Root exudates and microbial metabolites: signals and nutrients in plant-microbe interactions.

Xiaoyan Fan, An-Hui Ge, Shanshan Qi, Yuefeng Guan, Ran Wang, Nan Yu, Ertao Wang
Author Information
  1. Xiaoyan Fan: New Cornerstone Science Laboratory, Key Laboratory of Plant Carbon Capture, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  2. An-Hui Ge: New Cornerstone Science Laboratory, Key Laboratory of Plant Carbon Capture, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  3. Shanshan Qi: New Cornerstone Science Laboratory, Key Laboratory of Plant Carbon Capture, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  4. Yuefeng Guan: School of Life Sciences, Guangzhou University, Guangzhou, 510006, China. guan@gzhu.edu.cn.
  5. Ran Wang: College of Life Sciences, Henan Province Engineering Research Center of Crop Synthetic Biology, Henan Agricultural University, Zhengzhou, 450046, China. wangran@henau.edu.cn.
  6. Nan Yu: Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, 200234, China. nyu@shnu.edu.cn.
  7. Ertao Wang: New Cornerstone Science Laboratory, Key Laboratory of Plant Carbon Capture, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China. etwang@cemps.ac.cn.

Abstract

Plant roots meticulously select and attract particular microbial taxa from the surrounding bulk soil, thereby establishing a specialized and functionally diverse microbial community within the rhizosphere. Rhizosphere metabolites, including root exudates and microbial metabolites, function as both signals and nutrients that govern the assembly of the rhizosphere microbiome, playing crucial roles in mediating communications between plants and microbes. The environment and their feedback loops further influence these intricate interactions. However, whether and how specific metabolites shape plant-microbe interactions and facilitate diverse functions remains obscure. This review summarizes the current progress in plant-microbe communications mediated by chemical compounds and their functions in plant fitness and ecosystem functioning. Additionally, we raise some prospects on future directions for manipulating metabolite-mediated plant-microbe interactions to enhance crop productivity and health. Unveiling the biological roles of specific metabolites produced by plants and microbes will bridge the gap between fundamental research and practical applications.

Keywords

References

  1. Acharya, S.M., Yee, M.O., Diamond, S., Andeer, P.F., Baig, N.F., Aladesanmi, O.T., Northen, T.R., Banfield, J.F., and Chakraborty, R. (2023). Fine scale sampling reveals early differentiation of rhizosphere microbiome from bulk soil in young Brachypodium plant roots. ISME Commun 3, 54. [PMID: 37280433]
  2. Adessi, A., Cruz de Carvalho, R., De Philippis, R., Branquinho, C., and Marques da Silva, J. (2018). Microbial extracellular polymeric substances improve water retention in dryland biological soil crusts. Soil Biol Biochem 116, 67–69. [DOI: 10.1016/j.soilbio.2017.10.002]
  3. Alami, M.M., Xue, J., Ma, Y., Zhu, D., Abbas, A., Gong, Z., and Wang, X. (2020). Structure, function, diversity, and composition of fungal communities in rhizospheric soil of coptis chinensis franch under a successive cropping system. Plants 9, 244. [PMID: 32070003]
  4. Almpanis, A., Swain, M., Gatherer, D., and McEwan, N. (2018). Correlation between bacterial G+C content, genome size and the G+C content of associated plasmids and bacteriophages. Microb Genomics 4, e000168. [DOI: 10.1099/mgen.0.000168]
  5. Aylward, J., Steenkamp, E.T., Dreyer, L.L., Roets, F., Wingfield, B.D., and Wingfield, M. J. (2017). A plant pathology perspective of fungal genome sequencing. IMA Fungus 8, 1–15. [PMID: 28824836]
  6. Banerjee, S., and van der Heijden, M.G.A. (2023). Soil microbiomes and one health. Nat Rev Microbiol 21, 6–20. [PMID: 35999468]
