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 CO 2 emissions, ecosystem functioning, and how to improve the sustainability of agricultural production.

Root exudation of mature beech forests across a nutrient availability gradient: the role of root morphology and fungal activity

“…New Phytologist the associated priming effect respond to N deficiency (Dijkstra et al, 2013;Canarini et al, 2019). A low SON concentration increases the diffusion-driven (passive) exudation by a steeper concentration gradient between root cells and soil environment, which leads to increased exudation per unit root biomass at low N supply (Paterson & Sim, 2000).…”

Changes in root‐exudate‐induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling

“…Second, drought has been shown to increase the concentration of secondary metabolites in root exudates (Gargallo-Garriga et al, 2018), which might stimulate specific microbial functional groups and reduce others, which could potentially result in increased N availability for plant uptake (Liu et al, 2015;Czaban et al, 2018). Third, plants might increase the exudation of organic acids to mobilize inorganic P and thus increase plant P uptake during regrowth (Canarini et al, 2019); several studies show that organic acids have the potential to prime the decomposition of soil organic C (Falchini et al, 2003;Brant et al, 2006). Strikingly, the total respiration derived from root exudates was similar under control and drought conditions, suggesting that the effect on respiration of the change in root exudate quality compensated for the reduction in root exudate quantity.…”

Rhizosphere modelling reveals spatiotemporal distribution of daidzein shaping soybean rhizosphere bacterial community

“…Metabolites secreted into the rhizosphere are degraded by microbes and adsorbed onto soil organic matter and clay minerals, depending on the soil type and microbes present (Canarini, Kaiser, Merchant, Richter, & Wanek, 2019;Soma & Soma, 1989;Sugiyama, 2019). In order to gain insight into daidzein distribution in soybean fields, we used grey lowland soils obtained from a soybean farm where soybeans had been cultivated for more than 5 years.…”