Emerging sensing, imaging, and computational technologies to scale nano-to macroscale rhizosphere dynamics - Review and research perspectives.

The soil region influenced by plant roots, i.e., the rhizosphere, is one of the most complex biological habitats on Earth and significantly impacts global carbon flow and transformation. Understanding the structure and function of the rhizosphere is critically important for maintaining sustainable plant ecosystem services, designing engineered ecosystems for long-term soil carbon storage, and mitigating the effects of climate change. However, studying the biological and ecological processes and interactions in the rhizosphere requires advanced integrated technologies capable of decoding such a complex system at different scales. Here, we review how emerging approaches in sensing, imaging, and computational modeling can advance our understanding of the complex rhizosphere system. Particularly, we provide our perspectives and discuss future directions in developing rhizosphere sensing technologies that could potentially correlate local-scale interactions to ecosystem scale impacts. We first review integrated multimodal imaging techniques for tracking inorganic elements and organic carbon flow at nano- to microscale in the rhizosphere, followed by a discussion on the use of synthetic soil and plant habitats that bridge laboratory-to-field studies on the rhizosphere processes. We then describe applications of genetically encoded biosensors in monitoring nutrient and chemical exchanges in the rhizosphere, and the novel nanotechnology-mediated delivery approaches for introducing biosensors into the root tissues. Next, we review the recent progress and express our vision on field-deployable sensing technologies such as planar optodes for quantifying the distribution of chemical and analyte gradients in the rhizosphere under field conditions. Moreover, we provide perspectives on the challenges of linking complex rhizosphere interactions to ecosystem sensing for detecting biological traits across scales, which arguably requires using the best-available model predictions including the model-experiment and image-based modeling approaches. Experimental platforms relevant to field conditions like SMART (Sensors at Mesoscales with Advanced Remote Telemetry) soils testbed, coupled with ecosystem sensing and predictive models, can be effective tools to explore coupled ecosystem behavior and responses to environmental perturbations. Finally, we envision that with the advent of novel high-resolution imaging capabilities at nano- to macroscale, and remote biosensing technologies, combined with advanced computational models, future studies will lead to detection and upscaling of rhizosphere processes toward ecosystem and global predictions.