Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly

Abstract

Like all higher organisms, plants have evolved in the context of a microbial world, shaping both their evolution and their contemporary ecology. Interactions between plant roots and soil microorganisms are critical for plant fitness in natural environments. Given this co-evolution and the pivotal importance of plant-microbial interactions, it has been hypothesized, and a growing body of literature suggests, that plants may regulate the composition of their rhizosphere to promote the growth of microorganisms that improve plant fitness in a given ecosystem. Here, using a combination of comparative genomics and exometabolomics, we show that pre-programmed developmental processes in plants (Avena barbata) result in consistent patterns in the chemical composition of root exudates. This chemical succession in the rhizosphere interacts with microbial metabolite substrate preferences that are predictable from genome sequences. Specifically, we observed a preference by rhizosphere bacteria for consumption of aromatic organic acids exuded by plants (nicotinic, shikimic, salicylic, cinnamic and indole-3-acetic). The combination of these plant exudation traits and microbial substrate uptake traits interact to yield the patterns of microbial community assembly observed in the rhizosphere of an annual grass. This discovery provides a mechanistic underpinning for the process of rhizosphere microbial community assembly and provides an attractive direction for the manipulation of the rhizosphere microbiome for beneficial outcomes.

Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize

“…Contrasting root phenotypes may have differences in root exudate localization and oxygen availability, two factors that have important effects on the composition and function of root‐associated microorganisms (Hinsinger, Bengough, Vetterlein, & Young, ; Neumann & Römheld, ). The distribution and localization of root exudates and the effect of root architecture and anatomy on carbon rhizodeposition and rhizosphere oxygen content remain unclear (Walker, Bais, Grotewold, & Vivanco, ; Zhalnina et al, ), although recent research indicates that in addition to root tips, root zones coated with root hairs are zones of active carbon rhizodeposition (Holz, Zarebanadkouki, Kuzyakov, Pausch, & Carminati, ). Contrasting root phenotypes are expected to offer contrasting environments for soil microbes recruited to the rhizosphere, rhizoplane, and cortex.…”

Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

“…In addition, sampling of B. distachyon root exudates at different developmental stages showed a gradual shift of exudate profiles over time (Fig. S1d), consistent with reports for plants in other growth systems (Chaparro et al ., ; Zhalnina et al ., ).…”

“…Similarly, the B. distachyon exudation profile varied with developmental stage, as reported for other plants (Fig. S1; Chaparro et al ., ; Zhalnina et al ., ).…”

“…The metabolites detected in B. distachyon root exudates in this study (Table S3) were comparable to metabolites detected in exudates of other grasses, such as wheat (Iannucci et al ., ), maize ( Zea mays ; Carvalhais et al ., ), rice (Bacilio‐Jiménez et al ., ), Avena barbata (Zhalnina et al ., ), and dicots such as Arabidopsis (Chaparro et al ., ). Similarly, the B. distachyon exudation profile varied with developmental stage, as reported for other plants (Fig.…”

A suite of complementary biocontrol traits allows a native consortium of root‐associated bacteria to protect their host plant from a fungal sudden‐wilt disease

“…Root colonization is the first and fundamental step required of biocontrol agents to exert their activity against phytopathogens (Pal & Gardener, ). Plant roots secrete organic compounds, such as amino acids, fatty acids, phenolics, sugars and vitamins, which serve as chemoattractants that guide the microbial colonization of these nutrient‐rich niches (Zhalnina et al, ). Bacterial biocontrols protect plants from phytopathogens by competing for these nutrients and niches, which in turn limit pathogen growth (Duffy, ).…”