  7. Bardgett, R.D., Mommer, L., and De Vries, F.T. (2014). Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29, 692–699. [PMID: 25459399]
  8. Bauermeister, A., Mannochio-Russo, H., Costa-Lotufo, L.V., Jarmusch, A.K., and Dorrestein, P.C. (2022). Mass spectrometry-based metabolomics in microbiome investigations. Nat Rev Microbiol 20, 143–160. [PMID: 34552265]
  9. Beilsmith, K., Thoen, M.P.M., Brachi, B., Gloss, A.D., Khan, M.H., and Bergelson, J. (2019). Genome-wide association studies on the phyllosphere microbiome: embracing complexity in host–microbe interactions. Plant J 97, 164–181. [PMID: 30466152]
  10. Berendsen, R.L., Pieterse, C.M.J., and Bakker, P.A.H.M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci 17, 478–486. [PMID: 22564542]
  11. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E.V.L., and Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64, 807–838. [PMID: 23373698]
  12. Canarini, A., Kaiser, C., Merchant, A., Richter, A., and Wanek, W. (2019). Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10, 157. [PMID: 30881364]
  13. Carlström, C.I., Field, C.M., Bortfeld-Miller, M., Müller, B., Sunagawa, S., and Vorholt, J.A. (2019). Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat Ecol Evol 3, 1445–1454. [PMID: 31558832]
  14. Carrión, V.J., Perez-Jaramillo, J., Cordovez, V., Tracanna, V., de Hollander, M., Ruiz-Buck, D., Mendes, L.W., van Ijcken, W.F.J., Gomez-Exposito, R., Elsayed, S.S., et al. (2019). Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366, 606–612. [PMID: 31672892]
  15. Chai, Y.N., and Schachtman, D.P. (2022). Root exudates impact plant performance under abiotic stress. Trends Plant Sci 27, 80–91. [PMID: 34481715]
  16. Chakraborty, S., Venkataraman, M., Infante, V., Pfleger, B.F., and Ané, J.M. (2024). Scripting a new dialogue between diazotrophs and crops. Trends Microbiol 32, 577–589. [PMID: 37770375]
  17. Chantranupong, L., Wolfson, R.L., and Sabatini, D.M. (2015). Nutrient-sensing mechanisms across evolution. Cell 161, 67–83. [PMID: 25815986]
  18. Chari, N.R., and Taylor, B.N. (2022). Soil organic matter formation and loss are mediated by root exudates in a temperate forest. Nat Geosci 15, 1011–1016. [DOI: 10.1038/s41561-022-01079-x]
  19. Culp, E.J., and Goodman, A.L. (2023). Cross-feeding in the gut microbiome: ecology and mechanisms. Cell Host Microbe 31, 485–499. [PMID: 37054671]
  20. D’Souza, G., Shitut, S., Preussger, D., Yousif, G., Waschina, S., and Kost, C. (2018). Ecology and evolution of metabolic cross-feeding interactions in bacteria. Nat Prod Rep 35, 455–488. [PMID: 29799048]
  21. D’Auria, J.C., and Gershenzon, J. (2005). The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 8, 308–316. [PMID: 15860428]
  22. de Vries, F.T., Williams, A., Stringer, F., Willcocks, R., McEwing, R., Langridge, H., and Straathof, A.L. (2019). Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytol 224, 132–145. [PMID: 31218693]
  23. Deng, S., Caddell, D.F., Xu, G., Dahlen, L., Washington, L., Yang, J., and Coleman-Derr, D. (2021). Genome wide association study reveals plant loci controlling heritability of the rhizosphere microbiome. ISME J 15, 3181–3194. [PMID: 33980999]
  24. Van Deynze, A., Zamora, P., Delaux, P.M., Heitmann, C., Jayaraman, D., Rajasekar, S., Graham, D., Maeda, J., Gibson, D., Schwartz, K.D., et al. (2018). Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota. PLoS Biol 16, e2006352. [PMID: 30086128]
  25. Ding, W., Cong, W.F., and Lambers, H. (2021). Plant phosphorus-acquisition and -use strategies affect soil carbon cycling. Trends Ecol Evol 36, 899–906. [PMID: 34246498]
