Skip to main content

Advertisement

SpringerLink
Log in

Harnessing the plant microbiome for sustainable crop production

  • Review Article
  • Published:

From Nature Reviews Microbiology

View current issue Sign up to alerts

Abstract

Global research on the plant microbiome has enhanced our understanding of the complex interactions between plants and microorganisms. The structure and functions of plant-associated microorganisms, as well as the genetic, biochemical, physical and metabolic factors that influence the beneficial traits of plant microbiota have also been intensively studied. Harnessing the plant microbiome has led to the development of various microbial applications to improve crop productivity in the face of a range of challenges, for example, climate change, abiotic and biotic stresses, and declining soil properties. Microorganisms, particularly nitrogen-fixing rhizobia as well as mycorrhizae and biocontrol agents, have been applied for decades to improve plant nutrition and health. Still, there are limitations regarding efficacy and consistency under field conditions. Also, the wealth of expanding knowledge on microbiome diversity, functions and interactions represents a huge source of information to exploit for new types of application. In this Review, we explore plant microbiome functions, mechanisms, assembly and types of interaction, and discuss current applications and their pitfalls. Furthermore, we elaborate on how the latest findings in plant microbiome research may lead to the development of new or more advanced applications. Finally, we discuss research gaps to fully leverage microbiome functions for sustainable plant production.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: The plant microbiome and microbial interactions.
Fig. 2: The functions and influencing factors of the plant microbiome.
Fig. 3: Major microbial crop protection products.
Fig. 4: Major microbial biofertilizers and biostimulants.
Fig. 5: Current and emerging microbiome-based applications for sustainable crop production.

Similar content being viewed by others

References

  1. Hardoim, P. R. et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79, 293–320 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Compant, S., Clément, C. & Sessitsch, A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42, 669–678 (2010).

    Article  CAS  Google Scholar 

  3. Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020). This study underscores the crucial importance of understanding intricate relationships between plants and the microorganisms that colonize them to enhance plant health or crop performance in both agricultural and natural ecosystems.

    Article  CAS  PubMed  Google Scholar 

  4. 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 

  5. Dent, M. Biostimulants and biopesticides 2021–2031: technologies, markets and forecasts. idtechex.com https://www.idtechex.com/en/research-report/biostimulants-and-biopesticides-2021-2031-technologies-markets-and-forecasts/773 (2023).

  6. Markets and Markets. Aricultural biologicals market by function, product type (microbials, macrobials, semiochemicals, natural products), mode of application (foliar spray, soil & seed treatment), crop type (cereals & grains, fruits) & region - global forecast to 2028. marketsandmarkets.com https://www.marketsandmarkets.com/Market-Reports/agricultural-biological-market-100393324.html (2023).

  7. Singh, B. K. et al. Climate change impacts on plant pathogens, food security and paths forward. Nat. Rev. Microbiol. 21, 640–656 (2023).

    Article  CAS  PubMed  Google Scholar 

  8. Jansson, J. K. Microorganisms, climate change, and the Sustainable Development Goals: progress and challenges. Nat. Rev. Microbiol. 21, 622–623 (2023). This paper highlights the importance of microorganisms in biogeochemical cycles and ecosystem functioning. The author claims that microbiology research is key to mitigate climate change, and to maintain the health of terrestrial and aquatic ecosystems and thus to reaching SDGs.

    Article  CAS  PubMed  Google Scholar 

  9. Li, J., Wang, J., Liu, H., Macdonald, C. A. & Singh, B. K. Application of microbial inoculants significantly enhances crop productivity: a meta‐analysis of studies from 2010 to 2020. J. Sustain. Agric. Environ. 1, 216–225 (2022).

    Article  Google Scholar 

  10. French, E., Kaplan, I., Iyer-Pascuzzi, A., Nakatsu, C. H. & Enders, L. Emerging strategies for precision microbiome management in diverse agroecosystems. Nat. Plants 7, 256–267 (2021).

    Article  PubMed  Google Scholar 

  11. Zhan, C., Matsumoto, H., Liu, Y. & Wang, M. Pathways to engineering the phyllosphere microbiome for sustainable crop production. Nat. Food 3, 997–1004 (2022).

