The dynamic interplay of root exudates and rhizosphere microbiome

Abstract

The rhizosphere microbiome plays a vital role in plant growth, health, and nutrient acquisition. One of the key factors that shape the composition and function of the rhizosphere microbiome is root exudates, the complex mixture of organic compounds released by plant roots. Root exudates serve as a source of energy and nutrients for the rhizosphere microbiome, as well as a means of communication between plants and microbes. The dynamic interplay between root exudates and rhizosphere microbiome is a complex and highly regulated process that involves multiple feedback loops and interactions. Recent studies have revealed that the composition and quantity of root exudates are modulated by a range of biotic and abiotic factors, including plant genotype, soil type, nutrient availability, and microbial community structure. In turn, the rhizosphere microbiome can influence the production and composition of root exudates, through processes such as nutrient cycling, plant hormone synthesis, and modulation of plant defense responses. Understanding the dynamics of root exudates and rhizosphere microbiomes is crucial for developing effective strategies for microbiome engineering, plant-microbe symbiosis, and sustainable agriculture. This review provides an overview of the current state of knowledge on the dynamic interplay between root exudates and rhizosphere microbiomes, highlighting the key factors and mechanisms that govern this complex relationship.

Keywords

• Rhizosphere microbiome
• Root exudates
• Plant-microbe interactions
• Nutrient cycling
• Microbial ecology

References

1. Alphei, J., Bonkowski, M., & Scheu, S. (1996). Protozoa, Nematoda, and Lumbricidae in the rhizosphere of Hordelymus europeaus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia, 106(1), 111-126. http://doi.org/10.1007/BF00334413
2. Arshad, M., & Frankenberger, W. T. (1991). Microbial production of plant hormones. In The Rhizosphere and Plant Growth: Papers presented at a Symposium held May 8–11, 1989, at the Beltsville Agricultural Research Center (BARC), Beltsville, Maryland (pp. 327-334). Springer Netherlands. https://doi.org/10.1007/BF00011893
3. Azcón-Aguilar, C., & Barea, J. M. (1992). Interactions between mycorrhizal fungi and other rhizosphere microorganisms. Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, 163-198.
4. Badri, D. V., & Vivanco, J. M. (2009). Regulation and function of root exudates. Plant, cell & environment, 32(6), 666-681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
5. Bakker, M. G., Manter, D. K., Sheflin, A. M., Weir, T. L., & Vivanco, J. M. (2012). Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant and Soil, 360, 1-13.
6. Bano, S., Wu, X., & Zhang, X. (2021). Towards sustainable agriculture: rhizosphere microbiome engineering. Applied Microbiology and Biotechnology, 1-20. https://doi.org/10.1007/s11104-012-1361-x
7. Beneduzi, A., Ambrosini, A., & Passaglia, L. M. (2012). Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics and molecular biology, 35, 1044-1051. https://doi.org/10.1590/s1415-47572012000600020
8. Bennett, A. J., Bending, G. D., Chandler, D., Hilton, S., & Mills, P. (2012). Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biological reviews, 87(1), 52-71. https://doi.org/10.1111/j.1469-185X.2011.00184.x