  26. Edwards, J.A., Saran, U.B., Bonnette, J., MacQueen, A., Yin, J., Nguyen, T., Schmutz, J., Grimwood, J., Pennacchio, L.A., Daum, C., et al. (2023). Genetic determinants of switchgrass-root-associated microbiota in field sites spanning its natural range. Curr Biol 33, 1926–1938.e6. [PMID: 37080198]
  27. Flemming, H.C., van Hullebusch, E.D., Little, B.J., Neu, T.R., Nielsen, P.H., Seviour, T., Stoodley, P., Wingender, J., and Wuertz, S. (2025). Microbial extracellular polymeric substances in the environment, technology and medicine. Nat Rev Microbiol 23, 87–105. [PMID: 39333414]
  28. Flemming, H.C., and Wuertz, S. (2019). Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17, 247–260. [PMID: 30760902]
  29. Fortier, M., Lemaitre, V., Gaudry, A., Pawlak, B., Driouich, A., Follet-Gueye, M.L., and Vicré, M. (2023). A fine-tuned defense at the pea root caps: involvement of border cells and arabinogalactan proteins against soilborne diseases. Front Plant Sci 14, 1132132. [PMID: 36844081]
  30. Fujino, N., Tenma, N., Waki, T., Ito, K., Komatsuzaki, Y., Sugiyama, K., Yamazaki, T., Yoshida, S., Hatayama, M., Yamashita, S., et al. (2018). Physical interactions among flavonoid enzymes in snapdragon and torenia reveal the diversity in the flavonoid metabolon organization of different plant species. Plant J 94, 372–392. [PMID: 29421843]
  31. Getzke, F., Hassani, M.A., Crüsemann, M., Malisic, M., Zhang, P., Ishigaki, Y., Böhringer, N., Jiménez Fernández, A., Wang, L., Ordon, J., et al. (2023). Cofunctioning of bacterial exometabolites drives root microbiota establishment. Proc Natl Acad Sci USA 120, e2221508120. [PMID: 37018204]
  32. Gu, Y., Wei, Z., Wang, X., Friman, V.P., Huang, J., Wang, X., Mei, X., Xu, Y., Shen, Q., and Jousset, A. (2016). Pathogen invasion indirectly changes the composition of soil microbiome via shifts in root exudation profile. Biol Fertil Soils 52, 997–1005. [DOI: 10.1007/s00374-016-1136-2]
  33. Guerrieri, E., and Rasmann, S. (2024). Exposing belowground plant communication. Science 384, 272–273. [PMID: 38635697]
  34. Guo, K., Yang, J., Yu, N., Luo, L., and Wang, E. (2023). Biological nitrogen fixation in cereal crops: progress, strategies, and perspectives. Plant Commun 4, 100499. [PMID: 36447432]
  35. Haichar, F.Z., Santaella, C., Heulin, T., and Achouak, W. (2014). Root exudates mediated interactions belowground. Soil Biol Biochem 77, 69–80. [DOI: 10.1016/j.soilbio.2014.06.017]
  36. Hasegawa, M., Mitsuhara, I., Seo, S., Imai, T., Koga, J., Okada, K., Yamane, H., and Ohashi, Y. (2010). Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol Plant Microbe Interact 23, 1000–1011. [PMID: 20615111]
  37. Haskett, T.L., Paramasivan, P., Mendes, M.D., Green, P., Geddes, B.A., Knights, H.E., Jorrin, B., Ryu, M.H., Brett, P., Voigt, C.A., et al. (2022). Engineered plant control of associative nitrogen fixation. Proc Natl Acad Sci USA 119, e2117465119. [PMID: 35412890]
  38. He, J., Dai, H., Zhang, X., and Wang, E. (2024). Mycorrhizal signals promote root development dependent on LysM-receptor like kinases in rice. New Crops 1, 100009. [DOI: 10.1016/j.ncrops.2023.12.004]
  39. Herrera Paredes, S., Gao, T., Law, T.F., Finkel, O.M., Mucyn, T., Teixeira, P.J.P.L., Salas González, I., Feltcher, M.E., Powers, M.J., Shank, E.A., et al. (2018). Design of synthetic bacterial communities for predictable plant phenotypes. PLoS Biol 16, e2003962. [PMID: 29462153]
  40. Hoysted, G.A., Bell, C.A., Lilley, C.J., and Urwin, P.E. (2018). Aphid colonization affects potato root exudate composition and the hatching of a soil borne pathogen. Front Plant Sci 9, 1278. [PMID: 30237805]
  41. Hu, Q., Liu, H., He, Y., Hao, Y., Yan, J., Liu, S., Huang, X., Yan, Z., Zhang, D., Ban, X., et al. (2024). Regulatory mechanisms of strigolactone perception in rice. Cell 187, 7551–7567.e17. [PMID: 39500324]