    Article  PubMed  Google Scholar 

  12. Russ, D., Fitzpatrick, C. R., Teixeira, P. J. P. L. & Dangl, J. L. Deep discovery informs difficult deployment in plant microbiome science. Cell 186, 4496–4513 (2023).

    Article  CAS  PubMed  Google Scholar 

  13. Sessitsch, A. et al. Microbiome interconnectedness throughout environments with major consequences for healthy people and a healthy planet. Microbiol. Mol. Biol. Rev. 87, e0021222 (2023).

    Article  PubMed  Google Scholar 

  14. D’Hondt, K. et al. Microbiome innovations for a sustainable future. Nat. Microbiol. 6, 138–142 (2021).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Leach, J. E., Triplett, L. R., Argueso, C. T. & Trivedi, P. Communication in the phytobiome. Cell 169, 587–596 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Berg, G. et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 8, 103 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Philippot, L., Raaijmakers, J. M., Lemanceau, P. & van der Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Zhalnina, K. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3, 470–480 (2018). This paper shows that a wild oat genotype shows consistent patterns in the chemical composition of root exudates. The plant exudation trait is in line with microbial metabolite substrate preferences for organic aromatic acids, which are predictable from microbial genome sequences.

    Article  CAS  PubMed  Google Scholar 

  20. Kong, H. G., Song, G. C., Sim, H.-J. & Ryu, C.-M. Achieving similar root microbiota composition in neighbouring plants through airborne signalling. ISME J. 15, 397–408 (2021).

    Article  CAS  PubMed  Google Scholar 

  21. Compant, S., Mitter, B., Colli-Mull, J. G., Gangl, H. & Sessitsch, A. 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 (2011).

    Article  PubMed  Google Scholar 

  22. Shade, A., McManus, P. S. & Handelsman, J. Unexpected diversity during community succession in the apple flower microbiome. mBio 4, e00602-12 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Escobar Rodríguez, C. et al. Roots and panicles of the C4 model grasses Setaria viridis (L). and S. pumila host distinct bacterial assemblages with core taxa conserved across host genotypes and sampling sites. Front. Microbiol. 9, 2708 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Mitter, B. et al. A new approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds. Front. Microbiol. 8, 11 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Gagic, M. et al. Seed transmission of Epichloë endophytes in Lolium perenne is heavily influenced by host genetics. Front. Plant Sci. 9, 1580 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hacquard, S. et al. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17, 603–616 (2015).

    Article  CAS  PubMed  Google Scholar 

  27. Faist, H. et al. Potato root-associated microbiomes adapt to combined water and nutrient limitation and have a plant genotype-specific role for plant stress mitigation. Environ. Microbiome 18, 18 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Coleman‐Derr, D. et al. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 209, 798–811 (2016).

    Article  PubMed  Google Scholar 

  29. Compant, S., Samad, A., Faist, H. & Sessitsch, A. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J. Adv. Res. 19, 29–37 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Fitzpatrick, C. R. et al. The plant microbiome: from ecology to reductionism and beyond. Annu. Rev. Microbiol. 74, 81–100 (2020).

    Article  CAS  PubMed  Google Scholar 

  31. 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 

  32. Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl Acad. Sci. USA 110, 6548–6553 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wagner, M. R. et al. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 7, 12151 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L. & Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807–838 (2013).

    Article  CAS  PubMed  Google Scholar 

  35. Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–840 (2012).

    Article  CAS  PubMed  Google Scholar 

  36. Seabloom, E. W. et al. Globally consistent response of plant microbiome diversity across hosts and continents to soil nutrients and herbivores. Nat. Commun. 14, 3516 (2023). This study presents plant microbiome diversity of the leaf, spanning global-scale environmental gradients in different grassland ecosystems, with results indicating that general principles may govern microbiome diversity across spatial scales and host species.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Toju, H. et al. Core microbiomes for sustainable agroecosystems. Nat. Plants 4, 247–257 (2018).

    Article  PubMed  Google Scholar 

  38. Lemanceau, P., Blouin, M., Muller, D. & Moënne-Loccoz, Y. Let the core microbiota be functional. Trends Plant. Sci. 22, 583–595 (2017). The authors propose the definition of functional core microbiota that provide essential functions for the plant holobionts. These functions are enriched by enhanced horizontal transfers of genes with essential functions and by ecological enrichment of carrying microorganisms.

