Microbial drivers of root plasticity

Abstract

Soils are highly heterogeneous and dynamic systems, experiencing a constant flow of plant root exudates and moisture fluctuations that affect nutrient distribution, soil physicochemical properties, and microbial metabolisms. Plant roots adjust their development within the soil matrix (growth, branching, root angle, and anatomical features) by integrating local environmental conditions with physiologically informed signals. These physiological responses and the adaptability of roots are commonly defined as plasticity. Although genetically determined, root plasticity is modulated by local fluctuations in water and nutrient availability, environmental changes, and soil properties as well as by the root-associated microbiota. Roots and their vicinity are colonized by taxonomically and functionally diverse microbial species. Specific members within these communities can establish chemical communication with plants via root-derived signals, thereby tapping into the plant's hormonal and developmental network, influencing root plasticity. Given that most root traits associated with plasticity have been discovered under axenic conditions, our knowledge of the multiple potential mechanisms by which members of the root-associated microbiota modulate root plastic responses is still limited. In this review, we explore the recent progress in this field and identify specific avenues for future research toward advancing molecular and ecological understanding of microbial-mediated root plasticity in terrestrial systems.

Keywords: microbiota controlling root development; plant nutrition; plant–microbiota interactions; root plasticity in soil; soil heterogenicity.

Fig. 1

Schematic representation of plant–microbe interactions and microbial metabolism that influence root development and nutrient uptake. The figure displays the main identified mechanisms by which microbes interfere with the plant's endogenous developmental and nutrient uptake programs, resulting in changes in root development and plasticity, and plant nutritional status. MAMPs, microbe‐associated molecular patterns; NOD, Nod factors; PSB, phosphate‐solubilizing bacteria.

Fig. 2

Overview of plant‐root phenotypic (architecture and anatomical) plasticity in soil. (a) Schematic representations of root plasticity in response to intermittent contact with water, leading to xerobranching (upper panel) and soil compaction (lower panel). (b) Confocal microscopy images displaying root cross‐sections highlighting differences in the anatomical arrangement between monocotyledonous and dicotyledonous species. The upper images (left to right) illustrate root anatomical cross‐sections of Zea mays (maize) and Oryza sativa (rice) (monocotyledonous species), and the lower images (left to right) display root anatomical cross‐sections of Solanum lycopersicum (tomato) and Vitis vinifera (grapevine) (dicotyledonous species). In both cases, the blunt‐ended arrows identify and name the different tissue layers and relevant anatomical features in the root. Side images in each inset panel are X‐ray computed tomography (CT) scan images of Z. mays (maize) (monocotyledonous, upper image) and V. vinifera (grapevine) (dicotyledonous, lower image). X‐ray CT enables the visualization of 3D structures based on differences in X‐ray attenuation (see Mairhofer et al., ; Piovesan et al., 2021).