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Harnessing co-evolutionary interactions between plants and Streptomyces to combat drought stress

Nature Plants volume 10, pages 1159–1171 (2024)Cite this article

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Abstract

Streptomyces is a drought-tolerant bacterial genus in soils, which forms close associations with plants to provide host resilience to drought stress. Here we synthesize the emerging research that illuminates the multifaceted interactions of Streptomyces spp. in both plant and soil environments. It also explores the potential co-evolutionary relationship between plants and Streptomyces spp. to forge mutualistic relationships, providing drought tolerance to plants. We propose that further advancement in fundamental knowledge of eco-evolutionary interactions between plants and Streptomyces spp. is crucial and holds substantial promise for developing effective strategies to combat drought stress, ensuring sustainable agriculture and environmental sustainability in the face of climate change.

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Fig. 1: Drought-induced changes in the colonization and interaction patterns of plant-associated Streptomyces spp.
Fig. 2: Streptomyces engineering for enhanced agricultural production and ecosystem functions.

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References

  1. Pirozynski, K. & Malloch, D. The origin of land plants: a matter of mycotrophism. Biosystems 6, 153–164 (1975).

    Article  CAS  PubMed  Google Scholar 

  2. Hassani, M. A., Durán, P. & Hacquard, S. Microbial interactions within the plant holobiont. Microbiome 6, 58 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shepherdson, E. M. F., Baglio, C. R. & Elliot, M. A. Streptomyces behavior and competition in the natural environment. Curr. Opin. Microbiol. 71, 102257 (2023).

    Article  CAS  PubMed  Google Scholar 

  4. Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. Science 359, 320–325 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Vergnes, S. et al. Phyllosphere colonization by a soil Streptomyces sp. promotes plant defense responses against fungal infection. Mol. Plant Microbe Interact. 33, 223–234 (2020).

    Article  CAS  PubMed  Google Scholar 

  6. Wentzien, N. M. et al. Pitting the olive seed microbiome. Environ. Microbiome 19, 17 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 18, 152–163 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Abbasi, S., Sadeghi, A. & Safaie, N. Streptomyces alleviate drought stress in tomato plants and modulate the expression of transcription factors ERF1 and WRKY70 genes. Sci. Hortic. 265, 109206 (2020).

    Article  CAS  Google Scholar 

  9. Cordero, I., Leizeaga, A., Hicks, L. C., Rousk, J. & Bardgett, R. D. High intensity perturbations induce an abrupt shift in soil microbial state. ISME J. 17, 2190–2199 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Qin, S. et al. Plant growth-promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 416, 117–132 (2017).

    Article  CAS  Google Scholar 

  11. Kawicha, P. et al. Evaluation of soil Streptomyces spp. for the biological control of fusarium wilt disease and growth promotion in tomato and banana. Plant Pathol. J. 39, 108 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. LeBlanc, N. Bacteria in the genus Streptomyces are effective biological control agents for management of fungal plant pathogens: a meta-analysis. BioControl 67, 111–121 (2022).

    Article  CAS  Google Scholar 

  13. Köberl, M. et al. Bacillus and Streptomyces were selected as broad-spectrum antagonists against soilborne pathogens from arid areas in Egypt. FEMS Microbiol. Lett. 342, 168–178 (2013).

    Article  PubMed  Google Scholar 

  14. Viaene, T., Langendries, S., Beirinckx, S., Maes, M. & Goormachtig, S. Streptomyces as a plant’s best friend? FEMS Microbiol. Ecol. 92, fiw119 (2016).

    Article  PubMed  Google Scholar 

  15. Du, Y. et al. Biological control and plant growth promotion properties of Streptomyces albidoflavus St-220 isolated from Salvia miltiorrhiza rhizosphere. Front. Plant Sci. 13, 976813 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Xu, L. et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc. Natl Acad. Sci. USA 115, E4284–E4293 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Santos-Medellín, C. et al. Prolonged drought imparts lasting compositional changes to the rice root microbiome. Nat. Plants 7, 1065–1077 (2021).