9. Berendsen, R. L., Pieterse, C. M., & Bakker, P. A. (2012). The rhizosphere microbiome and plant health. Trends in plant science, 17(8), 478-486. https://doi.org/10.1016/j.tplants.2012.04.001
10. Calvo, P., Nelson, L., & Kloepper, J. W. (2014). Agricultural uses of plant biostimulants. Plant and soil, 383, 3-41. https://doi.org/10.1007/s11104-014-2131-8
11. Carvalhais, L. C., Dennis, P. G., Fan, B., Fedoseyenko, D., Kierul, K., Becker, A., ... & Borriss, R. (2013). Linking plant nutritional status to plant-microbe interactions. PLoS one, 8(7), e68555. https://doi.org/10.1371/journal.pone.0068555
12. Carvalhais, L. C., Dennis, P. G., Fedoseyenko, D., Hajirezaei, M. R., Borriss, R., & von Wirén, N. (2011). Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition and Soil Science, 174(1), 3-11. https://doi.org/10.1002/jpln.201000085
13. Choudhary, D. K., Varma, A., & Tuteja, N. (Eds.). (2016). Plant-microbe interaction: an approach to sustainable agriculture (pp. 1-509). Singapore: Springer. https://doi.org/10.1007/978-981-10-2854-0 De Mandal, S., Singh, S., Hussain, K., & Hussain, T. (2021). Plant–microbe association for mutual benefits for plant growth and soil health. Current trends in microbial biotechnology for sustainable agriculture, 95-121. https://doi.org/10.1007/978-981-15-6949-4_5
14. Etesami, H., & Adl, S. M. (2020). Plant growth-promoting rhizobacteria (PGPR) and their action mechanisms in availability of nutrients to plants. Phyto-microbiome in stress regulation, 147-203. https://doi.org/10.1007/978-981-15-2576-6_9
15. Franzino, T., Boubakri, H., Cernava, T., Abrouk, D., Achouak, W., Reverchon, S., ... & el Zahar Haichar, F. (2022). Implications of carbon catabolite repression for plant-microbe interactions. Plant Communications. https://doi.org/10.1016/j.xplc.2021.100272
16. Frey, S. D. (2019). Mycorrhizal fungi as mediators of soil organic matter dynamics. Annual review of ecology, evolution, and systematics, 50, 237-259. https://doi.org/10.1146/annurev-ecolsys-110617-062331
17. Garcia, J., & Kao-Kniffin, J. (2018). Microbial group dynamics in plant rhizospheres and their implications on nutrient cycling. Frontiers in microbiology, 9, 1516. https://doi.org/10.3389/fmicb.2018.01516
18. Giron, D., Frago, E., Glevarec, G., Pieterse, C. M., & Dicke, M. (2013). Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Functional Ecology, 27(3), 599-609. https://doi.org/10.1111/1365-2435.12042
19. Glick, B. R. (2012). Plant growth-promoting bacteria: mechanisms and applications. Scientifica, 2012. https://doi.org/10.6064/2012/963401
20. Goulet, O., Hojsak, I., Kolacek, S., Pop, T. L., Cokugras, F. C., Zuccotti, G., ... & Fabiano, V. (2019). Paediatricians play a key role in preventing early harmful events that could permanently influence the development of the gut microbiota in childhood. Acta Paediatrica, 108(11), 1942-1954. https://doi.org/10.1111/apa.14900
21. Hartmann, A., Schmid, M., Tuinen, D. V., & Berg, G. (2009). Plant-driven selection of microbes. Plant and Soil, 321, 235–257. https://doi.org/10.1007/s11104-008-9814-y
22. Hassani, M. A., Durán, P., & Hacquard, S. (2018). Microbial interactions within the plant holobiont. Microbiome, 6, 1-17. https://doi.org/10.1186/s40168-018-0445-0
23. Haudiquet, M., de Sousa, J. M., Touchon, M., & Rocha, E. P. (2022). Selfish, promiscuous and sometimes useful: how mobile genetic elements drive horizontal gene transfer in microbial populations. Philosophical Transactions of the Royal Society B, 377(1861), 20210234. https://doi.org/10.1098/rstb.2021.0234
24. Hayat, R., Ali, S., Amara, U., Khalid, R., & Ahmed, I. (2010). Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of microbiology, 60, 579-598. https://doi.org/10.1007/s13213-010-0117-1
