Diel Fluctuation of Extracellular Reactive Oxygen Species Production in the Rhizosphere of Rice

Abstract

Reactive oxygen species (ROS) are ubiquitous on earth and drive numerous redox-centered biogeochemical processes. The rhizosphere of wetland plants is a highly dynamic interface for the exchange of oxygen and electrons, presenting the basis of the precedent for ROS production, yet whether extracellular ROS are produced in the rhizosphere remains unknown. Here, we designed a microfluidic chip setup to detect in-situ ROS productions in the rhizosphere of rice with spatial and temporal resolutions. Fluorescence imaging clearly displayed the hot spots of ROS generation in the rhizosphere. The formation concentration of the hydroxyl radical (•OH, a representative ROS, 10–6 M) was comparable to those by the classical photochemical route (10–6–10–7 M) in aquatic systems, therefore highlighting the rhizosphere as an unrecognized hotspot for ROS production. Moreover, the rhizosphere ROS production exhibits diel fluctuation, which simultaneously fluctuated with dissolved oxygen, redox potential, and pH, all driven by radial oxygen loss near the root in the daytime. The production and diel fluctuation of ROS were confirmed in the rhizosphere of rice root incubated in natural soils. We demonstrated that the extracellular ROS production was triggered by the interplay between root-released oxygen and microbial respiration released extracellular electrons, while iron mineral and organic matter might play key roles in storing and shuttling electrons. Our results highlight the rhizosphere as a widespread but previously unappreciated hotspot for ROS production, which may affect pollutant redox dynamics and biogeochemical processes in soils.

Microscale Spatiotemporal Variation and Generation Mechanisms of Reactive Oxygen Species in the Rhizosphere of Ryegrass: Coupled Biotic–Abiotic Processes

“…The concentrations of ROS changed regularly with the whole life cycle of ryegrass, which may play an important role in mediating physiological processes in plants. 16,63 from previous studies of plant physiology and agronomy such as root exudates, enzymes activities, and microbial activity, which may have important implications for rhizosphere remediation of organic pollutants and revealing the degradation mechanism. 64 Considering the higher redox activity of ROS, rhizosphere ROS may trigger the oxidation or mineralization of organic matter and reductively dissolve iron minerals, which can promote the release of CO 2 to the atmosphere and facilitate the intake of iron.…”

“…Rhizosphere, a thin layer of soil at the plant root–soil interface, is a hotspot of intense biogeochemical processes. , As a highly active region of the soil profile, the rhizosphere is characterized by higher redox potential (Eh), oxygen content, root exudates amount, enzymes activities, and microbial abundance in comparison with bulk soil, − which may have a strong influence on the production of active species, mostly like ROS. For example, the accumulation of ROS in the rice rhizosphere in the nutrient solution and soil pore water was found, which derived from the reaction between root-released dioxygen and extracellular electrons released by microbial respiration . Despite this advance, the production of ROS in the rhizosphere surrounded by a real soil environment is far less explored.…”

“…For example, the accumulation of ROS in the rice rhizosphere in the nutrient solution and soil pore water was found, which derived from the reaction between rootreleased dioxygen and extracellular electrons released by microbial respiration. 16 Despite this advance, the production of ROS in the rhizosphere surrounded by a real soil environment is far less explored. In comparison with solo nutrient solution and soil pore water, the compositions of the real soil environment are much more complex with the coexistence of organic matter, multiple mineral mixtures, and microbes, 17,18 which may influence the redox processes via abiotic and biotic pathways and thus unavoidably alter the generation, accumulation, and fate of ROS in the rhizosphere.…”

The Root Tip of Submerged Plants: An Efficient Engine for Carbon Mineralization

“…4−6 Additionally, Fe(II) can react with H 2 O 2 to generate the reactive oxygen species that can enhance the oxidation of OC. 7,8 The rhizosphere of plants under short-term or longterm flooding is a typical environment in which these dual roles of Fe oxides may coexist. 9−11 Plants growing under flooding conditions can deliver O 2 from the shoot to the root and soil/sediment, thereby promoting the formation of Fe oxides and Fe−OC complexes in the rhizosphere.…”

“…Iron (Fe) oxides serve as an rusty sink that can protect organic carbon (OC) from decomposition through the formation of Fe–OC complexes. − However, Fe oxides can serve as terminal electron acceptors in microbially mediated dissimilatory Fe­(III) reduction in anaerobic or alternating redox environments, leading to the release of Fe-bound OC. − Additionally, Fe­(II) can react with H 2 O 2 to generate the reactive oxygen species that can enhance the oxidation of OC. , The rhizosphere of plants under short-term or long-term flooding is a typical environment in which these dual roles of Fe oxides may coexist. − Plants growing under flooding conditions can deliver O 2 from the shoot to the root and soil/sediment, thereby promoting the formation of Fe oxides and Fe–OC complexes in the rhizosphere. , The Fe oxides commonly precipitate on the root surface, which are termed Fe plaques. , In addition, the input of labile root exudates and other less decomposable rhizodeposits creates microbial hot spots in the rhizosphere. − As a result of accumulation of Fe oxide in the rhizosphere, the abundance of the microbial community and the dissimilatory Fe­(III) reduction rates in the rhizosphere are relatively greater than in the bulk soil/sediment. − Overall, the carbon pool of the rhizosphere is strongly affected by Fe oxidation–carbon sequestration and Fe reduction–carbon mineralization, and the influencing factors include radial oxygen loss (ROL), root exudates, the microbial community, manganese, etc. , …”