    Article  PubMed  Google Scholar 

  18. Maglangit, F., Yu, Y. & Deng, H. Bacterial pathogens: threat or treat (a review on bioactive natural products from bacterial pathogens). Nat. Prod. Rep. 38, 782–821 (2021).

    Article  CAS  PubMed  Google Scholar 

  19. Yin, J. et al. Future socio-ecosystem productivity threatened by compound drought–heatwave events. Nat. Sustain. 6, 259–272 (2023).

    Article  Google Scholar 

  20. Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Change 4, 17–22 (2014).

    Article  Google Scholar 

  21. Qing, Y., Wang, S., Ancell, B. C. & Yang, Z.-L. Accelerating flash droughts induced by the joint influence of soil moisture depletion and atmospheric aridity. Nat. Commun. 13, 1139 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Bei, Q. et al. Extreme summers impact cropland and grassland soil microbiomes. ISME J. 17, 1589–1600 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Francis, I., Holsters, M. & Vereecke, D. The Gram‐positive side of plant–microbe interactions. Environ. Microbiol. 12, 1–12 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Metze, D. et al. Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions. Nat. Commun. 14, 5895 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yang, Z. et al. Streptomyces alleviate abiotic stress in plant by producing pteridic acids. Nat. Commun. 14, 7398 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Niu, S. et al. The osmolyte-producing endophyte Streptomyces albidoflavus OsiLf-2 induces drought and salt tolerance in rice via a multi-level mechanism. Crop J. 10, 375–386 (2022).

    Article  Google Scholar 

  27. Xing, Y. et al. Multi-omics reveals the sugarcane rhizosphere soil metabolism-microbiota interactions affected by drought stress. Appl. Soil Ecol. 190, 104994 (2023).

    Article  Google Scholar 

  28. Wu, Y. et al. Ecological clusters based on responses of soil microbial phylotypes to precipitation explain ecosystem functions. Soil Biol. Biochem. 142, 107717 (2020).

    Article  CAS  Google Scholar 

  29. Williams, A. & de Vries, F. T. Plant root exudation under drought: implications for ecosystem functioning. N. Phytol. 225, 1899–1905 (2020).

    Article  Google Scholar 

  30. Koyama, A., Steinweg, J. M., Haddix, M. L., Dukes, J. S. & Wallenstein, M. D. Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants. FEMS Microbiol. Ecol. 94, fix156 (2018).

    Article  Google Scholar 

  31. Yang, X., Wang, B., Chen, L., Li, P. & Cao, C. The different influences of drought stress at the flowering stage on rice physiological traits, grain yield, and quality. Sci. Rep. 9, 3742 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Naylor, D., DeGraaf, S., Purdom, E. & Coleman-Derr, D. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 11, 2691–2704 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Gao, M. et al. Disease-induced changes in plant microbiome assembly and functional adaptation. Microbiome 9, 1–18 (2021).

    Article  CAS  Google Scholar 

  34. Batista, B. D. et al. Biotic and abiotic responses to soilborne pathogens and environmental predictors of soil health. Soil Biol. Biochem. 189, 109246 (2024).

    Article  CAS  Google Scholar 

  35. Qiu, Z. et al. Response of the plant core microbiome to Fusarium oxysporum infection and identification of the pathobiome. Environ. Microbiol. 24, 4652–4669 (2022).

    Article  CAS  PubMed  Google Scholar 

  36. Carrión, V. J. et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366, 606–612 (2019).

    Article  PubMed  Google Scholar 

  37. Simmons, T. et al. Drought drives spatial variation in the millet root microbiome. Front. Plant Sci. 11, 599 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Liu, T.-Y. et al. Drought stress and plant ecotype drive microbiome recruitment in switchgrass rhizosheath. J. Integr. Plant Biol. 63, 1753–1774 (2021).