    Article  CAS  PubMed  Google Scholar 

  39. Cassán, F. et al. Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur. J. Soil Biol. 45, 28–35 (2009).

    Article  Google Scholar 

  40. Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Banerjee, S., Schlaeppi, K. & van der Heijden, M. G. A. Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16, 567–576 (2018).

    Article  CAS  PubMed  Google Scholar 

  42. van der Heijden, M. G. A. & Hartmann, M. Networking in the plant microbiome. PLoS Biol. 14, e1002378 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Hol, W. H. G. et al. Context dependency and saturating effects of loss of rare soil microbes on plant productivity. Front. Plant Sci. 6, 485 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Venturi, V. & Keel, C. Signaling in the rhizosphere. Trends Plant Sci. 21, 187–198 (2016).

    Article  CAS  PubMed  Google Scholar 

  45. Peters, N. K., Frost, J. W. & Long, S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233, 977–980 (1986).

    Article  CAS  PubMed  Google Scholar 

  46. Gibelin‐Viala, C. et al. The Medicago truncatula LysM receptor‐like kinase LYK9 plays a dual role in immunity and the arbuscular mycorrhizal symbiosis. New Phytol. 223, 1516–1529 (2019).

    Article  PubMed  Google Scholar 

  47. Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63 (2011).

    Article  CAS  PubMed  Google Scholar 

  48. Nasir, F. et al. Strigolactones shape the rhizomicrobiome in rice (Oryza sativa). Plant Sci. 286, 118–133 (2019).

    Article  CAS  PubMed  Google Scholar 

  49. Han, S.-W. & Yoshikuni, Y. Microbiome engineering for sustainable agriculture: using synthetic biology to enhance nitrogen metabolism in plant-associated microbes. Curr. Opin. Microbiol. 68, 102172 (2022).

    Article  CAS  PubMed  Google Scholar 

  50. Hu, L. et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Voges, M. J. E. E. E., Bai, Y., Schulze-Lefert, P. & Sattely, E. S. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proc. Natl Acad. Sci. USA 116, 12558–12565 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Cotton, T. E. A. et al. Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME J. 13, 1647–1658 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Huang, A. C. et al. A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364, eaau6389 (2019).

    Article  CAS  PubMed  Google Scholar 

  54. Koprivova, A. et al. Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains. Proc. Natl Acad. Sci. USA 116, 15735–15744 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Pascale, A., Proietti, S., Pantelides, I. S. & Stringlis, I. A. Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front. Plant. Sci. 10, 1741 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Venturi, V. & Bez, C. A call to arms for cell–cell interactions between bacteria in the plant microbiome. Trends Plant Sci. 26, 1126–1132 (2021).

    Article  CAS  PubMed  Google Scholar 

  57. Teixeira, P. J. P., Colaianni, N. R., Fitzpatrick, C. R. & Dangl, J. L. Beyond pathogens: microbiota interactions with the plant immune system. Curr. Opin. Microbiol. 49, 7–17 (2019). This paper reports that plants possess specific receptors to perceive microbial molecules not only from pathogenic but also from commensal microorganisms, which can also suppress or evade immune response of the host. It is also proposed that as a consequence the plant immune system shapes the microbiome.

    Article  CAS  PubMed  Google Scholar 

  58. Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  59. Stringlis, I. A. et al. Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. Plant J. 93, 166–180 (2018).

    Article  CAS  PubMed  Google Scholar 

  60. Carvalhais, L. C., Schenk, P. M. & Dennis, P. G. Jasmonic acid signalling and the plant holobiont. Curr. Opin. Microbiol. 37, 42–47 (2017).

    Article  CAS  PubMed  Google Scholar 

  61. Lebeis, S. L. et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864 (2015).

    Article  CAS  PubMed  Google Scholar 

  62. Liu, Q., Cheng, L., Nian, H., Jin, J. & Lian, T. Linking plant functional genes to rhizosphere microbes: a review. Plant Biotechnol. J. 21, 902–917 (2023).

    Article  PubMed  Google Scholar 

  63. Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011). This article claims the importance of understanding the rhizosphere microbiome to identify disease-suppressive bacteria and introduces the concept of disease-suppressive soils.