  42. Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B., Goossens, A., Nützmann, H.W., Bai, Y., and Osbourn, A. (2019). A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364, eaau6389. [PMID: 31073042]
  43. Jain, D., Kour, R., Bhojiya, A.A., Meena, R.H., Singh, A., Mohanty, S.R., Rajpurohit, D., and Ameta, K.D. (2020). Zinc tolerant plant growth promoting bacteria alleviates phytotoxic effects of zinc on maize through zinc immobilization. Sci Rep 10, 13865. [PMID: 32807871]
  44. Jiang, Y., Wang, W., Xie, Q., Liu, N., Liu, L., Wang, D., Zhang, X., Yang, C., Chen, X., Tang, D., et al. (2017). Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175. [PMID: 28596307]
  45. Jin, L., Song, Z., Cai, F., Ruan, L., and Jiang, R. (2022). Chemistry and biological activities of naturally occurring and structurally modified podophyllotoxins. Molecules 28, 302. [PMID: 36615496]
  46. Kamali, A., Ziadlou, R., Lang, G., Pfannkuche, J., Cui, S., Li, Z., Richards, R.G., Alini, M., and Grad, S. (2021). Small molecule-based treatment approaches for intervertebral disc degeneration: current options and future directions. Theranostics 11, 27–47. [PMID: 33391459]
  47. Kaur, U., Johnson, D.T., Chea, E.E., Deredge, D.J., Espino, J.A., and Jones, L.M. (2019). Evolution of structural biology through the lens of mass spectrometry. Anal Chem 91, 142–155. [PMID: 30457831]
  48. Kirwa, H.K., Murungi, L.K., Beck, J.J., and Torto, B. (2018). Elicitation of differential responses in the root-knot nematode Meloidogyne incognita to tomato root exudate cytokinin, flavonoids, and alkaloids. J Agric Food Chem 66, 11291–11300. [PMID: 30346752]
  49. Knudsen, J.T., Eriksson, R., Gershenzon, J., and Ståhl, B. (2006). Diversity and distribution of floral scent. Botanical Rev 72, 1–120. [DOI: 10.1663/0006-8101(2006)72[1]
  50. Korenblum, E., Dong, Y., Szymanski, J., Panda, S., Jozwiak, A., Massalha, H., Meir, S., Rogachev, I., and Aharoni, A. (2020). Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling. Proc Natl Acad Sci USA 117, 3874–3883. [PMID: 32015118]
  51. Kost, C., Patil, K.R., Friedman, J., Garcia, S.L., and Ralser, M. (2023). Metabolic exchanges are ubiquitous in natural microbial communities. Nat Microbiol 8, 2244–2252. [PMID: 37996708]
  52. Kumar, L., Patel, S.K.S., Kharga, K., Kumar, R., Kumar, P., Pandohee, J., Kulshresha, S., Harjai, K., and Chhibber, S. (2022). Molecular mechanisms and applications of N-acyl homoserine lactone-mediated quorum sensing in bacteria. Molecules 27, 7584. [PMID: 36364411]
  53. Lebeis, S.L., Paredes, S.H., Lundberg, D.S., Breakfield, N., Gehring, J., McDonald, M., Malfatti, S., Glavina del Rio, T., Jones, C.D., Tringe, S.G., et al. (2015). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864. [PMID: 26184915]
  54. Lei, X., Shen, Y., Zhao, J., Huang, J., Wang, H., Yu, Y., and Xiao, C. (2023). Root exudates mediate the processes of soil organic carbon input and efflux. Plants 12, 630. [PMID: 36771714]
  55. Li, C., Haider, I., Wang, J.Y., Quinodoz, P., Suarez Duran, H.G., Méndez, L.R., Horber, R., Fiorilli, V., Votta, C., Lanfranco, L., et al. (2024). OsCYP706C2 diverts rice strigolactone biosynthesis to a noncanonical pathway branch. Sci Adv 10, eadq3942. [PMID: 39196928]
  56. Li, X., Chou, M.Y., Bonito, G.M., and Last, R.L. (2023a). Anti-fungal bioactive terpenoids in the bioenergy crop switchgrass (Panicum virgatum) may contribute to ecotype-specific microbiome composition. Commun Biol 6, 917. [PMID: 37679469]
  57. Li, Y., Long, M., Hou, Y., Li, W., Qin, X., Zhang, B., Wen, T., Cui, Y., Wang, Z., and Liao, Y. (2023b). Root exudation processes induce the utilization of microbial-derived components by rhizoplane microbiota under conservation agriculture. Soil Biol Biochem 178, 108956. [DOI: 10.1016/j.soilbio.2023.108956]
  58. Ling, N., Wang, T., and Kuzyakov, Y. (2022). Rhizosphere bacteriome structure and functions. Nat Commun 13, 836. [PMID: 35149704]