    Article  CAS  PubMed  Google Scholar 

  39. Wang, Z. et al. Enrichment of sugarcane rhizosphere bacterial community under different drought stress is driven by plant survival strategies. Preprint at SSRN https://doi.org/10.2139/ssrn.4155112 (2022).

  40. Xie, J. et al. Drought stress triggers shifts in the root microbial community and alters functional categories in the microbial gene pool. Front. Microbiol. 12, 744897 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Fitzpatrick, C. R. et al. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl Acad. Sci. USA 115, E1157–E1165 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chen, Q. et al. Alleviation role of functional carbon nanodots for tomato growth and soil environment under drought stress. J. Hazard. Mater. 423, 127260 (2022).

    Article  CAS  PubMed  Google Scholar 

  43. Xu, L. et al. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nat. Commun. 12, 3209 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Xu, L. & Coleman-Derr, D. Causes and consequences of a conserved bacterial root microbiome response to drought stress. Curr. Opin. Microbiol. 49, 1–6 (2019).

    Article  CAS  PubMed  Google Scholar 

  45. Singh, B. K., Trivedi, P., Egidi, E., Macdonald, C. A. & Delgado-Baquerizo, M. Crop microbiome and sustainable agriculture. Nat. Rev. Microbiol. 18, 601–602 (2020).

    Article  CAS  PubMed  Google Scholar 

  46. Chodak, M., Gołębiewski, M., Morawska-Płoskonka, J., Kuduk, K. & Niklińska, M. Soil chemical properties affect the reaction of forest soil bacteria to drought and rewetting stress. Ann. Microbiol. 65, 1627–1637 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Fuchslueger, L. et al. Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event. J. Ecol. 104, 1453–1465 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Naylor, D. & Coleman-Derr, D. Drought stress and root-associated bacterial communities. Front. Plant Sci. 8, 2223 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Si, J. et al. Interactions between soil compositions and the wheat root microbiome under drought stress: From an in silico to in planta perspective. Comput. Struct. Biotechnol. J. 19, 4235–4247 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Allsup, C. M., George, I. & Lankau, R. A. Shifting microbial communities can enhance tree tolerance to changing climates. Science 380, 835–840 (2023).

    Article  CAS  PubMed  Google Scholar 

  51. Liu, H., Brettell, L. E., Qiu, Z. & Singh, B. K. Microbiome-mediated stress resistance in plants. Trends Plant Sci. 25, 733–743 (2020).

    Article  CAS  PubMed  Google Scholar 

  52. Santos-Medellín, C., Edwards, J., Liechty, Z., Nguyen, B. & Sundaresan, V. Drought stress results in a compartment-specific restructuring of the rice root-associated microbiomes. mBio 8, e00764-17 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Lin, H. A. et al. Progressive drought alters the root exudate metabolome and differentially activates metabolic pathways in cotton (Gossypium hirsutum). Front. Plant Sci. 14, 1244591 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Gupta, A., Rico-Medina, A. & Caño-Delgado, A. I. The physiology of plant responses to drought. Science 368, 266–269 (2020).

    Article  CAS  PubMed  Google Scholar 

  55. de Vries, F. T., Griffiths, R. I., Knight, C. G., Nicolitch, O. & Williams, A. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368, 270–274 (2020).

    Article  PubMed  Google Scholar 

  56. Weng, J.-K., Lynch, J. H., Matos, J. O. & Dudareva, N. Adaptive mechanisms of plant specialized metabolism connecting chemistry to function. Nat. Chem. Biol. 17, 1037–1045 (2021).

    Article  CAS  PubMed  Google Scholar 

  57. Hasibeder, R., Fuchslueger, L., Richter, A. & Bahn, M. Summer drought alters carbon allocation to roots and root respiration in mountain grassland. N. Phytol. 205, 1117–1127 (2015).

    Article  CAS  Google Scholar 

  58. Malik, A. A. & Bouskill, N. J. Drought impacts on microbial trait distribution and feedback to soil carbon cycling. Funct. Ecol. 36, 1442–1456 (2022).

