Rhizophagy: A Nutritive Frontier
Rhizophagy, a term derived from the Greek words "rhizo" meaning root and "phagy" meaning eating or consuming, refers to the phenomenon in which certain microorganisms undergo a two-phase life cycle, that alternates between free-living in the rhizosphere surrounding and entering plant roots where the host will subsequently consume their cellular contents. This process constitues a symbiotic relationship between the bacterial or fungal microorganism and the host plant.
Source: White, J. F., Kingsley, K. L., Verma, S. K., & Kowalski, K. P. (2018). Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction from Symbiotic Microbes. Microorganisms, 6(3), 95. https://doi.org/10.3390/microorganisms6030095
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Originally discovered in experiments involving Arabidopsis thailiana and Solanum lycopersicum, researchers inoculated test plants with fluorescent-tagged specially selected non-pathogenic and non-symbiotic strains of Eschericia coli and Saccharomyces cerevisiae and observed plants digesting the intracellular microbes and stripping them of nitrogen which was then utilised to fuel shoot growth. Since this ground-breaking discovery in 2010, scientists have discovered numerous examples of plants employing rhizophagy in a wide range of genera including
Rhizophagy begins with plant recognition of microbes at the developing root tips, which initiates the production of a modified cell wall capturing microbes from the surrounding rhizosphere, as well as plant-derived enzymes which loosen or decay plant cell walls. Microbes are allowed to enter the plant through meristematic tissue, bundles of undifferentiated cells located at the tip of all roots and shoots. A key observation of rhizophagy is that host plants are in control of cellular colonisation whereas in the case of pathogenic and symbiotic microbes cell entry is mediated by the invading organism itself.
Once within the host plant cell architecture the intracellular microbes are exposed to superoxide (O2-) a reactive oxygen species (ROS) that strips the incoming microorganisms of their cell walls, converting them to wallless L-form, allowing their nutrient-rich contents to be absorbed into adjacent plant cells. Most of the microbes which enter a plant will not survive the process of being attacked by superoxide, however some do, and it is the presence of these surviving microbes that triggers the next stage of the rhizophagy cycle.
Surviving microbes, either fungal or bacterial, exit the plants intracellular space through the growing tips of elongating root hairs. Initially they begin to accumulate at the base of immature root hairs, known as initials, feeding on carbon provided by the host and using it to produce ethylene. Once ethylene levels reach a critical point, root hair growth is triggered which returns the microorganisms to the rhizosphere by ejecting them from the tip of the growing root hair and out back into the soil, away from the plant roots where they can acquire more nutrients before moving back to the root tip and restarting the whole cycle of rhizophagy.
Once returned to the rhizosphere both bacterial and fungal endophytes return to scavenging nutrients and rebuilding their cell walls. Immediately outside of plant root growing tips are sloughed cells and carbon-rich root exudates which provide the bacterial and fungal endophytes with a rich source from which they can rebuild their cell walls before once again entering the plant host. In this manner the process of rhizophagy is cyclical and may therefore represent a significant source of plant nutrition that has been previously overlooked in terms of scientific study.
HOST SPECIFICITY
Host ability to produce superoxide mediates rhizophagy activity between plant genera. For example, tomato (Solanum lycopersicum) plants commonly associate with Micrococcus luteus which in Solanum plant species has been shown to engage in rhizophagy. Experiments using Micrococcus luteus to inoculate plant species outside of the Solanum genus did not demonstrate rhizophagy and instead demonstrated a notable reduction in the growth of the host. These findings demonstrate host specificity in rhizophagy, whereby rhizophagic organisms are paired with their host by the selective pressure of host superoxide production – if the plant host cannot produce suitable levels of superoxide to neutralise the incoming microbe it cannot engage in the rhizophagy cycle with that microorganism.
References
Paungfoo-Lonhienne, C., Rentsch, D., Robatzek, S., Webb, R. I., Sagulenko, E., Näsholm, T., Schmidt, S., & Lonhienne, T. G. (2010). Turning the table: plants consume microbes as a source of nutrients. PloS one, 5(7), e11915. https://doi.org/10.1371/journal.pone.0011915
White, J. F., Kingsley, K. L., Verma, S. K., & Kowalski, K. P. (2018). Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction from Symbiotic Microbes. Microorganisms, 6(3), 95. https://doi.org/10.3390/microorganisms6030095
Micci, A., Zhang, Q., Chang, X., Kingsley, K., Park, L., Chiaranunt, P., Strickland, R., Velazquez, F., Lindert, S., Elmore, M., Vines, P. L., Crane, S., Irizarry, I., Kowalski, K. P., Johnston-Monje, D., & White, J. F. (2022). Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms. Biology, 11(6), 876.
https://doi.org/10.3390/biology11060876