    Article  CAS  PubMed  Google Scholar 

  64. Leontidou, K. et al. Plant growth promoting rhizobacteria isolated from halophytes and drought-tolerant plants: genomic characterisation and exploration of phyto-beneficial traits. Sci. Rep. 10, 14857 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Yang, J., Kloepper, J. W. & Ryu, C.-M. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant. Sci. 14, 1–4 (2009). In this paper the authors propose the term IST for bacteria-induced physical and chemical changes in plants that result in enhanced tolerance to abiotic stress.

    Article  CAS  PubMed  Google Scholar 

  66. Granada, C. E., Passaglia, L. M. P., de Souza, E. M. & Sperotto, R. A. Is phosphate solubilization the forgotten child of plant growth-promoting rhizobacteria? Front. Microbiol. 9, 2054 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Ribeiro, I. D. A. et al. Use of mineral weathering bacteria to enhance nutrient availability in crops: a review. Front. Plant Sci. 11, 590774 (2020). This paper shows how microorganisms can solubilize minerals using complexing ligands such as siderophores or specific organic acids, pH change or redox reactions.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Cassán, F. et al. Everything you must know about Azospirillum and its impact on agriculture and beyond. Biol. Fertil. Soils 56, 461–479 (2020).

    Article  Google Scholar 

  69. Liu, J., Yu, X., Qin, Q., Dinkins, R. D. & Zhu, H. The impacts of domestication and breeding on nitrogen fixation symbiosis in legumes. Front. Genet. 11, 583954 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zhang, J. et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37, 676–684 (2019).

    Article  CAS  PubMed  Google Scholar 

  71. Mora, V. et al. Azospirillum argentinense modifies Arabidopsis root architecture through auxin-dependent pathway and flagellin. J. Soil Sci. Plant Nutr. 23, 4543–4557 (2023).

    Article  CAS  Google Scholar 

  72. Ezawa, T. & Saito, K. How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism. New Phytol. 220, 1116–1121 (2018). This paper summarizes the biological strategies of mycorrhizal fungi for phosphate acquisition.

    Article  CAS  PubMed  Google Scholar 

  73. Pellegrino, E. & Bedini, S. Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol. Biochem. 68, 429–439 (2014).

    Article  CAS  Google Scholar 

  74. Samaras, A., Roumeliotis, E., Ntasiou, P. & Karaoglanidis, G. Bacillus subtilis MBI600 promotes growth of tomato plants and induces systemic resistance contributing to the control of soilborne pathogens. Plants 10, 1113 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Yu, Y. et al. Induced systemic resistance for improving plant immunity by beneficial microbes. Plants 11, 386 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Korenblum, E., Massalha, H. & Aharoni, A. Plant–microbe interactions in the rhizosphere via a circular metabolic economy. Plant Cell 34, 3168–3182 (2022). This paper shows that the chemical composition of root exudates affects rhizosphere microbiota and that there is metabolic crosstalk, in which microorganisms change plant metabolism and root exudate profiles by inducing systemic responses and in turn plants provide microhabitats for microbial colonization.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Köhl, J., Kolnaar, R. & Ravensberg, W. J. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front. Plant Sci. 10, 845 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Bravo, A., Likitvivatanavong, S., Gill, S. S. & Soberón, M. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41, 423–431 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Schellenberger, U. et al. A selective insecticidal protein from Pseudomonas for controlling corn rootworms. Science 354, 634–637 (2016).

    Article  CAS  PubMed  Google Scholar 

  80. Islam, W. et al. Insect-fungal-interactions: a detailed review on entomopathogenic fungi pathogenicity to combat insect pests. Microb. Pathog. 159, 105122 (2021).

    Article  CAS  PubMed  Google Scholar 

  81. Dhaliwal, S. S. et al. Biofortification of wheat (Triticum aestivum L.) genotypes with zinc and manganese lead to improve the grain yield and quality in sandy loam soil. Front. Sustain. Food Syst. 7, 1164011 (2023).

    Article  Google Scholar 

  82. Berg, G., Rybakova, D., Grube, M. & Köberl, M. The plant microbiome explored: implications for experimental botany. J. Exp. Bot. 67, 995–1002 (2016).

    Article  CAS  PubMed  Google Scholar 

  83. Bokulich, N. A. et al. Associations among wine grape microbiome, metabolome, and fermentation behavior suggest microbial contribution to regional wine characteristics. mBio 7, e00631-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Todeschini, V. et al. Impact of beneficial microorganisms on strawberry growth, fruit production, nutritional quality, and volatilome. Front. Plant Sci. 9, 1611 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Bona, E. et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza 27, 1–11 (2017).