25. Igiehon, N. O., & Babalola, O. O. (2018). Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. International journal of environmental research and public health, 15(4), 574. https://doi.org/10.3390/ijerph15040574
26. Jacoby, R., Peukert, M., Succurro, A., Koprivova, A., & Kopriva, S. (2017). The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions. Frontiers in plant science, 8, 1617. https://doi.org/10.3389/fpls.2017.01617
27. Khan, A. G. (2005). Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. Journal of trace Elements in Medicine and Biology, 18(4), 355-364. https://doi.org/10.1016/j.jtemb.2005.02.006.
28. Kotoky, R., Rajkumari, J., & Pandey, P. (2018). The rhizosphere microbiome: Significance in rhizoremediation of polyaromatic hydrocarbon contaminated soil. Journal of environmental management, 217, 858-870. https://doi.org/10.1016/j.jenvman.2018.04.022
29. Kumar, A., & Dubey, A. (2020). Rhizosphere microbiome: Engineering bacterial competitiveness for enhancing crop production. Journal of Advanced Research, 24, 337-352. https://doi.org/10.1016/j.jare.2020.04.014
30. Kumawat, K. C., Razdan, N., & Saharan, K. (2022). Rhizospheric microbiome: Bio-based emerging strategies for sustainable agriculture development and future perspectives. Microbiological Research, 254, 126901. https://doi.org/10.1016/j.micres.2021.126901
31. Kurepin, L. V., Zaman, M., & Pharis, R. P. (2014). Phytohormonal basis for the plant growth promoting action of naturally occurring biostimulators. Journal of the Science of Food and Agriculture, 94(9), 1715-1722. https://doi.org/10.1002/jsfa.6545
32. Li, Y., Gong, X., Xiong, J., Sun, Y., Shu, Y., Niu, D., ... & Zhang, R. (2021). Different dissolved organic matters regulate the bioavailability of heavy metals and rhizosphere microbial activity in a plant-wetland soil system. Journal of Environmental Chemical Engineering, 9(6), 106823. https://doi.org/10.1016/j.jece.2021.106823
33. Lopez-Bucio, J., Nieto-Jacobo, M. F., Ramırez-Rodrıguez, V., & Herrera-Estrella, L. (2000). Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science, 160(1), 1-13. https://doi.org/10.1016/S0168-9452(00)00347-2
34. Mahmud, K., Makaju, S., Ibrahim, R., & Missaoui, A. (2020). Current progress in nitrogen fixing plants and microbiome research. Plants, 9(1), 97. https://doi.org/10.3390/plants9010097
35. Mendes, R., Garbeva, P., & Raaijmakers, J. M. (2013). The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS microbiology reviews, 37(5), 634-663. https://doi.org/10.1111/1574-6976.12028
36. Morgan, J. A. W., Bending, G. D., & White, P. J. (2005). Biological costs and benefits to plant–microbe interactions in the rhizosphere. Journal of experimental botany, 56(417), 1729-1739. https://doi.org/10.1093/jxb/eri205
37. Munoz‐Ucros, J., Zwetsloot, M. J., Cuellar‐Gempeler, C., & Bauerle, T. L. (2021). Spatiotemporal patterns of rhizosphere microbiome assembly: From ecological theory to agricultural application. Journal of Applied Ecology, 58(5), 894-904. https://doi.org/10.1111/1365-2664.13850
38. Nadarajah, K., & Abdul Rahman, N. S. N. (2021). Plant–microbe interaction: aboveground to belowground, from the good to the bad. International Journal of Molecular Sciences, 22(19), 10388. https://doi.org/10.3390/ijms221910388
39. Narula, N., Kothe, E., & Behl, R. K. (2012). Role of root exudates in plant-microbe interactions. Journal of Applied Botany and Food Quality, 82(2), 122-130. https://doi.org/10.1002/9781119246329.ch10
40. Oburger, E., & Jones, D. L. (2018). Sampling root exudates–mission impossible? Rhizosphere, 6, 116-133. https://doi.org/10.1016/j.rhisph.2018.06.004
41. Oppenheimer-Shaanan, Y., Jakoby, G., Starr, M. L., Karliner, R., Eilon, G., Itkin, M., ... & Klein, T. (2022). A dynamic rhizosphere interplay between tree roots and soil bacteria under drought stress. Elife, 11, e79679. https://doi.org/10.7554/eLife.79679
