Artigo Atividade Bactéria

REVIEWS
Plant–microbiome interactions: from

community assembly to plant health
Pankaj Trivedi 1 ✉, Jan E. Leach1, Susannah G. Tringe 2
, Tongmin Sa 3
and
Brajesh K. Singh 4,5
Abstract | Healthy plants host diverse but taxonomically structured communities of microorganisms,
the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes
confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress
tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research
has unravelled the complex network of genetic, biochemical, physical and metabolic interactions
among the plant, the associated microbial communities and the environment. We also discuss
how those interactions shape the assembly of plant-associated microbiomes and modulate their
beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge
gaps and future directions.
Holobiont
Plants provide a multitude of niches for the growth and with the associated microbiomes23–26, thus increasing
A plant and the members proliferation of a diversity of microorganisms, includ- our understanding of how microorganisms adapt to
of its associated microbiota ing bacteria, fungi, protists, nematodes and viruses (the the plant environment. Numerous genes involved in
considered as a single entity; plant microbiota). These microorganisms can form plant adaptation have been identified that are consist-
this represents the ‘unit of
complex co-associations with plants and have important ent across phylogenetically diverse bacterial taxa, and a
selection’ at which plant–
microbiome interactions have roles in promoting the productivity and health of the few genes related to plant colonization are even shared
probably co-evolved in order plant in natural environments. It has been proposed1 that with plant-associated eukaryotes23. The products of
to maintain host functionality plants and the associated microbiota form a ‘holobiont’, these shared genes mimic plant proteins and function
and fitness over ecological and
whereby evolutionary selection between plants and as decoys to allow the microbiota to outcompete plant
even evolutionary timescales.
microorganisms contributes to the overall stability of defences for efficient colonization. However, the molec-
the system, but this concept has yet to be conclusively ular mechanisms that govern plant–microorganism
1
Microbiome Network and demonstrated. Complex plant microbial communities interactions at a community level are still not well
Department of Agricultural contain taxa from diverse phyla and have deep branch- understood.
Biology, Colorado State
University, Fort Collins,
ing lineages at lower phylogenetic resolution. In recent The members of a plant microbiota comprise benefi-
CO, USA. years, culture-independent high-throughput sequencing cial, neutral and pathogenic microorganisms. Microbial
2
Department of Energy Joint
has greatly expanded the repertoire of microorganisms communities associated with their hosts have been
Genome Institute, Berkeley, known to reside in and on plants as well as in the sur- shown to promote plant growth, nutrient uptake and
CA, USA. rounding environment2–19. Many studies have noted the pathogen resistance27–31. Although individual members
3
Department of Environmental presence of a subset of microbial lineages, designated of plant-associated microbial communities can possess
and Biological Chemistry, the ‘core microbiota’, that reproducibly associates with a certain beneficial traits30,31, the manifestation of a trait in
Chungbuk National
given host across a wide range of environments7,12,13,18,20. the community is an emergent property that cannot be
University, Cheongju,
Republic of Korea.
Among the plant-associated microbiota, bacteria and to predicted from the individual members. For example,
4
Hawkesbury Institute for the
lesser extent fungi are the most dominant forms and are Pseudomonas spp. can suppress plant pathogens through
Environment, Western Sydney relatively well-studied compared with other members antibiosis and competition, yet overall soil disease sup-
University, Penrith South, of the community, but other groups — such as archaea, pressiveness is an emergent property that depends on
NSW, Australia. algae, nematodes and protists — also have important multiple factors, including the population dynamics of
5
Global Centre for Land roles in plant functioning and health21,22. Genome- the pathogen, the genetic backgrounds of both the path-
Based Innovation, Western wide association studies (GWASs) and metagenome-wide ogen and host, biotic and abiotic conditions, and the
Sydney University, Penrith
South, NSW, Australia.
association studies have linked individual microbial composition and diversity of the plant microbiota32–34.
✉e-mail: Pankaj.trivedi@ taxa and genes to plant colonization, physiology and The benefits conferred by the microorganisms to their
colostate.edu fitness16–18 (Box 1, Supplementary text S1). Genomics host plants can be direct, including transformation and
https://doi.org/10.1038/ and multi-‘omics’ have enabled the identification and translocation of essential nutrients in the soil to make
s41579-020-0412-1 characterization of genes that govern plant interactions them available to plants (for example, nitrogen fixation),
NATure RevIeWS | MicroBioloGy volume 18 | November 2020 | 607

Reviews
Box 1 | Host and environmental factors (Box 1, Supplementary text S1). Their assembly is gov-
erned by complex interactions among microorgan-
Ecological theories suggest that the plant-associated microbiome is shaped by complex isms, their plant host and the environment, although
interactions among the host, microorganisms and the environment. Genome-wide the underlying mechanisms are not fully understood.
association studies have shown that the host genome does influence microbiome New insights into these complex interactions will help
composition, and many heritable taxa belong to the core microbiome, which
advance our understanding of the evolutionary and eco-
suggests positive feedback from the plant microbiome over evolutionary timescales.
Several quantitative trait loci associated with biotic and abiotic stress adaptation or logical processes that govern community assembly and
morphological and physiological traits have been identified that underlie variation will guide translational research to improve plant fitness
in the microbiome traits, species richness and community structure in roots and and productivity (Box 2, Box 3, Supplementary text S2).
phyllosphere. Metabolic diversification of root exudates within the plant kingdom To achieve a more comprehensive understanding, it
may provide a basis for communication and recognition that directs the assembly will be important first to characterize the mechanisms
and maintenance of a distinct microbiota tailored to the needs of the host115,127–129. that drive the assembly of plant-associated microbiomes
Comparative genomics and multi-‘omics’-based analysis has demonstrated that (Supplementary text S1). Second, the biochemical
metabolic synchronization between plant exudation traits and the microbial substrate’s and genetic features of metabolic microorganism–
utilization traits results in the predictable temporal patterns of microbial community microorganism and host–microorganism interactions
assembly observed in the rhizospheres of different plant species102,127. Interplay between
that result in beneficial ecological outcomes need to be
the microbiome, defence mechanisms (for example, cell wall and cuticle) and
multilayered surveillance systems (involving pattern recognition receptors (PRRs) identified. Such data will inform the design and con-
and hormones) has a critical role in maintaining microbial homeostasis, by activating struction of functional microbial systems de novo that
either symbiotic responses that promote microbial colonization or immune responses are based on predictive models of plant–microbiome
that limit it. For example, diversification of microorganism-associated molecular patterns interactions. Furthermore, the development of microbial
(MAMPs) and their PRRs in different hosts can have a fundamental role in the evasion inoculants, signalling compounds and other tools will
of MAMP-triggered immunity surveillance, thus enabling the assembly of distinct enhance microbiome function in the agricultural setting.
plant-associated microbial communities in natural plant populations in response to local In this Review, we explore the current knowledge of
environments130,131. Plants also recruit a ‘stress microbiome’ that provides protection the plant microbiome at the community level. In par-
against various abiotic or biotic stresses. Selective enrichment of the stress-tolerant
ticular, by drawing from forward genetic approaches
microbiome is driven by differences in plant metabolism and immune-associated
and comparative genome and computational analyses
traits107,128. This reinforces the functional links between immunity and nutrition and
suggests that plants may repurpose the same stress pathways to effectively respond of large plant genomic and metagenomic datasets, we
to both biotic and abiotic stresses. Changes in the microbial seed banks in bulk soil with discuss the current understanding of the composition,
long-term intensive crop management practices such as heavy fertilization132, tillage133 assembly and dynamics of plant-associated microbial
or organic farming134 affect the assemblages of the plant-associated microbiome. communities and the host functions they provide.
Agriculture intensification decreases network connectivity and the abundance of
keystone taxa, which suggests that intensively farmed systems are less resilient to The plant microbiome
environmental stresses than are those managed by low-intensity practices such as Composition of plant-associated microbiota. The rel-
organic farming134,135. Given the diversity of microorganisms that colonize plants, an ative abundance profiles of the major bacterial groups
emerging focus in the field of plant microbiomes is the role of multikingdom interactions are similar in bulk soil and in the rhizosphere , with
in shaping microbial communities. Although more work is needed to understand how
a slight increment in the bacteria belonging to phy-
bacterial diversity is influenced by microeukaryotes, data suggest that multitrophic
network stability is highly dependent on microbial hubs that transmit effects to the lum Proteobacteria in the rhizosphere8–11,13 (Fig. 1) .
microbial community via microorganism–microorganism interactions13,39,62. Community composition varies significantly between
the rhizosphere, endophytes and the phyllosphere. Plant
endophytic communities are frequently enriched in
mitigation of environmental stresses (such as drought) members of the Proteobacteria and Firmicutes (both
and protection from plant pathogens through com- ∼twofold or higher in relative abundance in the endo-
petition, antibiosis and the production of hydrolytic phytic community than in the rhizosphere) and to a
enzymes27,29–31. By contrast, the benefits can also be lesser extent in Bacteroidetes; they are depleted in mem-
Core microbiota indirect, through enhancement of a plant’s resistance bers of the Acidobacteria, Planctomycetes, Chloroflexi
The group of microorganisms
responses28. Because several plant traits are co-regulated and Verrucomicrobia (>twofold lower in relative
commonly found within
a microbiota; recurrence by the plant-associated microbiome, there is an emerg- abundance in the endophytic community than in the
of an association between ing paradigm in which interactions between plants and rhizosphere)8–11,13 (Fig. 1). Such enrichment of specific
microorganisms is used their associated microbiome should not be considered bacterial taxa is consistent even in soils that are dom-
as the criterion to select as inherently either beneficial or deleterious, but rather as inated by other taxa (for example, in soils dominated
the microorganisms that
potentially provide critical
means to generate new phenotypes with increased fit- by Acidobacteria). The phyllosphere community mainly
functions within the habitat ness under distinct environmental conditions35. The comprises bacteria belonging to phylum Proteobacteria
in which they are found. rational design and application of synthetic communities and to the Bacteroidetes, Firmicutes and Actinomycetes,
(SynComs) of microorganisms with broad, persistent where members of phylum Proteobacteria constitute
Genome-wide association
and durable plant-growth-promoting traits have the ~50% of the community composition (Fig. 1). The vast
studies
(GWASs). A method to survey potential to translate basic scientific findings into appli- diversity of fungi that colonize both aboveground and
entire genomes of the genetic cations in either greenhouse or field settings (Box 2, belowground plant tissues mainly belong to the phyla
variants of many individuals Supplementary text S2)14,33,36–39. Ascomycota and Basidiomycota 9–11,13,15,16,19 (Fig. 1) .
for genetic polymorphisms, One key finding is that plant-associated microbial Although arbuscular fungi (phylum Glomeromycota)
single-nucleotide
polymorphisms, that
communities do not represent random assemblages, but and ectomycorrhizal fungi are well-studied, these groups
are associated with a instead are structured by general rules for community represent only minor diversity among fungal communi-
particular trait. assembly and show a defined phylogenetic organization40 ties from roots9–11,13. The ‘winnowing’ of many bacterial
608 | November 2020 | volume 18 www.nature.com/nrmicro