  59. Liu, H., Li, J., Carvalhais, L.C., Percy, C.D., Prakash Verma, J., Schenk, P.M., and Singh, B.K. (2020). Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogens. New Phytol 229, 2873–2885. [PMID: 33131088]
  60. Liu, Z., Huang, H., Qi, M., Wang, X., Adebanjo, O.O., Lu, Z., and Liu, S.J. (2019). Metabolite cross-feeding between Rhodococcus ruber YYL and Bacillus cereus MLY1 in the biodegradation of tetrahydrofuran under pH stress. Appl Environ Microbiol 85, e01196-19. [PMID: 31375492]
  61. Loo, E.P.I., Durán, P., Pang, T.Y., Westhoff, P., Deng, C., Durán, C., Lercher, M., Garrido-Oter, R., and Frommer, W.B. (2024). Sugar transporters spatially organize microbiota colonization along the longitudinal root axis of Arabidopsis. Cell Host Microbe 32, 543–556.e6. [PMID: 38479394]
  62. Lu, P., Yang, T., Li, L., Zhao, B., Liu, J., and Sarma, B. (2020). Response of oat morphologies, root exudates, and rhizosphere fungal communities to amendments in a saline-alkaline environment. PLoS One 15, e0243301. [PMID: 33270753]
  63. Luo, J., Gu, S., Guo, X., Liu, Y., Tao, Q., Zhao, H.P., Liang, Y., Banerjee, S., and Li, T. (2022). Core Microbiota in the rhizosphere of heavy metal accumulators and its contribution to plant performance. Environ Sci Technol 56, 12975–12987. [PMID: 36067360]
  64. Ma, Z., Jiang, M., Liu, C., Wang, E., Bai, Y., Yuan, M.M., Shi, S., Zhou, J., Ding, J., Xie, Y., et al. (2024). Quinolone-mediated metabolic cross-feeding develops aluminium tolerance in soil microbial consortia. Nat Commun 15, 10148. [PMID: 39578460]
  65. Martin, F.M., Uroz, S., and Barker, D.G. (2017). Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356, eaad4501. [PMID: 28546156]
  66. McGivern, B.B., Cronin, D.R., Ellenbogen, J.B., Borton, M.A., Knutson, E.L., Freire-Zapata, V., Bouranis, J.A., Bernhardt, L., Hernandez, A.I., Flynn, R.M., et al. (2024). Microbial polyphenol metabolism is part of the thawing permafrost carbon cycle. Nat Microbiol 9, 1454–1466. [PMID: 38806673]
  67. McLaughlin, S., Zhalnina, K., Kosina, S., Northen, T.R., and Sasse, J. (2023). The core metabolome and root exudation dynamics of three phylogenetically distinct plant species. Nat Commun 14, 1649. [PMID: 36964135]
  68. Meier, I.C., Avis, P.G., and Phillips, R.P. (2013). Fungal communities influence root exudation rates in pine seedlings. FEMS Microbiol Ecol 83, 585–595. [PMID: 23013386]
  69. Morris, J.J., Lenski, R.E., and Zinser, E.R. (2012). The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036-12. [PMID: 22448042]
  70. Ni, H., Jing, X., Xiao, X., Zhang, N., Wang, X., Sui, Y., Sun, B., and Liang, Y. (2021). Microbial metabolism and necromass mediated fertilization effect on soil organic carbon after long-term community incubation in different climates. ISME J 15, 2561–2573. [PMID: 33712697]
  71. Oldroyd, G.E.D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11, 252–263. [PMID: 23493145]
  72. Panchal, P., Preece, C., Peñuelas, J., and Giri, J. (2022). Soil carbon sequestration by root exudates. Trends Plant Sci 27, 749–757. [PMID: 35606255]
  73. Peiffer, J.A., Spor, A., Koren, O., Jin, Z., Tringe, S.G., Dangl, J.L., Buckler, E.S., and Ley, R.E. (2013). Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110, 6548–6553. [PMID: 23576752]
  74. Qiu, M., Tian, M., Sun, Y., Li, H., Huang, W., Ouyang, H., Lin, S., Zhang, C., Wang, M., and Wang, Y. (2024). Decoding the biochemical dialogue: metabolomic insights into soybean defense strategies against diverse pathogens. Sci China Life Sci 67, 2234–2250. [PMID: 38965141]
  75. Roskova, Z., Skarohlid, R., and McGachy, L. (2022). Siderophores: an alternative bioremediation strategy? Sci Total Environ 819, 153144. [PMID: 35038542]
