Root surface as a frontier for plant microbiome research.

Plants associate—analogous to animals or us humans—with a multitude of microorganisms, which collectively function as a microbiome. A major discovery of the last decade is that numerous organisms of a microbiome (aka microbiota) are not unpretentious background actors. Instead, some microbiota members influence host processes including behavior, appetite, and health in animals (1) and contribute to nutrition and health of plants (2–4). Recently, the compositions of the plant root-associated microbiota from numerous plant species, including major crops, were revealed using high-throughput DNA sequencing. Factors such as soil type or host genotype influence the root-associated microbiota. However, the processes that determine the acquisition of the root microbiota, its resistance to stress, and its ecological function remain poorly understood. Edwards et al. (5) present the third publication in a recent series of PNAS articles about the bacterial microbiota associated with plant roots of maize (6), related Brassicaceae (7), and now Oryza sativa (rice). It comprises a comprehensive characterization of three microbial habitats that are in the proximity of, on, and inside plant roots, which are named rhizosphere, rhizoplane, and root endosphere (Fig. 1). A major advance of Edwards et al. is the description of the acquisition process of the root endosphere microbiota (5). In contrast to the gut microbiota, which is partly inherited from the mother, the root endosphere microbiota is largely reestablished every time a plant germinates. Until now, the acquisition of the endosphere microbiota was proposed to occur in two steps: root exudates, presenting a complex mixtures of organic compounds that are secreted by plant roots, trigger a first general enrichment in the rhizosphere, followed by a host genotype-dependent differentiation of the microbiota “thriving on the rhizoplane and within plant roots” (2). Edwards et al. (5) reveal the early steps of root microbiota acquisition based on a high spatial resolution of root habitats in time series experiments. The authors transplanted sterile germinated seedlings into soil and sampled the root-associated habitats from time points between 1 and 13 d after transplantation. The microbiota comparison in space and time revealed that the habitatspecific community structures were largely established after 1 d. Although the composition of the root endosphere was organized within 1 d, the steady-state size of the bacterial population was reached in 13 d. This work permitted refinement of a two-step model of root microbiota assembly (2) to a model with at least three selective steps, with the rhizoplane as a key component that serves a critical gating role for controlling microbial entry into the host tissue (Fig. 1).