    Article  CAS  Google Scholar 

  59. Jaeger, A. C., Hartmann, M., Conz, R. F., Six, J. & Solly, E. F. Prolonged water limitation shifts the soil microbiome from copiotrophic to oligotrophic lifestyles in Scots pine mesocosms. Environ. Microbiol. Rep. 16, e13211 (2023).

  60. Martinović, T. et al. Microbial utilization of simple and complex carbon compounds in a temperate forest soil. Soil Biol. Biochem. 173, 108786 (2022).

    Article  Google Scholar 

  61. Hassan, S. & Mathesius, U. The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J. Exp. Bot. 63, 3429–3444 (2012).

    Article  CAS  PubMed  Google Scholar 

  62. Kudjordjie, E. N., Sapkota, R., Steffensen, S. K., Fomsgaard, I. S. & Nicolaisen, M. Maize synthesized benzoxazinoids affect the host associated microbiome. Microbiome 7, 59 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Sousa Jesus de, J. A. & Olivares, F. L. Plant growth promotion by streptomycetes: ecophysiology, mechanisms and applications. Chem. Biol. Technol. Agric. 3, 24 (2016).

    Article  Google Scholar 

  64. Li, G. et al. Integrated microbiome and metabolomic analysis reveal responses of rhizosphere bacterial communities and root exudate composition to drought and genotype in rice (Oryza sativa L.). Rice 16, 19 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zou, Y.-N., Wu, Q.-S. & Kuča, K. Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biol. 23, 50–57 (2021).

    Article  CAS  PubMed  Google Scholar 

  66. Waszczak, C., Carmody, M. & Kangasjärvi, J. Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 69, 209–236 (2018).

    Article  CAS  PubMed  Google Scholar 

  67. Imlay, J. A. Where in the world do bacteria experience oxidative stress? Environ. Microbiol. 21, 521–530 (2019).

    Article  CAS  PubMed  Google Scholar 

  68. Mai-Prochnow, A., Clauson, M., Hong, J. & Murphy, A. B. Gram positive and Gram negative bacteria differ in their sensitivity to cold plasma. Sci. Rep. 6, 38610 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sahu, P. K. et al. ROS generated from biotic stress: effects on plants and alleviation by endophytic microbes. Front. Plant Sci. 13, 1042936 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Passari, A. K. et al. In vivo studies of inoculated plants and in vitro studies utilizing methanolic extracts of endophytic Streptomyces sp. strain dbt34 obtained from Mirabilis jalapa L. exhibit ROS-scavenging and other bioactive properties. Int. J. Mol. Sci. 21, 7364 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Brown, S., Santa Maria, J. P. Jr & Walker, S. Wall teichoic acids of Gram-positive bacteria. Annu. Rev. Microbiol. 67, 313–336 (2013).

    Article  CAS  PubMed  Google Scholar 

  72. Suzuki, M. et al. Development of a mugineic acid family phytosiderophore analog as an iron fertilizer. Nat. Commun. 12, 1558 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Chao, Z.-F. & Chao, D.-Y. Similarities and differences in iron homeostasis strategies between graminaceous and nongraminaceous plants. N. Phytol. 236, 1655–1660 (2022).

    Article  CAS  Google Scholar 

  74. Nozoye, T. et al. Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J. Biol. Chem. 286, 5446–5454 (2011).

    Article  CAS  PubMed  Google Scholar 

  75. Jones, S. E. et al. Streptomyces exploration is triggered by fungal interactions and volatile signals. eLife 6, e21738 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Meij der van, A. et al. The plant stress hormone jasmonic acid evokes defensive responses in Streptomycetes. Appl. Environ. Microbiol. 89, e0123923 (2023).

    Article  Google Scholar 

  77. Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Vlot, A. C. et al. Systemic propagation of immunity in plants. N. Phytol. 229, 1234–1250 (2021).