Reviews
Multi-‘omics’ and fungal genotypes to only a few successful coloniz- that shapes the composition of plant-associated micro
An approach (also known as ers could be explained in part by plant–microbiome biota (Fig. 1). A rapid loss of diversity from soil to root
integrative omics) to combine co-evolution12; however, niche adaptation may also have and then to shoot and flower indicates the increasing
sets of different omic groups — a major role in the selective filtering and recruitment of influence of host-specific factors at the root–soil and
such as the genome,
proteome, transcriptome
different microorganisms13,14,22,41,42. These successful col- root–shoot interfaces. The components of the rhizo
and metabolome — to study onizers inhabiting the same host niche can either com- sphere at coarse phylogenetic levels (for example, the
biological entities pete for the available resources or form stable co-existing phylum and family levels) for various plant species (for
in a concerted way. communities through mutual cooperation. example, citrus, barley, maize, sugarcane, Arabidopsis
Determinants of the bacterial and fungal commu- thaliana and rice) under field conditions are similar,
Microeukaryotes
Any microscopic eukaryotes,
nity composition at the genus and species levels include regardless of their geographical source location2–19. This
mainly protists, fungi, host compartment, environmental factors and host remarkable similarity suggests that the plant traits that
nematodes and small genotype13,43,44 (Box 1, Supplementary text S1). The rela- shape the rhizosphere compartment are themselves
zooplankton. tive importance of genotypes in shaping the microbiota uncorrelated with host phylogeny. By contrast, root
Synthetic communities
composition in the phyllosphere declines over time, endophytes tend to be phylogenetically clustered, which
(SynComs). Communities that which suggests robust habitat selection of these commu- indicates the co-existence of closely related microorgan-
comprise individually isolated nities over relatively short plant-host timescales44. Fungal isms, probably owing to the greater influence of the host
microorganisms for controlled establishment in the rhizosphere and on plant roots plant on the assembly of the endosphere microbiome.
studies of microbial
seems to be more affected by stochastic variations and Consistent with diversity, microbial network complexity
communities.
to respond differently to environmental factors than is decreases from the soil to endosphere compartments39.
true for bacteria9–11,13. There are clear differences among The inoculum source of the aboveground microbiota
the microbial communities in different plant compart- is more variable, owing to their open nature and rap-
ments (the rhizosphere, root endosphere, phyllosphere idly fluctuating environmental conditions. The mode
and the bulk and root-zone soils), which indicates of transmission probably involves transfer by aerosols,
that the plant compartment is a major selective force insects, soil, pollen and/or migration via other plant
tissues3,41,42. Although the assemblies of root-associated
bacteria and fungi differ substantially from the above
Box 2 | Microbiome engineering using synthetic microbial communities
ground communities, both represent a subset of the
Microorganisms have long been applied as inoculants for biocontrol or biostimulation; microbiota derived from soil communities and enriched
however, their field efficacy varies with the climate, soil type and other environmental in different plant-associated niches, which suggests
factors. In many cases, these products are single isolates from a different environment that soil functions as a common reservoir for both
that probably cannot compete with the indigenous microbiome. The highly inconsistent belowground and aboveground plant microbiota9–11,13.
performance of microbial inoculants suggests that the functionality and persistence of
However, there is smaller overlap between the fungal
microorganisms are dependent on interactions with the environment as well as with
other microorganisms within a community. To effectively harness the microbiome
community of aerial plant tissues and soil than is true for
requires new approaches that recognize that microorganisms living in natural and bacteria, which suggests that other sources are important
managed systems typically are members of multispecies communities. Explicit reservoirs for the phyllosphere fungal community13. The
consideration of fundamental ecological processes for the development of complex host’s genetic control of the aboveground microbiota is
microbial communities is in its infancy but is critical to the rational design and greater than for the root or rhizosphere microbiota17;
manipulation of microbiomes in agricultural systems. In recent years, synthetic microbial however, the rapidly fluctuating environmental con-
communities (SynComs) of varied complexity have been constructed using bottom-up ditions aboveground also have an important role, and
combinations and have been applied to plants as a means to study various aspects of only a few microbial groups of the microbiota that have
plant microbiome interactions, including elucidation of the specific mechanisms that adapted to harsh environments will flourish.
drive community assembly and the interactions among different members98. It is clear
In addition to the role of bacterial and fungal com-
that there will not be a ‘one size fits all’ SynComs, and therefore different strategies
are being explored in order to select the members of SynComs for reconstitution
munities, soil and plant processes are directly influ-
experiments98. Selection for core functional versus core taxonomic microbial members enced by other organisms, including viruses, archaea,
in SynComs has been emphasized20. Within this concept, functional keystone species nematodes and protists (Supplementary text S1).
can be predicted through topological networks derived from interactions and through Plant-a ssociated archaeal taxa primarily belong
metabolic models. This approach provides a pathway to maximize SynCom persistence to the phyla Thaumarchaeota, Crenarchaeota and
and trait expression success in natural settings, by identifying possible points of control Euryarchaeota22,43,45,46. Although they are consistent
for manipulating microbial diversity and microorganism–host interactions. It should be members of the plant-associated community, we have
noted that interaction networks and metabolic models are predictions that are often little understanding of the contribution of archaeal
based on correlations and in silico-inferred assumptions. SynComs provide the communities to host performance43,45,46. Recent studies
opportunity to validate these predictions and correlations experimentally and have
have demonstrated that the plant-associated archaeal
emerged as an important tool to demonstrate their applicability in an agricultural
context. Individual microbial members can be cultured using high-throughput platforms
community is highly diverse46,47 and niche specific
and characterized through genomic, metabolic and physiological analysis. Standardized (that is, distinct for different parts of the plant)47, and
fabricated ecosystems or microfluidic platforms can be used for reproducible that distinct archaeal members are plant specific46,47.
interrogation of beneficial traits. SynComs with different complexities can be designed Plant-associated archaeal communities possess the abil-
through predictive modelling that evaluates trait redundancy, dominance, modularity, ity to degrade glycogen, which is commonly stored and
interactions and assembly. Automated monitoring of the plant response and microbial exuded by fungi46,47. This suggests a possible interaction
community structures after the application of SynComs can be achieved by a variety between these different groups in the plant environ-
of sensors (including those in drones) together with mobile DNA sequencers. Further ment. Metagenomic studies have identified functional
integration of microbiome–phenome–environment datasets could forecast microbial genes involved in stress tolerance and nutrient cycling
dynamics and enable SynCom applications to be scaled up in smart farming systems.
in plant-associated archaeal communities46,47.