  76. Ross-Elliott, T.J., Jensen, K.H., Haaning, K.S., Wager, B.M., Knoblauch, J., Howell, A. H., Mullendore, D.L., Monteith, A.G., Paultre, D., Yan, D., et al. (2017). Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle. eLife 6, e24125. [PMID: 28230527]
  77. Russ, D., Fitzpatrick, C.R., Teixeira, P.J.P.L., and Dangl, J.L. (2023). Deep discovery informs difficult deployment in plant microbiome science. Cell 186, 4496–4513. [PMID: 37832524]
  78. Ryback, B., Bortfeld-Miller, M., and Vorholt, J.A. (2022). Metabolic adaptation to vitamin auxotrophy by leaf-associated bacteria. ISME J 16, 2712–2724. [PMID: 35987782]
  79. Sasse, J., Martinoia, E., and Northen, T. (2018). Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23, 25–41. [PMID: 29050989]
  80. Schäfer, M., Pacheco, A.R., Künzler, R., Bortfeld-Miller, M., Field, C.M., Vayena, E., Hatzimanikatis, V., and Vorholt, J.A. (2023). Metabolic interaction models recapitulate leaf microbiota ecology. Science 381, eadf5121. [PMID: 37410834]
  81. Schalk, I.J. (2024). Bacterial siderophores: diversity, uptake pathways and applications. Nat Rev Microbiol 23, 24–40. [PMID: 39251840]
  82. Seitz, V.A., McGivern, B.B., Daly, R.A., Chaparro, J.M., Borton, M.A., Sheflin, A.M., Kresovich, S., Shields, L., Schipanski, M.E., Wrighton, K.C., et al. (2022). Variation in root exudate composition influences soil microbiome membership and function. Appl Environ Microbiol 88, e00226. [PMID: 35536051]
  83. Sharma, P., Sharma, M.M.M., Malik, A., Vashisth, M., Singh, D., Kumar, R., Singh, B., Patra, A., Mehta, S., and Pandey, V. (2021). Rhizosphere, rhizosphere biology, and rhizospheric engineering. In: Mohamed, H.I., El-Beltagi, H.E.-D.S., and Abd-Elsalam, K.A., eds. Plant Growth-Promoting Microbes for Sustainable Biotic and Abiotic Stress Management. Cham: springer International Publishing. 577–624. [DOI: 10.1007/978-3-030-66587-6_21]
  84. Shen, J., Wang, M., and Wang, E. (2024). Exploitation of the microbiome for crop breeding. Nat Plants 10, 533–534. [PMID: 38514786]
  85. Shi, J., Wang, X., and Wang, E. (2023). Mycorrhizal symbiosis in plant growth and stress adaptation: from genes to ecosystems. Annu Rev Plant Biol 74, 569–607. [PMID: 36854473]
  86. Shi, J., Zhao, B., Zheng, S., Zhang, X., Wang, X., Dong, W., Xie, Q., Wang, G., Xiao, Y., Chen, F., et al. (2021). A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell 184, 5527–5540.e18. [PMID: 34644527]
  87. Siddiqi, K.S., and Husen, A. (2020). Current status of plant metabolite-based fabrication of copper/copper oxide nanoparticles and their applications: a review. BioMater Res 24, 11. [PMID: 32514371]
  88. Strehmel, N., Böttcher, C., Schmidt, S., and Scheel, D. (2014). Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry 108, 35–46. [PMID: 25457500]
  89. Sun, H., Jiang, S., Jiang, C., Wu, C., Gao, M., and Wang, Q. (2021). A review of root exudates and rhizosphere microbiome for crop production. Environ Sci Pollut Res 28, 54497–54510. [DOI: 10.1007/s11356-021-15838-7]
  90. Sun, L., Lu, Y., Yu, F., Kronzucker, H.J., and Shi, W. (2016). Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol 212, 646–656. [PMID: 27292630]
  91. Takeuchi, N., Fullmer, M.S., Maddock, D.J., and Poole, A.M. (2024). The Constructive Black Queen hypothesis: new functions can evolve under conditions favouring gene loss. ISME J 18, wrae011. [PMID: 38366199]
  92. Tan, W., Nian, H., Tran, L.S.P., Jin, J., and Lian, T. (2024). Small peptides: novel targets for modulating plant–rhizosphere microbe interactions. Trends Microbiol 32, 1072–1083. [PMID: 38670883]
  93. Tan, X., Wang, D., Zhang, X., Zheng, S., Jia, X., Liu, H., Liu, Z., Yang, H., Dai, H., Chen, X., et al. (2025). A pair of LysM receptors mediates symbiosis and immunity discrimination in Marchantia. Cell, doi: https://doi.org/10.1016/j.cell.2024.12.024 .
