COMMENTARY COMMENTARY Root surface as a frontier for plant microbiome research Marcel G. A. van der Heijdena,b,c and Klaus Schlaeppia,1 aPlant-Soil Interactions, Institute for Sustainability Sciences, Agroscope, 8046 Zürich, Switzerland; bPlant-Microbe Interactions, Institute of Environmental Biology, Faculty of Science, Utrecht University, 3584 CH Utrecht, The Netherlands; and cInstitute of Evolutionary Biology and Environmental Studies, University of Zurich, 8057 Zürich, Switzerland Plants associate—analogous to animals or us root microbiota acquisition based on a high humans—with a multitude of microorgan- spatial resolution of root habitats in time isms, which collectively function as a micro- series experiments. The authors trans- biome. A major discovery of the last decade planted sterile germinated seedlings into soil is that numerous organisms of a microbiome and sampled the root-associated habitats Fig. 1. Acquisition of the plant root endosphere micro- (aka microbiota) are not unpretentious back- from time points between 1 and 13 d after biota from soil. Gradual shifts in microbiota composition ground actors. Instead, some microbiota transplantation. The microbiota comparison occur in the root-associated habitats including a zone of members influence host processes including in space and time revealed that the habitat- soil surrounding the roots (rhizosphere, gray shading) behavior, appetite, and health in animals (1) to which root exudates are secreted, the root surface specific community structures were largely (rhizoplane), and the inner host tissue (root endosphere). and contribute to nutrition and health of established after 1 d. Although the compo- Bars illustrate compositional changes in each microbial plants (2–4). Recently, the compositions of sition of the root endosphere was organized habitat due to enrichment (black arrows) and exclusion the plant root-associated microbiota from within 1 d, the steady-state size of the bac- (black T-symbol) processes. Bars are scaled using the numerous plant species, including major number of DNA sequences that change in abundance terial population was reached in 13 d. This (enrichment/exclusion) in the rhizosphere (152/17), the rhi- crops, were revealed using high-throughput work permitted refinement of a two-step zoplane (422/730), and the root endosphere (394/1,961) DNA sequencing. Factors such as soil type model of root microbiota assembly (2) to compared with soil (see ref. 5). or host genotype influence the root-associ- a model with at least three selective steps, ated microbiota. However, the processes that with the rhizoplane as a key component that it appears, paradoxically, that plants permit determine the acquisition of the root micro- serves a critical gating role for controlling endosphere colonization, whereas host cells biota, its resistance to stress, and its ecological microbial entry into the host tissue (Fig. 1). function remain poorly understood. Edwards initiate defense responses on the detection et al. (5) present the third publication in a re- Model of molecular epitopes, which are conserved cent series of PNAS articles about the bacte- The root endosphere microbiota results from throughout the bacterial kingdom (8). Hence, rial microbiota associated with plant roots of gradual community shifts including enrich- we speculate that the host immune system maize (6), related Brassicaceae (7), and now ment and, mainly, depletion processes from influences microbiota selection in general Oryza sativa (rice). It comprises a compre- the surrounding soil microbiota presenting and that it has a strong impact at the second hensive characterization of three microbial the start inoculum (Fig. 1). The enrichment step of exclusion from the rhizoplane to the habitats that are in the proximity of, on, processbeginstoactatadistanceinthe root endosphere microbiota (Fig. 1). and inside plant roots, which are named rhizosphere, continues at the rhizoplane, and Host genotype-dependent variation in rhizosphere, rhizoplane, and root endo- is likely to be largely driven by root exuda- microbiota composition may occur where sphere (Fig. 1). tion. Unlike enrichment, the exclusion pro- host physiological processes (e.g., root exu- A major advance of Edwards et al. is the cess appears to operate more intimately: dates or immune system) are involved. The description of the acquisition process of the first on the rhizoplane and then more pro- different rice cultivars varied noticeably in root endosphere microbiota (5). In contrast nounced in the root endosphere. One ex- their rhizosphere communities, whereas the to the gut microbiota, which is partly in- planation for the first step of exclusion is rhizoplane or root endosphere microbiota herited from the