    Article  CAS  PubMed  Google Scholar 

  86. Devi, P. I., Manjula, M. & Bhavani, R. V. Agrochemicals, environment, and human health. Annu. Rev. Environ. Resour. 47, 399–421 (2022).

    Article  Google Scholar 

  87. FAO & WHO. Pesticide Residues in Food 2019 - Report 2019 - Joint FAO/WHO Meeting on Pesticide Residues (UN FAO & WHO, 2019).

  88. 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 

  89. Collinge, D. B. et al. Biological control of plant diseases – what has been achieved and what is the direction? Plant Pathol. 71, 1024–1047 (2022). This comprehensive review paper on biological control agents covers all aspects of their history, discovery pipeline, modes of action, efficacy improvements, product development, regulations and commercialization.

    Article  Google Scholar 

  90. Ghahremani, Z. et al. Bacillus firmus strain I-1582, a nematode antagonist by itself and through the plant. Front. Plant Sci. 11, 796 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Khan, M. & Tanaka, K. Purpureocillium lilacinum for plant growth promotion and biocontrol against root-knot nematodes infecting eggplant. PLoS ONE 18, e0283550 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Marrone, P. G. Status of the biopesticide market and prospects for new bioherbicides. Pest Manag. Sci. 80, 81–86 (2023). This paper gives an overview of the biopesticide (biocontrol, bioprotection) market.

    Article  PubMed  Google Scholar 

  93. Aynalem, B., Muleta, D., Jida, M., Shemekite, F. & Aseffa, F. Biocontrol competence of Beauveria bassiana, Metarhizium anisopliae and Bacillus thuringiensis against tomato leaf miner, Tuta absoluta Meyrick 1917 under greenhouse and field conditions. Heliyon 8, e09694 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  94. Schütz, L. et al. Improving crop yield and nutrient use efficiency via biofertilization – a global meta-analysis. Front. Plant Sci. 8, 2204 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Backer, R. et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 9, 1473 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Singh, S. K., Wu, X., Shao, C. & Zhang, H. Microbial enhancement of plant nutrient acquisition. Stress Biol. 2, 3 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Owen, D., Williams, A. P., Griffith, G. W. & Withers, P. J. A. Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl. Soil Ecol. 86, 41–54 (2015).

    Article  Google Scholar 

  98. Leggett, M. et al. Maize yield response to a phosphorus-solubilizing microbial inoculant in field trials. J. Agric. Sci. 153, 1464–1478 (2015).

    Article  CAS  PubMed  Google Scholar 

  99. Yakhin, O. I., Lubyanov, A. A., Yakhin, I. A. & Brown, P. H. Biostimulants in plant science: a global perspective. Front. Plant Sci. 7, 2049 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Calvo, P., Nelson, L. & Kloepper, J. W. Agricultural uses of plant biostimulants. Plant Soil 383, 3–41 (2014).

    Article  CAS  Google Scholar 

  101. Olmo, R. et al. Microbiome research as an effective driver of success stories in agrifood systems – a selection of case studies. Front. Microbiol. 13, 834622 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Borriss, R., Dietel, K. & Beifort, P. Selection and use of cold-tolerant Bacillus strains as biological phytostimulators. Patent W02016165685A4 (2016).

  103. Bhardwaj, A. K. et al. Agronomic biofortification of food crops: an emerging opportunity for global food and nutritional security. Front. Plant Sci. 13, 1055278 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Gupta, S., Thokchom, S. D., Koul, M. & Kapoor, R. Arbuscular mycorrhiza mediated mineral biofortification and arsenic toxicity mitigation in Triticum aestivum L. Plant Stress 5, 100086 (2022).

    Article  CAS  Google Scholar 

  105. Ku, Y.-S., Rehman, H. M. & Lam, H.-M. Possible roles of rhizospheric and endophytic microbes to provide a safe and affordable means of crop biofortification. Agronomy 9, 764 (2019).

    Article  CAS  Google Scholar 

  106. Li, J., Van Gerrewey, T. & Geelen, D. A meta-analysis of biostimulant yield effectiveness in field trials. Front. Plant Sci. 13, 836702 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Konar, A. & Datta, S. in Industrial Microbiology and Biotechnology (ed. Verma, P.) 169–193 (Springer, 2022).