  94. Thoms, D., Liang, Y., and Haney, C.H. (2021). Maintaining symbiotic homeostasis: how do plants engage with beneficial microorganisms while at the same time restricting pathogens? Mol Plant Microbe Interact 34, 462–469. [PMID: 33534602]
  95. Tiziani, R., Miras-Moreno, B., Malacrinò, A., Vescio, R., Lucini, L., Mimmo, T., Cesco, S., and Sorgonà, A. (2022). Drought, heat, and their combination impact the root exudation patterns and rhizosphere microbiome in maize roots. Environ Exp Bot 203, 105071. [DOI: 10.1016/j.envexpbot.2022.105071]
  96. Vives-Peris, V., de Ollas, C., Gómez-Cadenas, A., and Pérez-Clemente, R.M. (2020). Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39, 3–17. [PMID: 31346716]
  97. de Vries, F.T., Griffiths, R.I., Knight, C.G., Nicolitch, O., and Williams, A. (2020). Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368, 270–274. [PMID: 32299947]
  98. Walters, W.A., Jin, Z., Youngblut, N., Wallace, J.G., Sutter, J., Zhang, W., González-Peña, A., Peiffer, J., Koren, O., Shi, Q., et al. (2018). Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc Natl Acad Sci USA 115, 7368–7373. [PMID: 29941552]
  99. Wang, B., Zhang, Z., Xu, F., Yang, Z., Li, Z., Shen, D., Wang, L., Wu, H., Li, T., Yan, Q., et al. (2023). Soil bacterium manipulates antifungal weapons by sensing intracellular type IVA secretion system effectors of a competitor. ISME J 17, 2232–2246. [PMID: 37838821]
  100. Wang, D., Dong, W., Murray, J., and Wang, E. (2022a). Innovation and appropriation in mycorrhizal and rhizobial Symbioses. Plant Cell 34, 1573–1599. [PMID: 35157080]
  101. Wang, S., Alseekh, S., Fernie, A.R., and Luo, J. (2019). The structure and function of major plant metabolite modifications. Mol Plant 12, 899–919. [PMID: 31200079]
  102. Wang, X., Feng, H., Wang, Y., Wang, M., Xie, X., Chang, H., Wang, L., Qu, J., Sun, K., He, W., et al. (2021). Mycorrhizal symbiosis modulates the rhizosphere microbiota to promote rhizobia–legume symbiosis. Mol Plant 14, 503–516. [PMID: 33309942]
  103. Wang, Y., Bian, Z., and Wang, Y. (2022b). Biofilm formation and inhibition mediated by bacterial quorum sensing. Appl Microbiol Biotechnol 106, 6365–6381. [PMID: 36089638]
  104. Wang, Y., Wang, X., Sun, S., Jin, C., Su, J., Wei, J., Luo, X., Wen, J., Wei, T., Sahu, S. K., et al. (2022c). GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet. Nat Commun 13, 5913. [PMID: 36207301]
  105. Wang, Z., Li, Z., Zhang, Y., Liao, J., Guan, K., Zhai, J., Meng, P., Tang, X., Dong, T., and Song, Y. (2024). Root hair developmental regulators orchestrate drought triggered microbiome changes and the interaction with beneficial Rhizobiaceae. Nat Commun 15, 10068. [PMID: 39567534]
  106. Wei, Z., and Jousset, A. (2017). Plant breeding goes microbial. Trends Plant Sci 22, 555–558. [PMID: 28592368]
  107. Williams, A., and de Vries, F.T. (2020). Plant root exudation under drought: implications for ecosystem functioning. New Phytol 225, 1899–1905. [PMID: 31571220]
  108. Wright, P. (2011). Metabolite identification by mass spectrometry: forty years of evolution. Xenobiotica 41, 670–686. [PMID: 21434771]
  109. Xi, H., Nie, X., Gao, F., Liang, X., Li, H., Zhou, H., Cai, Y., and Yang, C. (2023). A bacterial spermidine biosynthetic pathway via carboxyaminopropylagmatine. Sci Adv 9, eadj9075. [PMID: 37878710]
  110. Xing, Y., Zhang, P., Zhang, W., Yu, C., and Luo, Z. (2024). Continuous cropping of potato changed the metabolic pathway of root exudates to drive rhizosphere microflora. Front Microbiol 14, 1318586. [PMID: 38249485]
  111. Xiong, Y.W., Li, X.W., Wang, T.T., Gong, Y., Zhang, C.M., Xing, K., and Qin, S. (2020). Root exudates-driven rhizosphere recruitment of the plant growth-promoting rhizobacterium Bacillus flexus KLBMP 4941 and its growth-promoting effect on the coastal halophyte Limonium sinense under salt stress. Ecotoxicol Environ Saf 194, 110374. [PMID: 32120174]
  112. Xu, L., Naylor, D., Dong, Z., Simmons, T., Pierroz, G., Hixson, K.K., Kim, Y.M., Zink, E. M., Engbrecht, K.M., Wang, Y., et al. (2018). Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci USA 115, E4284–E4293. [PMID: 29666229]