    Article  CAS  Google Scholar 

  79. Choudhary, A. & Senthil-Kumar, M. Drought attenuates plant defence against bacterial pathogens by suppressing the expression of CBP60g/SARD1 during combined stress. Plant Cell Environ. 45, 1127–1145 (2022).

    Article  CAS  PubMed  Google Scholar 

  80. Schwartz, D. A., Shoemaker, W. R., Măgălie, A., Weitz, J. S. & Lennon, J. T. Bacteria-phage coevolution with a seed bank. ISME J. 17, 1315–1325 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Elliot, M. A. & Talbot, N. J. Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr. Opin. Microbiol. 7, 594–601 (2004).

    Article  CAS  PubMed  Google Scholar 

  82. Humphreys, C. P. et al. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat. Commun. 1, 103 (2010).

    Article  PubMed  Google Scholar 

  83. Zhang, X. et al. Resistance of microbial community and its functional sensitivity in the rhizosphere hotspots to drought. Soil Biol. Biochem. 161, 108360 (2021).

    Article  CAS  Google Scholar 

  84. Oyserman, B. O. et al. Disentangling the genetic basis of rhizosphere microbiome assembly in tomato. Nat. Commun. 13, 3228 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kellogg, E. A. C4 photosynthesis. Curr. Biol. 23, R594–R599 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Ehleringer, J. & Björkman, O. Quantum yields for CO2 uptake in C3 and C4 plants: dependence on temperature, CO2, and O2 concentration. Plant Physiol. 59, 86–90 (1977).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Slessarev, E. W. et al. Water balance creates a threshold in soil pH at the global scale. Nature 540, 567–569 (2016).

    Article  CAS  PubMed  Google Scholar 

  88. Geilfus, C. M. The pH of the apoplast: dynamic factor with functional impact under stress. Mol. Plant 10, 1371–1386 (2017).

    Article  CAS  PubMed  Google Scholar 

  89. Bacon, M. A., Wilkinson, S. & Davies, W. J. pH-regulated leaf cell expansion in droughted plants is abscisic acid dependent. Plant Physiol. 118, 1507–1515 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Seipke, R. F., Kaltenpoth, M. & Hutchings, M. I. Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol. Rev. 36, 862–876 (2012).

    Article  CAS  PubMed  Google Scholar 

  91. Fu, W. et al. Community response of arbuscular mycorrhizal fungi to extreme drought in a cold-temperate grassland. N. Phytol. 234, 2003–2017 (2022).

    Article  Google Scholar 

  92. Li, J. et al. Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front. Plant Sci. 10, 499 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Courty, P.-E. et al. Species-dependent partitioning of C and N stable isotopes between arbuscular mycorrhizal fungi and their C3 and C4 hosts. Soil Biol. Biochem. 82, 52–61 (2015).

    Article  CAS  Google Scholar 

  94. Emery, S. M., Bell-Dereske, L., Stahlheber, K. A. & Gross, K. L. Arbuscular mycorrhizal fungal community responses to drought and nitrogen fertilization in switchgrass stands. Appl. Soil Ecol. 169, 104218 (2022).

    Article  Google Scholar 

  95. Bowles, S. & Gintis, H. The evolution of strong reciprocity: cooperation in heterogeneous populations. Theor. Popul. Biol. 65, 17–28 (2004).

    Article  PubMed  Google Scholar 

  96. Zhang, H., Liu, H. & Han, X. Traits-based approach: leveraging genome size in plant–microbe interactions. Trends Microbiol. 32, 333–341 (2024).

  97. Nikolaidis, M. et al. A panoramic view of the genomic landscape of the genus Streptomyces. Microb. Genom. 9, mgen001028 (2023).

  98. Liu, H. et al. Warmer and drier ecosystems select for smaller bacterial genomes in global soils. iMeta 2, e70 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Banerjee, S. & van der Heijden, M. G. Soil microbiomes and one health. Nat. Rev. Microbiol. 21, 6–20 (2023).