Reviews
Box 3 | Trait-based framework to understand plant–microbiome interactions different plant species, such as barley, rice, sugarcane,
grapevine, citrus, soybean and A. thaliana, are com-
It is intuitive and generally accepted that the functional traits conferred by microbiomes mon at the genus level (for example, Pseudomonas,
are more informative than taxonomic information, as we are more interested in Agrobacterium, Methylobacterium, Sphingomonas,
‘what they are doing (or can do)’ than in ‘who is there’. However, to date, most plant Erwinia, Cladosporium, Coniothyrium, Resinicium and
microbiome studies in the field have focused on community structure rather than
Fusarium). This suggests that co-occurring members
function. There are strong indications that plants select for traits rather than taxonomy,
as many functions provided by the microbiome are a part of the ‘accessory genome’ of the core microbiota are selectively recruited and
and are discontinuously distributed across taxonomies. Phenotyping the functional enriched in parallel and are well adapted to life on and/or
potential of a microbial community could provide comprehensive information on the inside plant tissues. A core archaeome for plants growing
possible mechanisms driving plant–microbiome interactions and therefore could be a in alpine bog46 and for arugula (Eruca sativa Mill.)47 has
powerful approach to understanding and modelling the microbial-community functions recently been reported. Microbial families belonging to
that support plant growth. The association of genetic variants with specific microbial Rhizobiales and Pseudomonadales are not only part of
genes rather than with phylogenetic identity will provide meaningful insight into the the core microbiota (5–17% mean relative abundance)61
possible mechanisms underlying multifaceted plant–microbiome interactions. Defining but also represent a universal core plant microbiome.
linkages between plant phenotypes and microbiome functions through genome-wide The community composition of these orders remains
association studies could help identify host genes that are responsible for the assembly
similar in different plant-associated niches, indicating
of beneficial microbiomes. In recent years, advances in metagenome-wide association
approaches, network analysis, genome-mining methods to identify biosynthetic a conserved adaptation to the plant environment61.
gene clusters, the reconstruction of transcriptional and regulatory networks, and the Multiple members affiliated with these core bacterial
integration of modelling and prediction approaches have provided strong foundations genera are known to positively influence plant growth
for developing a trait-based framework to understand and engineer plant–microbiome through the production of growth-regulating hor-
interactions. However, whether the functional contributions of the microbiome are the mones, nutrient mobilization and/or protecting plants
same across different plant species, growth stages and disturbances remains to be from biotic or abiotic stresses27–31. The identification of
determined. a co-occurring core of plant-associated microorganisms
also provides a useful starting point for studies of how
to build SynComs to manipulate plant–microbiome
Rhizosphere Viruses play a critical part in bacterial community interactions for increased growth and productivity
The region of soil in the vicinity assembly and turnover in the soil, but their function (Supplementary text S2).
of plant roots that is influenced
in plant-associated environments is not completely Within the core microbiota, a few members, such
by plant-derived nutrients and
oxygen availability; it is not a understood48. A recent report demonstrated that in as ‘hub microorganisms’, can influence the community
region of definable size or soils, viruses affect both the microbiome structure structure through strong biotic interactions with the
shape, but instead consists of a (top-d own control, inferred from lysis-d ominant host or with other microbial species, rather than simply
gradient in chemical, biological microbial members) and function (bottom-up con- by their own high abundance13,18,62,63. These hub species
and physical properties that
change both radially and
trol, inferred from the carriage of auxiliary metabolic may represent keystone species that can exert strong
longitudinally along the root. genes)49. Experimental studies have demonstrated that direct and indirect effects on microbiome assembly
natural phage communities influence the assembly of and that function as mediators between the plant and
Endophytes phyllosphere communities50. Similarly, protists and its associated microbiome. It must be noted that the
The microorganisms residing
nematodes greatly contribute to microbiome diversity, co-occurrence network approaches generally used to
within plant tissues (the
endosphere), such as leaves, and together with other microorganisms, they affect identify hub microorganisms may be insufficient for
roots or stems. soil–plant processes and ecosystem functioning51–53. interpreting species interactions and do not indicate
Protists may control bacterial and fungal community causal relationships64. However, elucidating hub micro-
Phyllosphere assembly by modulating predator–prey relationships at organisms through co-occurrence networks provides
All the aboveground organs
of plants, including the leaf,
different trophic levels54. Within protists, most oomy- an opportunity to test the causal relationships of hub
flower, stem and fruit. cete species that have been described so far are harmful species with other species and to understand how the
plant pathogens (for example, Pythium, Phytophthora, ‘keystone behaviour’ of identified hub species can be
Hub microorganisms Peronospora and Albugo species)55. Although Albugo spp. experimentally validated. Hub microorganisms have
Microbial groups that are
are plant pathogens, members of this obligate biotrophic a regulatory effect on the network of microbial inter-
substantially more connected
within a co-occurrence network genus frequently occur on asymptomatic Brassicaceae actions, as their removal results in the loss of interac-
than other groups on the basis plants, which suggests a role for environmental factors in tions. For example, Albugo laibachii and Dioszegia spp.
of centrality measurements, triggering the development of symptoms56. Also closely have been identified62 as highly interactive hubs in
such as degree, between-ness related, non-p athogenic oomycetes can have posi- the phyllosphere of A. thaliana. Through these hubs,
centrality and closeness
centrality.
tive effects on plant growth57,58. A study in A. thaliana host plants selectively influence the structure of their
observed that the phenotypic effects of oomycetes vary associated microbiota by modulating microorganism–
Keystone species substantially in the presence and absence of bacterial microorganism interactions and changing host fitness.
Highly connected microbial communities39. Variation of two hub microorganisms had a significant
taxa that individually or in a
effect on the assembly of the microbiome, and this influ-
guild show great explanatory
power for network structure Core and hub microbiota. The plant core microbiota ence was independent from external factors such as loca-
and functioning, irrespective consists of members of the microbial community that tion and sampling time62. Host genomic regions involved
of their abundance; not all hub are persistent and are ubiquitous in almost all the in carbohydrate metabolism and stress responses con-
species are keystone species, communities associated with a particular host1,59,60. trol the abundance of hub microorganisms18. It has been
as a high number of direct
correlations (a requirement for
The core microbiota contains key microbial taxa that postulated that hub microorganisms have important
hubs) is not a requirement carry genes with functions that are essential for host roles in organizing the plant-associated microbiome
for keystone species. fitness1,20,59,60. Many members of the core microbiota of as a network, via selective assembly and recruitment,

Reviews
a Bacteria Fungi
Phyllosphere
Proteobacteria
Bacteroidetes Leaf endosphere
Firmicutes
Actinobacteria
Ascomycetes
Cyanobacteria
Basidiomycetes
Planctomycetes
Others
Verrucomicrobia
Gemmatimonadetes
Acidobacteria
Root endosphere
Others
Bulk soil Bulk soil