  108. Giddings, G. The release of genetically engineered micro‐organisms and viruses into the environment. New Phytol. 140, 173–184 (1998).

    Article  PubMed  Google Scholar 

  109. Miller, T. A. et al. Dissection of the epoxyjanthitrem pathway in Epichloë sp. LpTG-3 strain AR37 by CRISPR gene editing. Front. Fungal Biol. 3, 944234 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Kawall, K. The generic risks and the potential of SDN-1 applications in crop plants. Plants 10, 2259 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Guo, K., Yang, J., Yu, N., Luo, L. & Wang, E. Biological nitrogen fixation in cereal crops: progress, strategies, and perspectives. Plant Commun. 4, 100499 (2023).

    Article  CAS  PubMed  Google Scholar 

  112. Wen, A. et al. Enabling biological nitrogen fixation for cereal crops in fertilized fields. ACS Synth. Biol. 10, 3264–3277 (2021).

    Article  CAS  PubMed  Google Scholar 

  113. Albright, M. B. N. et al. Solutions in microbiome engineering: prioritizing barriers to organism establishment. ISME J. 16, 331–338 (2022).

    Article  PubMed  Google Scholar 

  114. Arif, I., Batool, M. & Schenk, P. M. Plant microbiome engineering: expected benefits for improved crop growth and resilience. Trends Biotechnol. 38, 1385–1396 (2020).

    Article  CAS  PubMed  Google Scholar 

  115. Jing, J., Cong, W.-F. & Bezemer, T. M. Legacies at work: plant-soil-microbiome interactions underpinning agricultural sustainability. Trends Plant Sci. 27, 781–792 (2022).

    Article  CAS  PubMed  Google Scholar 

  116. Ke, J., Wang, B. & Yoshikuni, Y. Microbiome engineering: synthetic biology of plant-associated microbiomes in sustainable agriculture. Trends Biotechnol. 39, 244–261 (2021).

    Article  CAS  PubMed  Google Scholar 

  117. Li, T. et al. Soil antibiotic abatement associates with the manipulation of soil microbiome via long-term fertilizer application. J. Hazard. Mater. 439, 129704 (2022).

    Article  CAS  PubMed  Google Scholar 

  118. Mitter, B., Brader, G., Pfaffenbichler, N. & Sessitsch, A. Next generation microbiome applications for crop production — limitations and the need of knowledge-based solutions. Curr. Opin. Microbiol. 49, 59–65 (2019).

    Article  CAS  PubMed  Google Scholar 

  119. Liu, X., Mei, S. & Salles, J. F. Inoculated microbial consortia perform better than single strains in living soil: a meta-analysis. Appl. Soil Ecol. 190, 105011 (2023).

    Article  Google Scholar 

  120. Hu, J. et al. Probiotic diversity enhances rhizosphere microbiome function and plant disease suppression. mBio 7, e01790-16 (2016). This paper shows how defined consortia of pseudomonads suppress pathogen populations and that the survival of the introduced consortia increases with increasing diversity.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Wang, X. et al. Phage combination therapies for bacterial wilt disease in tomato. Nat. Biotechnol. 37, 1513–1520 (2019).

    Article  CAS  PubMed  Google Scholar 

  122. Zhang, L. et al. Long-term field application of a plant growth-promoting rhizobacterial consortium suppressed root-knot disease by shaping the rhizosphere microbiota. Plant Dis. 108, 94–103 (2023).

    Article  Google Scholar 

  123. Hu, J. et al. Introduction of probiotic bacterial consortia promotes plant growth via impacts on the resident rhizosphere microbiome. Proc. R. Soc. B Biol. Sci. 288, 20211396 (2021).

    Article  CAS  Google Scholar 

  124. Liu, H. et al. Effective colonisation by a bacterial synthetic community promotes plant growth and alters soil microbial community. J. Sustain. Agric. Environ. 1, 30–42 (2022).