    Article  CAS  PubMed  Google Scholar 

  100. Coban, O., De Deyn, G. B. & van der Ploeg, M. Soil microbiota as game-changers in restoration of degraded lands. Science 375, abe0725 (2022).

    Article  PubMed  Google Scholar 

  101. Sessitsch, A., Pfaffenbichler, N. & Mitter, B. Microbiome applications from lab to field: facing complexity. Trends Plant Sci. 24, 194–198 (2019).

    Article  CAS  PubMed  Google Scholar 

  102. Muok, A. R., Claessen, D. & Briegel, A. Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria. ISME J. 15, 2591–2600 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. King, W. L. & Bell, T. H. Can dispersal be leveraged to improve microbial inoculant success? Trends Biotechnol. 40, 12–21 (2022).

    Article  CAS  PubMed  Google Scholar 

  104. Wang, L., Ning, C., Pan, T. & Cai, K. Role of silica nanoparticles in abiotic and biotic stress tolerance in plants: a review. Int. J. Mol. Sci. 23, 1947 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Wen, T. et al. Tapping the rhizosphere metabolites for the prebiotic control of soil-borne bacterial wilt disease. Nat. Commun. 14, 4497 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Kimura, I. et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4, 1829 (2013).

    Article  PubMed  Google Scholar 

  107. Salminen, S. et al. The International Scientific Association of Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics. Nat. Rev. Gastroenterol. Hepatol. 18, 649–667 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Kim, D.-R. & Kwak, Y.-S. Endophytic Streptomyces population induced by L-glutamic acid enhances plant resilience to abiotic stresses in tomato. Front. Microbiol. 14, 1180538 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Batista, B. D. & Singh, B. K. Realities and hopes in the application of microbial tools in agriculture. Microb. Biotechnol. 14, 1258–1268 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Wang, J. Y. & Doudna, J. A. CRISPR technology: a decade of genome editing is only the beginning. Science 379, eadd8643 (2023).

    Article  CAS  PubMed  Google Scholar 

  111. Jurburg, S. D. et al. Potential of microbiome-based solutions for agrifood systems. Nat. Food 3, 557–560 (2022).

    Article  PubMed  Google Scholar 

  112. Özbolat, O. et al. Long-term adoption of reduced tillage and green manure improves soil physicochemical properties and increases the abundance of beneficial bacteria in a Mediterranean rainfed almond orchard. Geoderma 429, 116218 (2023).

    Article  Google Scholar 

  113. Hannula, S. E. et al. Persistence of plant-mediated microbial soil legacy effects in soil and inside roots. Nat. Commun. 12, 5686 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Wang, M. et al. Sugarcane straw returning is an approaching technique for the improvement of rhizosphere soil functionality, microbial community, and yield of different sugarcane cultivars. Front. Microbiol. 14, 1133973 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Del Carratore, F., Hanko, E. K. R., Breitling, R. & Takano, E. Biotechnological application of Streptomyces for the production of clinical drugs and other bioactive molecules. Curr. Opin. Biotechnol. 77, 102762 (2022).

    Article  PubMed  Google Scholar 

  116. Lin, D. et al. Reduction of antibiotic resistance genes (ARGs) in swine manure-fertilized soil via fermentation broth from fruit and vegetable waste. Environ. Res. 214, 113835 (2022).

    Article  CAS  PubMed  Google Scholar 

  117. Helepciuc, F.-E. & Todor, A. EU microbial pest control: a revolution in waiting. Pest Manag. Sci. 78, 1314–1325 (2022).

    Article  CAS  PubMed  Google Scholar 

  118. Semchenko, M. et al. Deciphering the role of specialist and generalist plant–microbial interactions as drivers of plant–soil feedback. N. Phytol. 234, 1929–1944 (2022).

    Article  CAS  Google Scholar 

  119. Mittler, R., Zandalinas, S. I., Fichman, Y. & Van Breusegem, F. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol. 23, 663–679 (2022).