Rhizosphere
b c
6
(Shannon diversity index (H))
(Shannon diversity index (H))
4.0
Bacterial diversity
5 3.5
Fungal diversity
4 3.0
2.5
3
2.0
2
re
e
re
re
re
re
re
re
il
il
er
so
so
he
e
e
he
he
he
he
ph
ph
ph
sp
lk
lk
sp
p
sp
sp
os
os
os
os
Bu
Bu
llo
do
izo
izo
yll
nd
nd
nd
y
en
Rh
Rh
Ph
Ph
fe
fe
te
ot
a
o
Le
Le
Ro
Ro
Sample Sample
Fig. 1 | General structure of the bacterial and fungal communities from various plant-associated niches.
a | Microbiome composition varies depending on the plant compartment. Pie charts show averages of the relative
abundances of the major bacterial (left) and fungal (right) phyla that are detected in the bulk soil, rhizosphere, root
endosphere, leaf endosphere and phyllosphere of various plant species (sugarcane10,13, grapes8, cactus species
(Myrtillocactus geometrizans and Opuntia robusta)11 and Agave species9 (A. tequilana, A. salmiana and A. deserti)).
Abundances were estimated by marker-gene sequencing (16S rRNA for bacteria, and internal transcribed spacer (ITS)
for fungi). Only phyla that represented >0.5% of the total population in at least one sample are included. The studies
used high-throughput sequencing to profile the bacterial and fungal communities in different niches in a single study.
b,c | Box plots show bacterial (part b) and fungal (part c) diversity (in terms of the Shannon diversity index (H)) in
the bulk soil, rhizosphere, root endosphere, leaf endosphere and phyllosphere of various plant species (data based
on refs8–11,13).

Reviews
Chemotaxis and thus also have an important role in orchestrating from the roots of A. thaliana than in bacteria that had
Movement of organisms host–microbiome interactions. been isolated from soil42. Combined phylogenomic and
in response to a chemical phenotypic analyses suggest that such root coloniza-
stimulus in the direction Dynamics of the plant-associated microbiome. The tion traits pre-date the acquisition of symbiosis genes
of a higher concentration of
beneficial substances or a
assembly of a plant-associated microbiome is a suc- in members that belong to the order Rhizobiales, which
lower concentration of toxins. cessional, multistep process that is determined by dis- are part of the core microbiome61. Polyamines such as
persal, species interactions, the environment and the arginine and putrescine function as signalling mole-
Plant exudates host. Early colonizers could be transmitted vertically, cules in the root–rhizosphere interface and inform the
Complex mixtures of soluble
via the parents, through seed transmission pathways65. microbiome of the presence of eukaryotic hosts. Sensing
organic substances — which
may contain sugars, amino
Therefore, these microorganisms may lack features of such molecules triggers a lifestyle switch in order to
acids, organic acids, enzymes that would otherwise facilitate early colonization — for promote attachment and biofilm formation in many
and other substances — that example, active dispersal — and instead have charac- microbial groups25,73. After successful colonization,
are secreted by living plants, teristics selected by the host plants that depend on dif- diverse host processes, such as the activation of plant
along with microbially modified
products of these substances.
ferences in terms of seed morphology and anatomy. signalling pathways and/or nutrient-stress-mediated
Once seeds germinate, microbiome assembly is likely root inhibition that alters the host root architecture, can
Biofilm to be driven by horizontal transfer, where seed-borne lead to differential niche colonization patterns among
An assemblage of microbial microorganisms preferentially become associated with various microbial groups.
cells that is irreversibly
aboveground plant tissues, whereas soil-derived micro-
associated with a surface and
is enclosed in a matrix of
organisms are mainly associated with the rhizosphere Uptake of plant metabolites. Plant metabolism generates
primarily polysaccharide and roots66. The root-associated microbiome is likely to chemically distinct environments, and many of the core
material. be dynamically recruited and assembled over the life- functional traits that are reported to be over-represented
cycle of its plant host, and the temporal shifts in this in plant-associated microbiomes correlate with the
Carbohydrate-active
enzymes
microbiome are consistent across geographic locations43. requirements for microbial growth and survival in
Enzymes involved in the The microbial composition of microbiomes, which can such plant environments. Comparative genomic analysis23
biosynthesis, modification, be highly dynamic in the early vegetative phase, begins has confirmed the trends of metagenome analysis15
binding and breakdown to converge throughout vegetative growth and stabilizes towards positive selection for genes involved in car-
of carbohydrates.
during the reproductive phase43,67. Repeated sampling bohydrate metabolism and transport and for tran-
to study the structure of plant-associated microbiomes scriptional regulators of these genes in the genomes of
has shown that, although their composition varies with phylogenetically diverse plant-associated bacteria.
time, a small fraction of microbial taxa belonging to the Of note, several carbohydrate-active enzymes are shared
core microbiota are consistently maintained in high rel- between plant-associated bacteria and fungi, despite
ative abundances throughout plant development10,19,43,67. large evolutionary distances74. Genomic analysis has
These microorganisms possess multiple traits, for effi- shown that fast-growing bacteria, such as the alphapro-
cient colonization, stress tolerance and beneficial effects teobacteria and gammaproteobacteria that are typically
on the hosts66,68. Moreover, traits such as drought toler- enriched in plant environments, have a high number of
ance and disease resistance that are conferred by associ- total transporters — including ATP-binding cassettes,
ations with a particular microbial group can be passed phosphotransferase systems and drug/metabolite trans-
from mother plants to their offspring, which indicates porters — that could import or export a broad range
the interlinked importance of host genetics and the of compounds23,75. The presence of low-affinity trans-
host-associated microbiome69,70. porters in plant-associated microorganisms enables fast
growth during periods of feast and endurance of star-
Plant colonization and community assembly vation during periods of famine, fluctuating conditions
Plant sensing and the initiation of colonization. Plant- that are typical in the rhizosphere.
associated microorganisms use chemotaxis to sense and Plant hosts provide stable metabolite availability,
respond to plant-derived signals, such as organic acids and this reduces the selective pressure on the associated
and/or sugars present in plant exudates, and to initiate microbiome to maintain capabilities for the biosynthe-
colonization (Fig. 2). Once a signal is perceived, micro- sis of various essential compounds25,26. A recent study
organisms move towards the plant primarily through the identified mutations in 50 bacterial genes required for
use of flagella. Subsequently, microorganisms attach to amino acid metabolism that confer a fitness advan-
the root surface and form a biofilm. Genes that encode tage to mutants relative to the wild-t ype strain of
proteins involved in bacterial chemotaxis, flagella assem- Pseudomonas simiae WCS417r26. Genes for amino acid
bly, bacterial motility, biofilm formation, bacterial secre- biosynthesis were depleted in the global citrus rhizos-
tion and two-component regulatory systems are highly phere compared with bulk soils15. The findings indi-
abundant in microorganisms and microbial communi- cate that auxotrophy for specific amino acids confers a
ties found in the root environment15,23,38,71,72 as well as in selective fitness advantage when plant-exuded amino
the stem and phyllosphere environments, as compared acids are abundant. Interestingly, thiamine auxotrophy
with the bulk soil3,24,25. A higher number of substrate of the plant-beneficial endophytic fungus Serendipita
transporters in the bacterial phyla Proteobacteria and indica could be satisfied by the ubiquitous soil micro-
Firmicutes facilitate the increased presence of these organism Bacillus subtilis, but the success of this inter-
bacterial groups in nutrient-rich plant environments. action was only visible when inoculation of B. subtilis
Similarly, a substantially higher fraction of motility genes was separated from that of S. indica in either time or
was observed in the genomes of bacterial isolates derived space76. This highlights the interkingdom cooperation