42. Osorio Vega, N. W. (2007). A review on beneficial effects of rhizosphere bacteria on soil nutrient availability and plant nutrient uptake. Revista Facultad Nacional de Agronomía Medellín, 60(1), 3621-3643. Pettit, R. E. (2004). Organic matter, humus, humate, humic acid, fulvic acid and humin: their importance in soil fertility and plant health. CTI Research, 10, 1-7.
43. Pritsch, K., & Garbaye, J. (2011). Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter. Annals of Forest Science, 68, 25-32. https://doi.org/10.1007/s13595-010-0004-8
44. Rengel, Z., & Marschner, P. (2005). Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytologist, 168(2), 305-312. https://doi.org/10.1111/j.1469-8137.2005.01558.x
45. Saad, M. M., Eida, A. A., & Hirt, H. (2020). Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. Journal of Experimental Botany, 71(13), 3878-3901. https://doi.org/10.1093/jxb/eraa111
46. Singh, G., & Mukerji, K. G. (2006). Root exudates as determinant of rhizospheric microbial biodiversity. Microbial activity in the rhizoshere, 39-53. https://doi.org/10.1007/3-540-29420-1_3
47. Ström, L. (1997). Root exudation of organic acids: importance to nutrient availability and the calcifuge and calcicole behaviour of plants. Oikos, 459-466. https://doi.org/10.2307/3546618
48. Tapia-Vázquez, I., Montoya-Martínez, A. C., De los Santos-Villalobos, S., Ek-Ramos, M. J., Montesinos-Matías, R., & Martínez-Anaya, C. (2022). Root-knot nematodes (Meloidogyne spp.) a threat to agriculture in Mexico: Biology, current control strategies, and perspectives. World Journal of Microbiology and Biotechnology, 38(2), 26. https://doi.org/10.1007/s11274-021-03211-2
49. Tiziani, R., Miras-Moreno, B., Malacrinò, A., Vescio, R., Lucini, L., Mimmo, T., ... & Sorgonà, A. (2022). Drought, heat, and their combination impact the root exudation patterns and rhizosphere microbiome in maize roots. Environmental and Experimental Botany, 203, 105071. https://doi.org/10.1016/j.envexpbot.2022.105071
50. Van Loon, L. C. (2007). Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol, 119, 243–254. https://doi.org/10.1007/s10658-007-9165-1
51. Vives-Peris, V., De Ollas, C., Gómez-Cadenas, A., & Pérez-Clemente, R. M. (2020). Root exudates: from plant to rhizosphere and beyond. Plant cell reports, 39, 3-17. https://doi.org/10.1007/s00299-019-02447-5
52. Wang, W., Li, Y., Dang, P., Zhao, S., Lai, D., & Zhou, L. (2018). Rice secondary metabolites: structures, roles, biosynthesis, and metabolic regulation. Molecules, 23(12), 3098. https://doi.org/10.3390/molecules23123098
53. White, L. J., Ge, X., Brözel, V. S., & Subramanian, S. (2017). Root isoflavonoids and hairy root transformation influence key bacterial taxa in the soybean rhizosphere. Environmental Microbiology, 19(4), 1391-1406. https://doi.org/10.1111/1462-2920.13602
54. Yue, H., Yue, W., Jiao, S., Kim, H., Lee, Y. H., Wei, G., ... & Shu, D. (2023). Plant domestication shapes rhizosphere microbiome assembly and metabolic functions. Microbiome, 11(1), 1-19. https://doi.org/10.1186/s40168-023-01513-1
55. Zaunmüller, T., Eichert, M., Richter, H., & Unden, G. (2006). Variations in the energy metabolism of biotechnologically relevant heterofermentative lactic acid bacteria during growth on sugars and organic acids. Applied microbiology and biotechnology, 72, 421-429. https://doi.org/10.1007/s00253-006-0514-3
56. Zehra, A., Raytekar, N. A., Meena, M., & Swapnil, P. (2021). Efficiency of microbial bio-agents as elicitors in plant defense mechanism under biotic stress: A review. Current Research in Microbial Sciences, 2, 100054. https://doi.org/10.1016/j.crmicr.2021.100054