    Article  Google Scholar 

  125. Finkel, O. M., Castrillo, G., Herrera Paredes, S., Salas González, I. & Dangl, J. L. Understanding and exploiting plant beneficial microbes. Curr. Opin. Plant Biol. 38, 155–163 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  126. Schäfer, M., Vogel, C. M., Bortfeld-Miller, M., Mittelviefhaus, M. & Vorholt, J. A. Mapping phyllosphere microbiota interactions in planta to establish genotype–phenotype relationships. Nat. Microbiol. 7, 856–867 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Delgado‐Baquerizo, M. Simplifying the complexity of the soil microbiome to guide the development of next‐generation SynComs. J. Sustain. Agric. Environ. 1, 9–15 (2022).

    Article  Google Scholar 

  128. Gerrits, G. M. et al. Synthesis on the effectiveness of soil translocation for plant community restoration. J. Appl. Ecol. 60, 714–724 (2023).

    Article  Google Scholar 

  129. 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 

  130. Chen, Q.-L. et al. Potential of indigenous crop microbiomes for sustainable agriculture. Nat. Food 2, 233–240 (2021).

    Article  CAS  PubMed  Google Scholar 

  131. Raaijmakers, J. M. & Kiers, E. T. Rewilding plant microbiomes. Science 378, 599–600 (2022).

    Article  CAS  PubMed  Google Scholar 

  132. Kaur, S. et al. Synthetic community improves crop performance and alters rhizosphere microbial communities. J. Sustain. Agric. Environ. 1, 118–131 (2022).

    Article  Google Scholar 

  133. Berg, G., Kusstatscher, P., Abdelfattah, A., Cernava, T. & Smalla, K. Microbiome modulation – toward a better understanding of plant microbiome response to microbial inoculants. Front. Microbiol. 12, 650610 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  134. Li, G., Liu, T., Whalen, J. K. & Wei, Z. Nematodes: an overlooked tiny engineer of plant health. Trends Plant Sci. 29, 52–63 (2023).

    Article  CAS  PubMed  Google Scholar 

  135. Khan Mirzaei, M. & Deng, L. New technologies for developing phage-based tools to manipulate the human microbiome. Trends Microbiol. 30, 131–142 (2022).

    Article  CAS  PubMed  Google Scholar 

  136. Badri, D. V., Chaparro, J. M., Zhang, R., Shen, Q. & Vivanco, J. M. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J. Biol. Chem. 288, 4502–4512 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Robertson-Albertyn, S. et al. Root hair mutations displace the barley rhizosphere microbiota. Front. Plant Sci. 8, 1094 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Ramírez-Flores, M. R. et al. The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation. eLife 9, e61701 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  139. Johnson, L. J. et al. The exploitation of epichloae endophytes for agricultural benefit. Fungal Divers. 60, 171–188 (2013).

    Article  Google Scholar 

  140. Johnson, L. J. et al. in Improving Sown Grasslands through Breeding and Management. (eds. Huguenin-Elie, O. et al.) 351–363 (Wageningen Academic Publishers, 2019).

  141. Zhao, L., Walkowiak, S. & Fernando, W. G. D. Artificial intelligence: a promising tool in exploring the phytomicrobiome in managing disease and promoting plant health. Plants 12, 1852 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Chang, H.-X., Haudenshield, J. S., Bowen, C. R. & Hartman, G. L. Metagenome-wide association study and machine learning prediction of bulk soil microbiome and crop productivity. Front. Microbiol. 8, 519 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  143. Gu, Y. et al. Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations. ISME J. 16, 2448–2456 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Herrera Paredes, S. et al. Design of synthetic bacterial communities for predictable plant phenotypes. PLoS Biol. 16, e2003962 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Hernández Medina, R. et al. Machine learning and deep learning applications in microbiome research. ISME Commun. 2, 98 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  146. Kraxberger, K., Antonielli, L., Kostić, T., Reichenauer, T. & Sessitsch, A. Diverse bacteria colonizing leaves and the rhizosphere of lettuce degrade azoxystrobin. Sci. Total Environ. 891, 164375 (2023).

    Article  CAS  PubMed  Google Scholar 

  147. Tétard-Jones, C. & Edwards, R. Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag. Sci. 72, 203–209 (2016).

    Article  PubMed  Google Scholar 

  148. Santos, M. S., Nogueira, M. A. & Hungria, M. Outstanding impact of Azospirillum brasilense strains Ab-V5 and Ab-V6 on the Brazilian agriculture: lessons that farmers are receptive to adopt new microbial inoculants. Rev. Bras. Ciência do Solo 45, e0200128 (2021).