Reviews
among microbiomes in order to promote the successful and cross-kingdom signalling. Siderophore-producing
colonization of plant habitats. gene clusters were enriched in the rhizosphere of
Siderophores are important in various ecological barley6, citrus15 and grapes8 compared with the bulk
phenomena, including iron biogeochemical cycling in soil. Metagenomic analysis further revealed enrichment
soils, pathogen competition, plant growth promotion of siderophore-producing genes in the endosphere
Plant interior
Root exudates
Endophytic colonization
• Enzymes
Intermicrobial interactions (detoxification↑, lytic↓)
• Toxins • Transcriptional regulators Receptor
Start soil • MAMP↓
• Defence systems
inoculum • Secretion systems↓
• Antibiotic-resistance genes
• CRISPR • Effectors
• PREPARADOs ↓ MAMP
• Quorum-sensing systems
• Two-component systems Effectors
Metabolism Chemotaxis and Biofilm production

and transport cell motility • Two-component, Stress
• Degradation • Motility proteins three-component or
• Substrate • Flagellum assembly multicomponent
utilization systems
• Metabolite • c-di-AMP
uptake • Plant compounds Scopoletin
• Amino acid and signals
metabolism
Recruitment of stress-resistant microbiome
Altered root exudation
Fig. 2 | Plant colonization and microbiome assembly. Multiple and coordinated regulation of biofilm formation. The second messenger cyclic
complex plant–microorganism and microorganism–microorganism di-adenylate monophosphate (c-di-AMP) mediates interbacterial cell–cell
interactions are required for the selective assembly of plant-associated communication and the initiation of biofilm formation by influencing the
microbiomes. Microbial-mediated processes, pathways and proteins that expression of genes involved in biofilm production. Genes involved in
are related to colonization (metabolism and transport; intermicrobial motility, chemotaxis, adhesion and biofilm production further contribute to
interactions; chemotaxis and cell motility; biofilm production; and plant colonization and the endophytic lifestyle within the host plant.
effector-mediated colonization and stress responses) are shown. The plant Suppression of plant-produced reactive oxygen species by microbial
interacts with the microbiome through the release of root exudates detoxification enzymes such as superoxide dismutase, catalase, peroxidase,
(for example, organic acids, sugars and secondary metabolites) throughout alkyl hydroperoxide reductase and glutathione-S-transferase facilitates
its developmental stages. The microorganisms in the bulk soil act initial endophytic colonization. Entry into plant tissues is facilitated
as ‘seed banks’ and vary in their genomic potential to degrade, utilize by the production of lytic enzymes such as lysozymes or cell-wall-
and metabolize distinct metabolite substrates in the root exudate. degrading enzymes. It is postulated that endophytes produce low levels of
A rich repertoire of transporters confers selective advantage to a few lytic enzymes as compared with pathogens, thus avoiding triggering the
microorganisms in taking up various plant-derived metabolites. Subsequently, plant immune response. Diversification of microbial-associated molecular
the community is shaped by intense microorganism–microorganism patterns (MAMPs) circumvents recognition by the plant immune response
interactions mediated via the strain-specific production and perception of and is likely to shape endosphere microbial assemblages in plant
antimicrobial molecules. Signalling events mediated by quorum sensing or populations. Type 3 and type 4 secretion systems that deliver effector
other two-component systems have a key role in both intermicrobial and proteins are absent or are present in low numbers in the endophytes, thus
intramicrobial communications among different species. CRISPR-associated minimizing the activation of plant defences. However, effector-mediated
genes provide adaptive immunity against bacteriophages and are under colonization of the plant interior has been reported for Rhizobium-type
strong selection pressure in plant-associated microbiomes. The presence bacteria or mycorrhizal fungi. Gene products from eukaryotic-like plant-
of antibiotic-resistance genes may provide protection against biological resembling plant-associated and root-associated domains (PREPARADOs)
and chemical warfare (for example, toxins and defence systems) that occurs are speculated to mimic the host cell signalling, thus acting as decoys to
during the initial stages of community assembly. Subsequently, the circumvent plant defences and gain entry into plant tissues. Overall, the
microbial community moves towards the plants through chemotaxis, interplay between plants and their endophytic microbiota is complex and
involving motility proteins and the assembly of flagella. Further colonization still far from being fully elucidated. Under biotic and abiotic stress conditions,
is mediated through sophisticated communications between plants plants can change their exudation patterns in order to selectively recruit
and microbial communities, leading to the formation of a biofilm on a beneficial ‘stress-tolerant microbiome’. For example, under iron or
plant surfaces. Plant-produced compounds and signals not only induce phosphorus stress conditions, the transcription factor MYB72 and the
biofilm production but also affect the architecture of the biofilm. β-glucosidase BGLU42 (not shown) induce the biosynthesis and exudation
Different two-component, three-component or multicomponent sensing of scopoletin, which has antimicrobial activity and selects for beneficial
and regulatory microbial pathways are involved in the integrated and microorganisms that ameliorate stress (altered root exudation).

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Siderophores compared with the rhizosphere in Populus deltoides77 and of plant–microbiome co-evolution in the rhizosphere
Low-molecular-weight organic rice78. However, this was not reflected in the comparative and suggest an arms-race co-evolution model in natural
chelators with a very high and genome analysis of bacterial isolates77. The prevalence of communities similar to the model proposed for binary
specific affinity for ferric iron, siderophore gene clusters across multiple biosynthetic plant–pathogen interactions82. Another mechanism
which scavenge iron from the
environment and make the
pathways suggests that the possession of traits that of plant defence evasion in plant-associated micro
element available to microbial facilitate competition for limiting resources provides organisms could be the ability to disperse from the ini-
cells and/or a plant host. a selective advantage to microorganisms in colonizing tial site of colonization after triggering a plant defence
plant roots. response25. In this respect, genes involved in biofilm
Effector proteins
production or in the regulation of such genes are impor-
Proteins produced by
plant-associated Evading plant defences. Evasion or suppression of the tant to altering colonization patterns and evading the
microorganisms that modify plant immune system is not only essential for path- induction of a host defence.
plant functioning in order ogens to successfully infect plant hosts but also crit-
to promote microbial ical for commensals to colonize different plant niches Microbial interactions. It is not surprising that several
colonization.
(Supplementary text S1). The plant-associated micro- microbial genes active and/or enriched in plant envi-
Quorum sensing biota must cope with a host immune system that can ronments have a role in cooperative or competitive
Population-density-dependent recognize microorganism-associated molecular pat- interactions with other members of the microbiome.
regulation of gene expression, terns (MAMPs), such as flagellin, lipopolysaccharides, Diverse and distinct gene clusters for natural-product
mediated by the production
chitin and elongation factor Tu-derived peptides79. biosynthesis from 339 plant-associated bacteria were
of signal molecules called
autoinducers. Plant perception of MAMPs involves conserved signal- reported77. As the genetic potential of bacteria to syn-
transduction mechanisms, including the generation thesize different types of natural products influences
of reactive oxygen species, the activation of mitogen- microorganism–microorganism and microorganism–
activated protein kinases (MAPKs) and the induction plant interactions, a comprehensive understanding of
of salicylic acid-signalling and jasmonic acid-signalling the plant microbiome will require greater knowledge
pathways79. To overcome host immune surveillance, of how these compounds are produced and regulated
microorganisms secrete effector proteins . Some of and of their mechanism of action. The genomes of
these effector proteins emerged from convergent evo- many plant-associated bacteria encode interspecific and
lution and horizontal transfer of genes encoding pro- intraspecific bacteria-killing mechanisms (for example,
tein domains from eukaryotes, such that the effectors the production of antibiotics), through which they can
mimic plant proteins. Recently it was revealed that modulate the distribution, abundance and diversity of
plant-resembling plant-associated and root-associated other microbial groups within the plant host77. Specific
domains (PREPARADOs) were highly abundant in the functional traits related to pathogen suppression (for
genomes of plant-associated and root-associated bacte- example, protein secretion systems and biosynthesis
ria compared with soil and non-plant-associated bac- genes for antifungal compounds) are more abundant in
terial genomes23. Some PREPARADOs themselves are the bacterial rhizosphere community of disease-resistant
domains within effectors and are predicted to be secreted varieties of bean and tomato than in susceptible varie-
by the general secretory pathway or type 3 secretion sys- ties or in bulk soil83–85. Pathogen-induced activation of
tem (T3SS)80. PREPARADOs may represent a ‘camou- chitinase genes and various unknown biosynthetic gene
flage’ strategy to evade MAMP-triggered immunity by clusters encoding non-ribosomal peptide synthetases
binding to extracellular MAMP molecules (for exam- (NRPSs) and polyketide synthases (PKSs) is responsi-
ple, mannose) and thereby functioning as a molecular ble for disease-suppressive functions in the endophytic
invisibility cloak. A large set of PREPARADO domains root microbiome86. Genome mining of phyllosphere
are shared between plants, plant-associated fungi, oomy- bacteria has identified more than 1,000 biosynthetic
cetes and bacteria, which suggests convergent evolution gene clusters (BGCs) that belong to diverse biosyn-
or cross-kingdom horizontal gene transfer between phy- thetic classes, including ribosomally synthesized and
logenetically distinct organisms subjected to the shared post-translationally modified peptide and terpene sys-
selective forces of the plant environment. Interestingly, tems, NPRSs and trans-AT PKSs87. These BGCs are pos-
genes encoding proteins involved in the T3SS are higher tulated to be involved in microorganism–microorganism
in nodule-forming symbionts and phytopathogens interactions and niche adaptations. In addition to anti-
than in endophytes. By contrast, those genes are found in biotic production, genes related to antibiotic resistance
a substantially larger number of endophytes than in soil were also enriched in the plant environment15, which
bacteria81. Thus, it will be essential to understand how suggests an intense microbial arms race that controls the
some taxa exploit virulence mechanisms for symbiotic microbial community structure.
associations and plant colonization. Quorum sensing is a well-e stablished mechanism
Notably, several factors implicated in host–pathogen of bacterial cell-to-cell communication that involves
interactions (such as T3SS, regulation of virulence, the production and sensing of signalling molecules
invasion and intracellular resistance), microorganism– (such as homoserine lactone (HSL))88. Different bac-
microorganism interactions (T6SS) and bacteria–phage terial taxa can generate the same type of signalling
interactions (bacteriophage integration and transposable molecule, which enables either cooperation or inter-
elements) were found to be enriched in healthy citrus ference (quorum quenching) with other unrelated
rhizosphere samples collected from across the globe15,71, taxa. Moreover, quorum-sensing molecules also have
as well as in the barley6 rhizosphere, relative to bulk soil a role in interkingdom interactions. The perception
samples. These signs of positive selection are evidence of HSLs by plants leads to modulation of the plant