mother, the root endosphere that the rhizoplane selects for bacteria which was little affected by the host genotype (5). microbiota is largely reestablished every time are able to form biofilms and successfully Also, maize inbred lines exhibited quantita- a plant germinates. Until now, the acquisition compete in the presence of elevated nutrient tive differences in rhizosphere microbiota of the endosphere microbiota was proposed levels. Presumably, the second step of ex- composition (6). This contrasts observations to occur in two steps: root exudates, present- clusion results from the selection of the in Arabidopsis where endosphere and not ing a complex mixtures of organic compounds rhizoplane bacteria which possess traits en- rhizosphere communities were affected by that are secreted by plant roots, trigger a abling the colonization of the root endo- first general enrichment in the rhizosphere, sphere. Such microbial traits may allow the Author contributions: M.G.A.v.d.H. and K.S. wrote the paper. followed by a host genotype-dependent dif- bacteria e.g., to evade recognition or to The authors declare no conflict of interest. “ ferentiation of the microbiota thriving on manipulate host defense reactions. We as- See companion article on page E911. ” the rhizoplane and within plant roots (2). sume the involvement of microbial traits 1To whom correspondence should be addressed. Email: klaus. Edwards et al. (5) reveal the early steps of that subvert host immune processes because [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1500709112 PNAS | February 24, 2015 | vol. 112 | no. 8 | 2299–2300 Downloaded by guest on September 25, 2021 the host genotype (9, 10). It appears that host microbial communities in soil, including Tools genetic differences in microbiota composition major members of the plant root microbiota, One approach for new insights in the plant can occur in all root-associated habitats, but has a positive impact on a range of plant microbiome relies on the systematic isolation that the habitat where the host genotype- species and on the functionality of an eco- of root microbiota members (16). Reference dependent variation emerges depends on the system, exemplifies the benefits from com- stocks of pure isolates together with the in- plant species. Note that the host genotype- plex diverse microbial communities (13). formation on community composition allow dependent effects discussed here affect com- The advances in basic microbiome science the reconstruction of at least the cultivable munity composition at best at the level of in the human and animal fields have triggered fraction of the root microbiota. Inoculation microbial species because the 16S profiling experiments should make it possible to ex- technique(usedinrefs.5,6,9,and10)does Edwards et al. reveal amine the interaction of such synthetic com- not resolve subspecies variation between the early steps of root munities with the host plant to unravel the microbiota members, and this is the level of functions of whole communities and their variation that determines the outcomes microbiota acquisition individual members. Here, genome and tran- of most plant–microbe interactions (8). based on a high spatial script sequencing is expected to reveal the microbial traits which are expressed and rel- Frontiers resolution of root hab- evant in the interaction with the plant. Com- Numerous key questions emerge for further itats in time series plementary to such cultivation approaches, the plant microbiome research including the direct sequencing of complex mixtures of following. What is the ecological function of experiments. DNA from various organisms of a habitat the plant microbiome? What are the roles of efforts for using the microbiome to improve (metagenomics) reveals the metabolic capacity core microbiota members that are shared human health (1). Likewise, can we exploit of a microbiome. In rice, numerous microbial between many plant species? How do plants the microbiome to enhance plant produc- traits such as nitrogen fixation, the flagellum, interact with the microbiota and what is the tivity in agricultural settings (14)? The con- protein secretion systems, or quorum sensing, molecular cross-talk between host and asso- trol of pathogen burden or the increase of and their habitat specificity were predicted ciated microbes? Can we localize the micro- using metagenomics (17, 18). biota in the endosphere by, for example, nutrient use efficiency would permit the using in situ hybridization methods? Finally, reduction of agrochemical inputs, thereby Conclusion can we capitalize on the plant microbiome to promoting a more sustainable agriculture. The study by Edwards et al. (5) unifies in- enhance yield and sustainability in agricul- We may be