  113. Xu, L., Pierroz, G., Wipf, H.M.L., Gao, C., Taylor, J.W., Lemaux, P.G., and Coleman-Derr, D. (2021). Holo-omics for deciphering plant-microbiome interactions. Microbiome 9, 69. [PMID: 33762001]
  114. Xun, W., Ren, Y., Yan, H., Ma, A., Liu, Z., Wang, L., Zhang, N., Xu, Z., Miao, Y., Feng, H., et al. (2023). Sustained inhibition of maize seed-borne Fusarium using a Bacillus-dominated rhizospheric stable core microbiota with unique cooperative patterns. Adv Sci 10, 2205215. [DOI: 10.1002/advs.202205215]
  115. Yang, C., Shen, S., Zhou, S., Li, Y., Mao, Y., Zhou, J., Shi, Y., An, L., Zhou, Q., Peng, W., et al. (2022a). Rice metabolic regulatory network spanning the entire life cycle. Mol Plant 15, 258–275. [PMID: 34715392]
  116. Yang, J., Lan, L., Jin, Y., Yu, N., Wang, D., and Wang, E. (2022b). Mechanisms underlying legume–rhizobium symbioses. J Integr Plant Biol 64, 244–267. [PMID: 34962095]
  117. Yang, R., Shi, Q., Huang, T., Yan, Y., Li, S., Fang, Y., Li, Y., Liu, L., Liu, L., Wang, X., et al. (2023). The natural pyrazolotriazine pseudoiodinine from Pseudomonas mosselii 923 inhibits plant bacterial and fungal pathogens. Nat Commun 14, 734. [PMID: 36759518]
  118. Yang, X., Feng, K., Wang, S., Yuan, M.M., Peng, X., He, Q., Wang, D., Shen, W., Zhao, B., Du, X., et al. (2024). Unveiling the deterministic dynamics of microbial meta-metabolism: a multi-omics investigation of anaerobic biodegradation. Microbiome 12, 166. [PMID: 39244624]
  119. Yin, H., Li, Y., Xiao, J., Xu, Z., Cheng, X., and Liu, Q. (2013). Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob Change Biol 19, 2158–2167. [DOI: 10.1111/gcb.12161]
  120. Youssef, R.M., MacDonald, M.H., Brewer, E.P., Bauchan, G.R., Kim, K.H., and Matthews, B.F. (2013). Ectopic expression of AtPAD4 broadens resistance of soybean to soybean cyst and root-knot nematodes. BMC Plant Biol 13, 67. [PMID: 23617694]
  121. Yu, G., Xu, C., Zhang, D., Ju, F., and Ni, Y. (2022a). MetOrigin: discriminating the origins of microbial metabolites for integrative analysis of the gut microbiome and metabolome. iMeta 1, e10. [PMID: 38867728]
  122. Yu, J.S.L., Correia-Melo, C., Zorrilla, F., Herrera-Dominguez, L., Wu, M.Y., Hartl, J., Campbell, K., Blasche, S., Kreidl, M., Egger, A.S., et al. (2022b). Microbial communities form rich extracellular metabolomes that foster metabolic interactions and promote drug tolerance. Nat Microbiol 7, 542–555. [PMID: 35314781]
  123. Yuan, J., Zhao, J., Wen, T., Zhao, M., Li, R., Goossens, P., Huang, Q., Bai, Y., Vivanco, J.M., Kowalchuk, G.A., et al. (2018). Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6, 156. [PMID: 30208962]
  124. Yue, H., Yue, W., Jiao, S., Kim, H., Lee, Y.H., Wei, G., Song, W., and Shu, D. (2023). Plant domestication shapes rhizosphere microbiome assembly and metabolic functions. Microbiome 11, 70. [PMID: 37004105]
  125. Zhalnina, K., Louie, K.B., Hao, Z., Mansoori, N., da Rocha, U.N., Shi, S., Cho, H., Karaoz, U., Loqué, D., Bowen, B.P., et al. (2018). Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3, 470–480. [PMID: 29556109]
  126. Zhang, J., Liu, Y.X., Zhang, N., Hu, B., Jin, T., Xu, H., Qin, Y., Yan, P., Zhang, X., Guo, X., et al. (2019). NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37, 676–684. [PMID: 31036930]
  127. Zhao, Y., Xue, Q., Wang, M., Meng, B., Jiang, Y., Zhai, R., Zhang, Y., Dai, X., and Fang, X. (2023). Evolution of mass spectrometry instruments and techniques for blood proteomics. J Proteome Res 22, 1009–1023. [PMID: 36932955]
  128. Zhou, J., Wen, Y., Shi, L., Marshall, M.R., Kuzyakov, Y., Blagodatskaya, E., and Zang, H. (2021). Strong priming of soil organic matter induced by frequent input of labile carbon. Soil Biol Biochem 152, 108069. [DOI: 10.1016/j.soilbio.2020.108069]
  129. Zhou, X., Zhang, J., Khashi u Rahman, M., Gao, D., Wei, Z., Wu, F., and Dini-Andreote, F. (2023). Interspecific plant interaction via root exudates structures the disease suppressiveness of rhizosphere microbiomes. Mol Plant 16, 849–864. [PMID: 36935607]
  130. Zhu, S., Vivanco, J.M., and Manter, D.K. (2016). Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107, 324–333. [DOI: 10.1016/j.apsoil.2016.07.009]

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