Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli

Abstract

Root exudation is an important process determining plant interactions with the soil environment. Many studies have linked this process to soil nutrient mobilization. Yet, it remains unresolved how exudation is controlled and how exactly and under what circumstances plants benefit from exudation. The majority of root exudates including primary metabolites (sugars, amino acids, and organic acids) are believed to be passively lost from the root and used by rhizosphere-dwelling microbes. In this review, we synthetize recent advances in ecology and plant biology to explain and propose mechanisms by which root exudation of primary metabolites is controlled, and what role their exudation plays in plant nutrient acquisition strategies. Specifically, we propose a novel conceptual framework for root exudates. This framework is built upon two main concepts: (1) root exudation of primary metabolites is driven by diffusion, with plants and microbes both modulating concentration gradients and therefore diffusion rates to soil depending on their nutritional status; (2) exuded metabolite concentrations can be sensed at the root tip and signals are translated to modify root architecture. The flux of primary metabolites through root exudation is mostly located at the root tip, where the lack of cell differentiation favors diffusion of metabolites to the soil. We show examples of how the root tip senses concentration changes of exuded metabolites and translates that into signals to modify root growth. Plants can modify the concentration of metabolites either by controlling source/sink processes or by expressing and regulating efflux carriers, therefore challenging the idea of root exudation as a purely unregulated passive process. Through root exudate flux, plants can locally enhance concentrations of many common metabolites, which can serve as sensors and integrators of the plant nutritional status and of the nutrient availability in the surrounding environment. Plant-associated micro-organisms also constitute a strong sink for plant carbon, thereby increasing concentration gradients of metabolites and affecting root exudation. Understanding the mechanisms of and the effects that environmental stimuli have on the magnitude and type of root exudation will ultimately improve our knowledge of processes determining soil CO₂ emissions, ecosystem functioning, and how to improve the sustainability of agricultural production.

Keywords: mycorrhiza; nutrient sensing; priming effect; root architecture; root exudates; soil micro-organisms.

Figure 1

Root structure and areas of root exudation. The upper figure represents the longitudinal section of a root. Tissues are indicated in different colors for the different zones of the root (listed at the bottom). The two circles focus on two distinct zones, a differentiated vs. an undifferentiated area, to show the presence of a Casparian strip and low abundance of plasmodesmata in the differentiated area (left circle), and the presence of funnel plasmodesmata in the undifferentiated area (right circle). The square represents a cross section close to the meristematic area where root exudation is the highest. The lower figures represent a schematic representation of solute movement sites from phloem unloading to the soil environment, either in the differentiation zone (A) or in the undifferentiated root tip (B). (A) Solutes move both through the symplastic and apoplastic pathways, but then they are re-uptaken into the cytoplasm as the Casparian strip limits the apoplastic pathway. Only the cortex and epidermis are responsible for the flux of metabolites into the apoplast and consecutively into the soil (root exudation). Cortex and epidermis represents the major control point for root exudation. (B) At the phloem unloading site, both symplastic and apoplastic pathways are used. Because of the lack of a Casparian strip solutes can move out of the root (root exudation) through both the apoplastic and the symplastic pathway.

Figure 2

Summary of the main exudation mechanisms through the plasmamembrane at the root tip. The top panel represents active transport mechanisms, either primary active (direct consumption of ATP) or secondary active (e.g. coupled to H⁺ pumps that actively consume ATP). The bottom panel represents passive transport mechanisms, which allow diffusion following electrochemical gradients. Red arrows represent movement of solutes against their electrochemical gradient, while green arrows represent movement following their electrochemical gradient. On the right side of the figure, examples of membrane transporters allowing movement of primary metabolites are provided.

Figure 3

Involvement of common metabolites in nutrient sensing at the root tip. Schematic representation of how common primary metabolites allows nutrient sensing at the root tip for nitrogen (left panel) and phosphorus (right panel). Amino acid concentration can be sensed by specific receptors (GLR) and can interfere with N transporter expression (NRT). Amino acid concentration inside the root tip depends on the delivery from the phloem and on root exudation, the latter of which depends on concentration gradients mediated by soil micro-organisms. Organic acids can deliver Fe to the root tip, which activates the RAM exhaustion and temporarily increases sugar concentrations. Sugars can be sensed at the root tip and activate changes in root architecture. AA: amino acids; OA: organic acids; Pi: inorganic phosphorus; RAM: root apical meristem; NRT: nitrate transporters; GLR: glutamate-like receptors.

Figure 4

Root exudates link soil nutrients to plant nutrient strategy. Figure illustrates a summary of the concepts proposed for the role of root exudates in plant-microbe interactions and consequences for ecosystems. Plant nutrient strategy determines different exudation patterns, while the soil physical and nutrient composition determines the microbial community and its nutrient demand. Root exudation is a flux with a bi-directional influence between plant and soil microbes. Indeed, while plants can regulate root exudation, soil micro-organism can enhance exudation rates and release molecules that affect root exudation patterns. Ultimately, root exudation has a significant effect on SOM decomposition and greenhouse gases (GHGs) release from soil. Also, plant-soil feedbacks can significantly affect plant performance and plant community composition.