Reviews
Carotenoid metabolism, immune response and root development89. are systematically isolated and functionally character-
An organic pigment produced Quorum-sensing-mediated swarming of the finger millet ized, followed by the reconstitution of communities with
by plants, algae and several endophyte M6 (Enterobacter sp.) towards root-invading increasing complexity and gnotobiotic assays in order
groups of bacteria and fungi. Fusarium graminearum, along with its formation of to quantitatively assess host–microbiome interactions98.
microcolonies, results in a multilayer root-hair endo- Recent research has emphasized the importance
phyte stack90 that forms a physical barrier that prevents of eco-e volutionary processes in the assembly of
entry and/or traps the pathogen, which is subsequently plant-associated microbiomes, such as dispersal (move-
killed. The metagenomic analysis of plant-associated ment of microorganisms between different niches),
microbiomes15 has shown enrichment of HSLs in the selection (biotic and abiotic effects causing fitness dif-
plant environment compared with bulk soils. About ferences), ecological drift (stochastic changes in popu-
40–50% of the bacteria isolated from plant environments lation size that influence the abundance of a particular
showed HSL activity77,91. Genes for terpene biosynthe- member) and diversification (processes that generate
sis were present in the largest number of genomes of genetic variation)99. Both stochastic colonization and
plant-associated bacteria, with 49% of isolates carry- historical contingency may have essential roles in struc-
ing a gene encoding a terpene synthase77. Terpenoids turing the plant-associated microbiome. Microbial com-
have diverse biological and ecological functions, such munity structure in the rhizosphere67 and phyllosphere40
as carotenoid production, as well as functioning as is initially determined by stochastic processes. The order
chemical defences against herbivores and pathogens92. and timing of species arrival and dispersal (also known
Bacterial terpenes are implicated in interkingdom sig- as priority effects) influence all the eco-evolutionary
nalling, as these volatile compounds elicit profound processes that affect assembly of the plant-associated
responses from plants93. Specific microbial colonization microbiome. Priority effects can cause historical con-
on the ‘local side’ induces microbiome-reprogrammed tingency to affect both the structure and function of
systemically induced root exudation of metabolites the plant-associated microbiome and therefore can
(SIREM), and microbial colonization on the ‘systemic have long-lasting consequences for plant performance.
side’ results in long-distance communication between Although the initial microbiome community is robust,
unshared microhabitats of tomato rhizosphere94. For plants can accommodate new species without substan-
example, inoculation of bacteria that belong to the tially changing the pre-existing community40. Rare taxa
orders Bacillales or Pseudomonadales on the local side are postulated to provide a robust reservoir of ecological
induces the accumulation of bacterial-specific SIREMs. functions and could drive priority effects in microbiome
Transportation of these signals through shoots to the assembly during the early stages of plant development,
unshared area of roots facilitates the assembly and colo- with variable consequences for plant performance at
nization of SIREM-specific microbial populations on the later stages67. Determining the principles governing
systemic side. the assembly, dynamics, stability and vulnerability to
Bacterial T6SSs inhibit competitor cells through disturbance of the microbiome, including the roles of
a toxic effector and its cognate immunity protein95. biotic and abiotic factors, will lead to a better mechanis-
Microorganisms that can successfully colonize plant tic understanding of the influence of the microbiome
environments may use not only host colonization factors on both the fitness and function of plant hosts (Box 1,
but also mechanisms to exclude closely related compet- Supplementary text S1).
itors. Multiple T6SS genes were found to be enriched
in the rhizosphere communities of barley6, citrus15, Functions of plant-associated microbiomes
wheat and cucumber5. A new family of T6SS effectors, Nutrient acquisition. Plant-associated microbiomes have
‘Hyde1’, which is specific to Acidovorax phytopathogens essential functions in improving plant nutrition (Fig. 3).
(absent from Acidovorax commensals), is efficient in The molecular mechanisms driving nutrient acquisition
controlling various leaf bacterial isolates, suggesting a have been thoroughly studied for plant symbioses with
role in interbacterial competition in plants23. Despite the arbuscular mycorrhizal fungi (AMF) and Rhizobium
broad distribution of interbacterial T6SS killing mech- bacteria27–30. Moreover, non-symbiotic plant-growth-
anisms, few studies have investigated their ecological promoting bacteria can either enhance the bioavaila-
roles96,97. Interestingly, some CRISPR-associated pro- bility of insoluble minerals or improve the root system
teins have shown positive selection pressure in the root architecture of host plants, thus increasing the explor-
environment6, which indicates that microorganisms face atory capacity of the root for water and minerals27,29.
intense selection pressures from bacteriophages. The functional plant traits related to the acquisition or
In summary, an extensive repertoire of traits involv- conservation of nutrients that differentiate exploitative
ing resource acquisition, motility, habitat modification (fast-growing) versus conservative (slow-growing) plant
and various microorganism–microorganism or plant– species are contributed by their associated microbiome27.
microorganism interactions may be needed by members A recent study showed that differences in the nitrogen
of the plant microbiota in order to colonize the plant use efficiency of rice varieties is due to the recruitment
environment (Fig. 2). However, most of this knowledge of a higher proportion of nitrogen-cycle-related bacteria,
has come from reductionist experiments and does leading to more efficient nitrogen transformation pro-
not consider the modular and synergistic interactions cesses in the root environment of Oryza indica than of
under the holobiome concept. Bottom-up experimental Oryza japonica varieties38. Notably, a 16-member indica-
approaches are now needed, whereby diverse microbial enriched SynCom substantially promoted the growth
members from different plant-associated environments of an indica variety in comparison to a 3-member

Reviews
Mitigate
abiotic stress
Promote
growth Defence
Prevent dysbiosis Induced systemic

resistance
• Microorganism–
microorganism
interactions
• Hub microorganisms
Protect against pathogens

and invertebrate pests
Stimulate
Indirect Direct
• Plant hormones • Secretion systems • Competition
• ACC deaminase • Pili • Siderophores
• Osmoprotectants • Lytic enzymes
• Detoxification enzymes • Antibiotic secretion
• Volatiles
NH4+ NO3–
Unlock essential nutrients Enhance nutrient uptake Nitrogen fixation
SO42– Fe2– Pi Nodules