    Article  Google Scholar 

  149. Bejarano, A. & Puopolo, G. in How Research Can Stimulate the Development of Commercial Biological Control Against Plant Diseases (eds. De Cal, A., Melgarejo, P. & Magan, N.) 275–293 (Springer, 2020). [Series eds. Hokkanen, H. M. T. & Yulin Gao, Y. Progress in Biological Control Vol. 21].

  150. Escudero-Martinez, C. et al. Identifying plant genes shaping microbiota composition in the barley rhizosphere. Nat. Commun. 13, 3443 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Berg, G. et al. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol. Ecol. 93, fix050 (2017).

    Article  Google Scholar 

  152. Ryan, M. J. et al. Towards a unified data infrastructure to support European and global microbiome research: a call to action. Environ. Microbiol. 23, 372–375 (2021).

    Article  PubMed  Google Scholar 

  153. Biermann, F. et al. Scientific evidence on the political impact of the Sustainable Development Goals. Nat. Sustain. 5, 795–800 (2022).

    Article  Google Scholar 

  154. Stoepler, T., Elliott, T. & Alisic, E. Scientists must boost input into Sustainable Development Goals. Nature 571, 326–326 (2019).

    Article  CAS  PubMed  Google Scholar 

  155. Dye, C. One Health as a catalyst for sustainable development. Nat. Microbiol. 7, 467–468 (2022).

    Article  CAS  PubMed  Google Scholar 

  156. Yan, Z., Xiong, C., Liu, H. & Singh, B. K. Sustainable agricultural practices contribute significantly to One Health. J. Sustain. Agric. Environ. 1, 165–176 (2022).

    Article  Google Scholar 

  157. Meng, J., Zhang, X., Han, X. & Fan, B. Application and development of biocontrol agents in China. Pathogens 11, 1120 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  158. Basu, A. et al. Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13, 1140 (2021).

    Article  CAS  Google Scholar 

  159. Sundh, I., Del Giudice, T. & Cembalo, L. Reaping the benefits of microorganisms in cropping systems: is the regulatory policy adequate? Microorganisms 9, 1437 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  160. Ashaolu, C. A., Okonkwo, C. O., Njuguna, E. & Ndolo, D. Recommendations for effective and sustainable regulation of biopesticides in Nigeria. Sustainability 14, 2846 (2022).

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank F. Purtscher (AIT) and A. Baillie (AgResearch) for help with drafts of the graphical artwork. S.C. and G.B. received funding from the Bio-Based Industries Joint Undertaking (BBI-JU) for the project BIOVEXO – Biocontrol of Xylella and its vector in olive trees for integrated pest management under grant agreement no. 887281. The BBI-JU receives support from the European Union’s Horizon 2020 Research and Innovation Programme and the Bio-Based Industries consortium. G.B. and A.S. received funding from the European Union for the project Risk Assessment Innovation for Low-risk Pesticides (RATION) under grant agreement no. 101084163. F.C. received funding from the Fondo para la Investigación Científica y Tecnológica (FONCyT), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto (SECyT-UNRC).

Author information

Authors and Affiliations

  1. AIT Austrian Institute of Technology, Vienna, Austria

    Stéphane Compant, Tanja Kostić, Günter Brader, Friederike Trognitz & Angela Sessitsch

  2. National University of Rio Cuarto, Rio Cuarto, Argentina

    Fabricio Cassan

  3. AgResearch Limited, Palmerston North, New Zealand

    Linda Johnson

Authors
  1. Stéphane Compant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabricio Cassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tanja Kostić
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Linda Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Günter Brader
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Friederike Trognitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Angela Sessitsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors researched data for the article. All authors contributed substantially to discussion of the content. All authors wrote the article. S.C. and A.S. reviewed and/or edited the manuscript before submission.

Corresponding author

Correspondence to Angela Sessitsch.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Microbiology thanks Yang Bai and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Disclaimer The content of this publication has not been approved by the United Nations and does not reflect the views of the United Nations or its officials or Member States.

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

Related links

United Nations Sustainable Development Goals: https://www.un.org/sustainabledevelopment

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

Compant, S., Cassan, F., Kostić, T. et al. Harnessing the plant microbiome for sustainable crop production. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01079-1

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41579-024-01079-1

  • Springer Nature Limited

Search

Navigation