104601.

    Article  CAS  Google Scholar 

  36. Bonanomi G, Capodilupo M, Incerti G, Gaglione SA, Scala F. Fungal diversity increases soil fungistasis and resistance to microbial invasion by a non resident species. Biol Control. 2014;72:38–45.

    Article  Google Scholar 

  37. Shen C, Wang J, He J, Yu F, Ge Y. Plant diversity enhances soil fungal diversity and microbial resistance to plant invasion. Appl Environ Microbiol. 2021;87:e00251–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Luo J, Ran W, Hu J, Yang X, Xu Y, Shen Q. Application of bio-organic fertilizer significantly affected fungal diversity of soils. Soil Sci Soc Am J 2010;74:2039–48.

    Article  CAS  Google Scholar 

  39. Li Y, Xu L, Letuma P, Lin W. Metabolite profiling of rhizosphere soil of different allelopathic potential rice accessions. BMC Plant Biol. 2020;20:265.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018;23:25–41.

    Article  CAS  PubMed  Google Scholar 

  41. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol. 2004;2:43–56.

    Article  CAS  PubMed  Google Scholar 

  42. Larena I, Sabuquillo P, Melgarejo P, Cal A. Biocontrol of Fusarium and Verticillium wilt of tomato by Penicillium Oxalicum under greenhouse and field conditions. J Phytopathol. 2003;151:507–12.

    Article  Google Scholar 

  43. Fravel D, Olivain C, Alabouvette C. Fusarium oxysporum and its biocontrol. N. Phytol. 2003;157:493–502.

    Article  CAS  Google Scholar 

  44. Saleem M, Hu J, Jousset A. More than the sum of its parts: microbiome biodiversity as a driver of plant growth and soil health. Annu Rev Ecol Evol Syst. 2019;50:145–68.

    Article  Google Scholar 

  45. Tucci M, Ruocco M, De Masi L, De Palma M, Lorito M. The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol. 2011;12:341–54.

    Article  CAS  PubMed  Google Scholar 

  46. Gu Y, Wang X, Yang T, Friman V-P, Geisen S, Wei Z, et al. Chemical structure predicts the effect of plant-derived low-molecular weight compounds on soil microbiome structure and pathogen suppression. Funct Ecol. 2020;34:2158–69.

    Article  Google Scholar 

  47. Wen T, Xie P, Penton CR, Hale L, Thomashow LS, Yang S, et al. Specific metabolites drive the deterministic assembly of diseased rhizosphere microbiome through weakening microbial degradation of autotoxin. Microbiome 2022;10:177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Shen Z, Penton CR, Lv N, Xue C, Yuan X, Ruan Y, et al. Banana Fusarium wilt disease incidence is influenced by shifts of soil microbial communities under different monoculture spans. Micro Ecol. 2018;75:739–50.

    Article  Google Scholar 

  49. Shen Z, Xue C, Penton CR, Thomashow LS, Zhang N, Wang B, et al. Suppression of banana Panama disease induced by soil microbiome reconstruction through an integrated agricultural strategy. Soil Biol Biochem. 2019;128:164–74.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  51. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–8.

    Article  CAS  PubMed  Google Scholar 

  53. White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols. San Diego: Academic Press; 1990. pp 315–22.

  54. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011;27:2957–63.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.

    Article  CAS  PubMed  Google Scholar 

  57. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–7.

    Article  PubMed  Google Scholar 

  58. Zheng Y, Gong X. Niche differentiation rather than biogeography shapes the diversity and composition of microbiome of Cycas panzhihuaensis. Microbiome 2019;7:152.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara RB, et al. Package ‘vegan’. Community Ecol Package Version. 2013;2:1–295.

    Google Scholar 

  61. Shen Z, Xue C, Taylor PWJ, Ou Y, Wang B, Zhao Y, et al. Soil pre-fumigation could effectively improve the disease suppressiveness of biofertilizer to banana Fusarium wilt disease by reshaping the soil microbiome. Biol Fertil Soils. 2018;54:793–806.

    Article  CAS  Google Scholar 

  62. Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol. 2005;71:4117–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lin Y, Su C, Chao C, Chen C, Chang C, Huang J, et al. A molecular diagnosis method using real-time PCR for quantification and detection of Fusarium oxysporum f. sp. cubense race 4. Eur J Plant Pathol. 2013;135:395–405.

    Article  CAS  Google Scholar 

  64. Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, et al. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 2020;8:137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, et al. Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils. 2013;49:435–46.

    Article  Google Scholar 

  66. Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, et al. Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 2018;6:156.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Wen T, Yuan J, He X, Lin Y, Huang Q, Shen Q. Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion. Hortic Res. 2020;7:154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhang X, Li Y, Yu Z, Liang X, Qi S. Phylogenetic diversity and bioactivity of culturable deep-sea-derived fungi from Okinawa Trough. J Oceano Limnol. 2021;39:892–902.

    Article  Google Scholar 

  69. Singh MP. Application of Biolog FF MicroPlate for substrate utilization and metabolite profiling of closely related fungi. J Microbiol Methods. 2009;77:102–8.

    Article  CAS  PubMed  Google Scholar 

  70. Hagn A, Wallisch S, Radl V, Munch JC, Schloter M. A new cultivation independent approach to detect and monitor common Trichoderma species in soils. J Microbiol Methods. 2007;69:86–92.

    Article  CAS  PubMed  Google Scholar 

  71. Géry A, Delanoë A, Heutte N, Chosson E, Bonhomme J, Garon D. A novel qPCR based-method for detection and quantification of three recurrent species of Penicillium isolated from bioaerosols in mold-damaged homes. J Microbiol Methods. 2021;186:106236.

    Article  PubMed  Google Scholar 

  72. Khan-Malek R, Wang Y. Statistical analysis of quantitative RT-PCR Results. Methods Mol Biol. 2017;1641:281–96.

    Article  CAS  PubMed  Google Scholar 

  73. Deng Y, Jiang Y, Yang Y, He Z, Luo F, Zhou J. Molecular ecological network analyses. BMC Bioinform. 2012;13:1–20.

    Article  Google Scholar 

  74. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2007;2:2366–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by National Natural Science Foundation of China (31972509, 32102475 and 42090065), the Fundamental Research Funds for the Central Universities (KYQN2022020), the China Postdoctoral Science Foundation (2021TQ0156 and 2021M691613), and the Hainan Provincial Natural Science Foundation of China (322MS092).

Author information

Authors and Affiliations

Authors

Contributions

SL, CT, ZS, CL and RL conceived experiments and discussed results. DX and OS performed field. SL, CT, LZ, ZW and JW designed assays and performed pot experiments. SL and CT analyzed data. SL wrote the manuscript with input from ZS, CL, CT, RL, GAK, WX and QS. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Zongzhuan Shen or Chunyu Li.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

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

Liu, S., Tao, C., Zhang, L. et al. Plant pathogen resistance is mediated by recruitment of specific rhizosphere fungi. ISME J 17, 931–942 (2023). https://doi.org/10.1038/s41396-023-01406-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-023-01406-z

This article is cited by

Search

Quick links