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Scientia Agricola
http://dx.doi.org/10.1590/0103-9016-2014-0195

Review
Exploring interactions of plant microbiomes
Fernando Dini Andreote*, Thiago Gumiere, Ademir Durrer

University of São Paulo/ESALQ – Dept. of Soil Science, C.P. ABSTRACT: A plethora of microbial cells is present in every gram of soil, and microbes are found
09 – 13418-900 – Piracicaba, SP – Brazil. extensively in plant and animal tissues. The mechanisms governed by microorganisms in the
*Corresponding author <fdandreo@gmail.com> regulation of physiological processes of their hosts have been extensively studied in the light
of recent findings on microbiomes. In plants, the components of these microbiomes may form
Edited by: Paulo Cesar Sentelhas distinct communities, such as those inhabiting the plant rhizosphere, the endosphere and the
phyllosphere. In each of these niches, the “microbial tissue” is established by, and responds to,
specific selective pressures. Although there is no clear picture of the overall role of the plant mi-
crobiome, there is substantial evidence that these communities are involved in disease control,
enhance nutrient acquisition, and affect stress tolerance. In this review, we first summarize fea-
tures of microbial communities that compose the plant microbiome and further present a series
of studies describing the underpinning factors that shape the phylogenetic and functional plant-
associated communities. We advocate the idea that understanding the mechanisms by which
plants select and interact with their microbiomes may have a direct effect on plant development
and health, and further lead to the establishment of novel microbiome-driven strategies, that can
Received May 30, 2014 cope with the development of a more sustainable agriculture.
Accepted July 22, 2014 Keywords: microbial communities, rhizosphere, endophytes, phyllosphere

Introduction space in our body” (Lederberg and McCray, 2001). Hence,

the human body is a great reservoir of microbes, recent-
Surveys performed on interactions between plants ly broadly studied by the Human Microbiome project,
and microbes are numerous, and have traditionally fo- which linked several features of the host to the presence
cused on pathogenic interactions. However, after several of specific sets of microbial groups (Turnbaugh et al.,
descriptions and attempts to assess the occurrence and 2006; Djikeng et al., 2011; The Human Microbiome Proj-
the role of microbial diversity associated with plants, ect Consortium, 2012). More recently, the use of this term
it is assumed that only a minor fraction of plant-inter- has been broadly applied to different sets of microbes
acting microbes are pathogenic. Most microbes inhabit- found in specific hosts or inhabiting a given environment
ing plant-related niches have neutral or beneficial roles (Boon et al., 2014; Ofek et al., 2014). Boon et al. (2014)
in plant health and development (Beattie and Lindow, proposed that the best definition of ‘microbiome’ would
1995; Hallmann et al., 1997; Mendes et al., 2013; Philip- relate to the set of genes encountered in association with
pot et al., 2013). the host or a defined environment, thus diminishing the
Microorganisms can affect agricultural produc- importance of the link between taxonomy and functional-
tivity, for instance by assisting and controlling nutrient ity of the microbial community members. These assump-
availability/acquisition and promoting stress tolerance tions made feasible the application of the microbiome
(Doornbos et al., 2011; Ferrara et al., 2012; Kavamura concept to plants, which carry out several essential func-
et al., 2013). Most of the research on this topic has fo- tions in association with distinct microbial groups. Some
cused on the functional roles of single microbial groups authors have addressed this issue, such as Bulgarelli et al.
(e.g., specific species or organisms from the same genera) (2013), Turner et al. (2013a) and Rout (2014).
associated with plants, mostly because of methodologi- In this review article, we focus on the description
cal limitations to assess non-culturable microbial groups of plant microbiomes by not only describing the compart-
(Amann et al., 1995; Andreote et al., 2009). Examples of ments where the microbes live (rhizosphere, endosphere
these inferences are related to specific microbial groups and phyllosphere) but by also discussing the importance
able to promote plant growth, such as nitrogen-fixing of interactions between plants and microorganisms. Due
bacteria (Raymond et al., 2004) and mycorrhiza-forming to the availability of data, most examples focus on bacte-
fungi (Chagnon et al., 2013). However, a holistic view rial fractions of the microbiome or the bacteriome. How-
of this system highlights the importance of interactions ever, data and discussions on fungal communities are
occurring amongst distinct microbial groups, resulting in also presented. This review was organized to offer an
the coining of the term ‘microbiome’. overview of the plant-associated microbial communities,
The word ‘microbiome’ was first used by Joshua followed by a description of the role played by plant mi-
Lederberg as the “ecological community of commensal mi- crobiomes, and finally a portrayal of microbiome-related
croorganisms, symbionts or pathogens, that literally occupy a initiatives underway in Brazil.