K+ Mg++ PO4+
NO3– N2
Plant available nutrients
Mycelium
Nodulating bacteria
(for example, Rhizobium,
Mineral elements Frankia, Bradyrhizobium)
Arbuscle Nitrogen-fixing
Nitrifying bacteria
• Solubilize
• Oxidize
NO3 –
bacteria
• Chelate
NH4+
Organic acid,
siderophore Ammonifying
bacteria
Root NH4+ Hyphae of arbuscular
exudates mycorrhiza
Arg Humus
japonica-enriched SynCom when organic nitrogen was nitrogen into bioavailable forms) resulted in a ten-
used as the sole nitrogen source. This suggested that fold increase in the uptake of nitrogen from organic
effective transformation of organic nitrogen into nitrate matter in Brachypodium distachyon as compared with
and ammonium by the indica-enriched microbiome non-microbial controls100. It is predicted that these pre-
may contribute to higher nitrogen use efficiency in viously unquantified associations may contribute to
indica rice. >70 teragrams (1012 g) of annually assimilated plant nitro-
Multipartite microbial synergies between mycor- gen, with a positive impact on net primary productivity100.
rhizal fungi (which promote nitrogen acquisition but Plant traits involved in nutrient use efficiency are related
have limited ability to access organic nitrogen) and to the differential colonization of plants with two major
soil microbial communities (which mineralize organic groups of mycorrhizal fungi101. Plants that are colonized

Reviews
◀ Fig. 3 | Beneficial effects of the plant-associated microbiome. The plant-associated thereby increasing the uptake of inorganic phosphate
microbiome can provide benefits to the plant through various direct or indirect by plants37. Non-mycorrhizal plants assemble a core
mechanisms. These benefits include growth promotion (blue), stress control (green) inorganic-phosphate-assimilating fungal microbiome
and defence against pathogens and pests (red). Microbiome-mediated benefits can be that expands the ability of plants to grow in phosphate-
initiated in any part of a plant (mostly belowground) and can be transmitted to other
depleted soils 104. Phosphate- s tarvation- m ediated
parts via plant-mediated transport or signals (shown as blue, green and red dashed
arrows, representing mechanisms that contribute to plant growth, stress relief and
repression of the immune response enables a build-up
defence, respectively). Direct effects are mediated through nitrogen fixation, through of mutualistic plant–fungal associations that increases
unlocking of essential nutrients from minerals and through enhancing the capability plant inorganic-phosphate uptake105. Such observa-
of plants to take up nutrients from the soil. In addition, other direct effects include tions suggest that fine-tuned interactions between
the stimulation of plant growth via stress alleviation, through the modulation of the nutritional and immune status of plants regu-
aminocyclopropane-1-carboxylate (ACC) deaminase expression and the production late microbiota-mediated beneficial functions. The
of plant hormones, detoxification enzymes and osmoprotectants. Benefits can also be A. thaliana root bacterial community is shaped by
indirect, as the plant-associated microbiome protects the plant against pathogens or coumarins, plant-derived specialized secondary metab-
pests through antagonism or through inducing systemic resistance in plants. Complex olites that on the one hand facilitate iron mobilization
microorganism–microorganism and host–microorganism interactions maintain the
and on the other generate reactive oxygen species
balance between different members of the microbial community in favour of beneficial
microorganisms that contribute to plant health (yellow). Diazotrophic bacteria can fix that inhibit the proliferation of a relatively abundant
atmospheric nitrogen (N2) and might actively transport ammonium (NH4+) and nitrate Pseudomonas species that competes with plants for
(NO3−) to the host. Ammonifying bacteria convert organic N2 present in the soil to NH4+, iron106. The root-specific transcription factor MYB72
which is further converted to NO3− by nitrifying bacteria. Leguminous plants develop root has an important role in both rhizobacteria-mediated
nodule symbiosis with N2-fixing bacteria. Arbuscular mycorrhizal fungi convert arginine induced systemic resistance (ISR) and iron acquisition107.
(Arg) to urea and then to NH4+. Microbiomes can unlock essential elements by oxidizing, Interestingly, volatile compounds from ISR-inducing
solubilizing or chelating minerals into plant-available nutrients such as phosphate (Pi), rhizobacteria and Trichoderma fungi elicit the expres-
nitrogen (NH4+) and potassium (K+) through the production of organic acids and sion of MYB72 in order to induce the genetic machin-
siderophores. Furthermore, arbuscular mycorrhizal fungi might enhance nutrient ery for enhanced iron uptake by roots108. Adjustments
availability by long-distance transport through the mycelium and specialized structures
in local iron homeostasis transmit systemic signals to
called arbuscules (fungal hyphae ensheathed in a modified form of the cortical cell
plasma membrane) that transport elements directly to the host cytoplasm. Microbiomes
plant shoots to induce jasmonic-acid-dependent ISR108.
can stimulate plant growth by metabolizing tryptophan and other small molecules in These recent studies have shed light on the vital role
the plant exudates and producing phytohormones that include auxins, gibberellins, of plant-associated microbiomes on plant functioning
cytokinins and phytohormone mimics. Auxins can also induce transcription of the ACC and open up multiple opportunities to manipulate plant
synthase that catalyses the formation of ACC. ACC, the direct precursor of ethylene, is characteristics by using microbial interventions.
metabolized by bacteria via the enzyme ACC deaminase, thus ameliorating abiotic stress.
Members of plant-associated microbiomes produce a range of enzymes that can detoxify Disease resistance. The impact of natural microorganism-
reactive oxygen species, thus minimizing plant-induced stress. The plant-associated based plant defence on plant health is evidenced most
microbiome protects the plant against pathogens by the production of antibiotics, lytic clearly in disease-suppressive soils, whereby plant root
enzymes, volatiles and siderophores. Various microbial structures — such as secretion
exudates stimulate, enrich and support soil microor-
systems, flagella and pili — along with proteins such as effector proteins, indirectly
contribute to plant defence by triggering an induced systemic resistance response. ganisms as the first line of defence against soil-borne
Siderophore-mediated nutrient competition between commensals and plant pathogens pathogens32. Community-based analyses of suppres-
can reduce pathogen titres. Interkingdom and intrakingdom interactions within the sive soils have demonstrated that no single phylum was
microbiome maintain the microbial balance, thus protecting plants from dysbiosis. uniquely associated with disease suppression32–34,109,110.
Furthermore, hub microorganisms can amplify host signals in order to promote the Although the interactions between microbial consor-
assembly of a microbiome that provides benefits to the plant. Overall, beneficial tia and a specific pathogen that result in disease sup-
plant–microbiome interactions improve the growth performance and/or health of plants. pression are biologically complex, similar mechanisms,
such as the production of antifungal metabolites32,110 and
with ectomycorrhizal fungi adopt nutrient conserva- volatiles111,112 by different bacterial genera, are responsi-
tion strategies, whereas plants that are colonized with ble for the build-up of disease-suppressive soils. If the
AMF are nutrient acquisitive101. Rhizosphere micro pathogen breaches the first line of rhizosphere-mediated
organisms that prolong nitrogen bioavailability by disease resistance, the endophytic microbiome can pro-
nitrification delay flowering time and stimulate plant vide an additional layer of protection through selective
growth by converting tryptophan to the phytohormone enrichment of microbiome members that possess genetic
indole acetic acid (IAA), which downregulates genes that machinery to produce enzymes and secondary meta
trigger flowering102. bolites against the pathogen86. Interestingly, the MAMP-
Plant-associated microbiota can mobilize nutri- triggered immunity pathway is induced to higher levels
ents that are not readily available to plants, such as in disease-suppressive soils113. Management practices
inorganic phosphate and iron, through solubilization, such as crop rotation, residue retention and compost
mineralization or excretion via iron-chelating sidero- additions can induce general or specific disease sup-
Induced systemic resistance phores (Fig. 3) . Under conditions of low inorganic pression by affecting microbiome composition driven
(ISR). A physiological ‘state of phosphate, plants rely on microbial cooperation part- by the greater availability of carbon114. A recent study34
enhanced defensive capacity’ ners, including AMF and their symbiotic endophytes, modelled general disease suppression against Fusarium
of the entire plant against
to satisfy needs for this essential nutrient103. Under oxysporum and determined that the abundances of bac-
diverse pathogens and
herbivores that is induced
phosphate-limiting conditions, SynComs of differ- teria in the phyla Actinobacteria and Firmicutes can
by local stimulation through ent complexity enhanced the transcription of plant be used as predictive markers of disease-suppressive
beneficial microorganisms. genes involved in phosphate starvation responses, soils at the continental scale. Disease-resistant traits of