    Article  CAS  PubMed  Google Scholar 

  120. Genus Streptomyces. List of Prokaryotic names with Standing in Nomenclature https://lpsn.dsmz.de/genus/streptomyces (accessed 21 December 2023).

  121. de Lima Procópio, R. E., da Silva, I. R., Martins, M. K., de Azevedo, J. L. & de Araújo, J. M. Antibiotics produced by Streptomyces. Braz. J. Infect. Dis. 16, 466–471 (2012).

    Article  Google Scholar 

  122. Barka Essaid, A. et al. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. https://doi.org/10.1128/mmbr.00019-15 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Jones, S. E. et al. Streptomyces volatile compounds influence exploration and microbial community dynamics by altering iron availability. mBio 10, e00171-19 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Muok, A. R. & Briegel, A. Intermicrobial hitchhiking: how nonmotile microbes leverage communal motility. Trends Microbiol. 29, 542–550 (2021).

    Article  CAS  PubMed  Google Scholar 

  125. Kim, D.-R. et al. A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees. Nat. Commun. 10, 4802 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  126. Madin, J. S. et al. A synthesis of bacterial and archaeal phenotypic trait data. Sci. Data 7, 170 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Zhang, H.-Y., Bissett, A., Aguilar-Trigueros, C. A., Liu, H.-W. & Powell, J. R. Fungal genome size and composition reflect ecological strategies along soil fertility gradients. Ecol. Lett. 26, 1108–1118 (2023).

    Article  PubMed  Google Scholar 

  128. Hershberg, R. & Petrov, D. A. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet. 6, e1001115 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Becher, P. G. et al. Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nat. Microbiol. 5, 821–829 (2020).

    Article  CAS  PubMed  Google Scholar 

  130. Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. figshare https://figshare.com/s/82a2d3f5d38ace925492 (2022).

  131. Groussin, M., Mazel, F. & Alm, E. J. Co-evolution and co-speciation of host-gut bacteria systems. Cell Host Microbe 28, 12–22 (2020).

    Article  CAS  PubMed  Google Scholar 

  132. Henry, L. P., Bruijning, M., Forsberg, S. K. G. & Ayroles, J. F. The microbiome extends host evolutionary potential. Nat. Commun. 12, 5141 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Wang, J., Li, Y., Pinto-Tomás, A. A., Cheng, K. & Huang, Y. Habitat adaptation drives speciation of a Streptomyces species with distinct habitats and disparate geographic origins. mBio 13, e02781-21 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  134. van Bergeijk, D. A., Terlouw, B. R., Medema, M. H. & van Wezel, G. P. Ecology and genomics of Actinobacteria: new concepts for natural product discovery. Nat. Rev. Microbiol. 18, 546–558 (2020).

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Australian Research Council Discovery Grants (DP21010081 and DP230101448). B.K.S. research on plant–microbial science is also supported by the Cooperative Research Centre—Future for Food Systems.

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  1. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, Australia

    Hongwei Liu, Jiayu Li & Brajesh K. Singh

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  1. Hongwei Liu
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  2. Jiayu Li
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  3. Brajesh K. Singh
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Contributions

H.L. and B.K.S. developed the concept. The first draft of the paper was written by H.L. with substantial contributions from B.K.S. J.L. contributed to writing and discussion.

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Correspondence to Hongwei Liu or Brajesh K. Singh.

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Nature Plants thanks Samiran Banerjee, Gabriele Berg and Ioannis Stringlis for their contribution to the peer review of this work.

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Supplementary Table 1 (download PDF )

Modes of action of Streptomyces spp. included in this study.

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Liu, H., Li, J. & Singh, B.K. Harnessing co-evolutionary interactions between plants and Streptomyces to combat drought stress. Nat. Plants 10, 1159–1171 (2024). https://doi.org/10.1038/s41477-024-01749-1

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