Reviews
a tomato variety have been attributed to the selective The mechanisms underlying microbiome-induced
recruitment of bacteria that can antagonize the wilt path- flowering plasticity remain unknown, but probably
ogen, Ralstonia solanacearum84. Microbiome-mediated they include a combination of direct effects of the micro
plant protection can be transferred and maintained via biome on plant physiology and indirect effects mediated
soil transplantations67,84. SynComs constructed on the by soil nutrient availability. Drought-mediated produc-
basis of knowledge of the microorganisms in disease- tion of the plant hormone abscisic acid dampens the
suppressive soils have been reported to control diseases plant immune response, thus facilitating large shifts in
in field conditions32,33. the root endophytic community12. These fluctuations
ISR can be triggered by plant-growth-promoting bac- mitigate water stress, possibly through the production
teria and fungi residing in the rhizosphere28. Local sup- of plant hormones and/or changes in the biochemi-
pression of root immune responses is a common feature cal activity of host plants12. Plants respond to multiple
of ISR-eliciting beneficial microorganisms.28. Pathogen stresses by upregulating the physiologically costly ethyl-
infection causes alterations in root exudation patterns ene signalling pathway, which causes trade-offs between
that result in the selective recruitment of ISR-inducing stress resistance and growth rate125. Both microbial eth-
microbiota83,113. The presence of heterogeneous microbial ylene reduction and gene mutations that disrupt ethyl-
communities living on the surface of the aboveground ene signalling in plants have strong pleiotropic effects,
portion (the episphere) and the endosphere of tomato with increased plant growth, but at the cost of strong
plants modulates phenylpropanoid metabolism (involved stress hypersensitivity35. These findings suggest that
in salicylic acid synthesis), which leads to cell wall fortifi- plant–microbiome interactions are neither beneficial
cation that protects the plant from Fusarium oxysporum nor deleterious, but instead function as modulators,
f. sp. lycopersici110. Cell wall fortification functions as a generating new phenotypes by reshuffling existing
barrier not just against pathogen attack but also against traits. Interestingly, for fungal endophytes, traits related
abiotic stresses such as salinity, which suggests a direct to resource use and stress tolerance predicted 26–53% of
interplay between stress tolerance and immunity115. The the endophyte-mediated effects on plant performance
induction of jasmonic acid signalling and plant defences under water stress126. The moderately predictive effect of
modulated by root-associated bacterial and fungal com- functional microbial traits for plant performance can be
munities also affects aboveground insect herbivory116. used to develop a framework for screening new micro-
Remarkably, ISR induction by plant-associated microorganisms that can increase plant fitness under stress
biomes drives the secretion of antimicrobial compounds conditions (Box 3).
such as coumarin107 and benzoxazinoids117 that further
intensify the recruitment of ISR-inducing strains. This Conclusions
suggests that plant immune responses can be manipu- In recent years, plant–microbiome research has bene-
lated so as to recruit microorganisms that provide sta- fited enormously from cross-disciplinary efforts that
ble plant protection over multiple generations. Through have brought concepts from multi-‘omics’, engineer-
plant–soil feedbacks and legacy effects, the selective ing, theory, experimental biology, computational bio
enrichment of microbial communities in response logy and statistics to generate quantitative insights into
to both biotic and abiotic stresses can affect plant plant–microbiome interactions. The extensive survey
immunity in subsequent generations118. Engineering of a few models and of important crops, plants and
plant-associated microbiomes to control plant disease trees have established a ‘parts list’ of the major bacterial
will continue to require a deeper understanding of the and fungal associates, although a vast amount of novel
plant–microbiome–environment interactions among diversity remains to be discovered for most plants.
diverse crops of interest. A systematic approach to identifying the microbiomes
of ecologically and economically important plant spe-
Stress tolerance. Plant- a ssociated microorganisms cies, comparable to human microbiome approaches, will
could modify plant evolutionary responses to environ- be needed in order to identify core and hub microbiota
mental stress in at least three non-mutually-exclusive and the host functions they provide. Although bacterial
pathways: by altering the fitness of individual plant and fungal lineages contribute the vast majority of the
genotypes, the expression of plant traits related to fit- plant-associated microbiome by abundance, there is a
ness, and the strength or direction of natural selection critical knowledge gap concerning the shape and drivers
occurring within populations that experience environ- of other fractions of the plant microbiome (for example,
mental stress through the microorganisms’ effects on viruses, archaea, protists and nematodes) that influence
reproductive fitness12,69,119,120. Plants generally select a bacterial and fungal communities via bottom-up and
stress-resistance-promoting microbiome under abiotic top-down processes. GWASs and metagenome-wide
or biotic stress conditions119–124 (Box 3, Supplementary association studies have identified key drivers that
text S1). The plant traits favoured under adverse con- influence the assembly of plant-associated microbiota
ditions, especially drought, may depend on changes in and have linked individual microbial taxa and genes to
the associated microbiome. Several recent studies have plant colonization, plant physiology and traits related
shown that naturally occurring and artificial variation to plant fitness. However, they have also revealed that
in the microbiome can alter plant flowering time on the large proportions of the variation in community assem-
order of 1–5 days69,119,124. Drought-induced early flow- bly and the effects of microbiomes on plant fitness
ering has been proposed as a potential mechanism of remain unexplained. To elucidate these gaps, larger-scale
drought avoidance. longitudinal studies will be needed to establish baselines

Reviews
Phytobiome
for plant-associated microbiomes, with explicit consid- will be able to resolve some methodological and tech-
Plants, their environment eration of temporal dynamics and host age. In recent nological challenges. These include the translation of
and all microorganisms and years, some progress has been made in elucidating data into phenotypic links, experimental modelling
macroorganisms living in, multipartite (for example, plant–animal–soil or plant– through co-cultivation or gnotobiotic methods, and
on or around the plants.
environment–soil) interactions in the phytobiome; how- multiscale computational simulations. These integrative
ever, we have very little knowledge on the functional approaches will combine the skills, methodologies and
properties of the microbiome. The limited but increas- expertise from a range of disciplines within the sciences,
ing functional understanding of the microbiome is engineering and beyond. Increased understanding of
beginning to be translated into accepted practice, in the the dynamic plant–microbiome–environment interac-
form of the development and application of SynComs to tions will provide a way forward to engineering com-
increase plant fitness and productivity (Supplementary plex microbial consortia with predictable behaviour
text S2). However, a consensus on the desired microbial and robust outcomes. By closely coupling modelling
endpoints (what is a ‘healthy’ microbiome) has yet to be with experimental approaches, we expect that scien-
determined. Similarly to breeding, the plant microbiota tific advancement will be accelerated, creating a future
may affect the plant phenotype. Although the optimi- in which the activities of indigenous microbiomes
zation of SynComs is rapidly advancing, crop-breeding can be reliably enhanced and in which engineered
programmes have not yet incorporated the selection of microbiomes can be deployed safely and effectively in
beneficial plant–microorganism interactions in order to large-scale field settings for improved and sustainable plant
breed ‘microorganism-optimized’ plants. production.
Moving forward, we envision that the next gener-
ation of computational and experimental approaches Published online 12 August 2020
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REVIEWS

Plant–microbiome interactions: from

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Bulk soil Bulk soil

(Shannon diversity index (H))

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Metabolism Chemotaxis and Bioﬁlm production

Altered root exudation

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Prevent dysbiosis Induced systemic

Protect against pathogens

SO42– Fe2– Pi Nodules

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