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Plant-associated microbial communities

The soil matrix is the major reservoir of microbes
that interact with plants, being described as the most bio-
diverse ecosystem on Earth (Vogel et al., 2009). The soil
microbiome is responsible for important processes occur-
ring in this environment, which directly relate to plant
health. For instance, the soil microbiome suppresses plant
diseases by imposing physiological restrictions on patho-
gens establishing and infecting plant tissues (Weller et al.,
2002; Mendes et al., 2011). Equally, the soil microbiome
also imparts a certain degree of resistance to the system
against “invaders”, thereby linking the diversity of the mi-
crobiome to its intrinsic ability to restrict or inhibit the
survival of exogenous organisms (Elsas et al., 2012).
Although the presence of microbes in plants ini-
tially related to the occurrence of diseases, it is now rec-
ognized that the vast majority of microbial organisms are
not causal agents of damage in plants (Mendes et al., Figure 1 − Schematic representation of the major sources for
2013). Several functions have been attributed to micro- microbes that compose the plant-associated communities: the
bial cells in close association with plants, for instance, rhizosphere, endosphere and phyllosphere. Thickness and fill of
their ability to provide nutrients, such as (i) phosphorus connections indicate the contribution of environmental sources
solubilization and nitrogen fixation; (ii) their support of for the composition of microbial communities in plant-harboring
nutrient uptake from the soil, as described for the mycor- niches.
rhiza; and (iii) their capacity to promote plant protection
by hindering agents of plant stresses, such as infection
by pathogens and pests (Halmann et al., 1997; Mendes sphere is composed of those organisms that intimately
et al., 2011; Mendes et al., 2013; Quecine et al., 2014). interact with the host and inhabit inner plant tissues as-
Despite the substantial progress allowed by culti- ymptomatically (Hallmann et al., 1997; Hardoim et al.,
vation-dependent methods, due to “the great plate count 2008), and the phyllosphere is defined by microbial cells
anomaly,” only a small fraction of the microbes in nature that are able to colonize plant surfaces (Lambais et al.,
(ca. 1 to 5 %) are represented by standard cultivation 2006; Lindow and Brandl, 2003).
methods for communities retrieved from natural envi- The richness of species and diversity of microbial
ronments (Amann et al., 1995). Hence, an exploration communities that comprise the plant microbiome, as
of plant microbiomes that encompasses the whole set well as the factors affecting it and their performance, are
of microorganisms interacting with plants might lead to mostly unknown. It is likely that one single plant species
the description of numerous other functions that the as- has thousands of epiphytic and endophytic microbial
sociated “microbial tissue” exerts when interacting with species, and the interactions between these microorgan-
the host plant. Some authors claim that a co-evolution isms might regulate several physiological processes in
process occurs between plants and its associated micro- the host. In combination with these factors, the influ-
biome, resulting in a strong genomic interdependency, ence of abiotic drivers, such as soil characteristics or the
leading to the “metaorganism” concept (Bosch and Mc- edaphoclimatic area where the plant is cultivated, may
Fall-Ngai, 2011). play a role. In the following discussion, we character-
Considering the microbiome as an active compo- ize each of these “microbial compartments” and provide
nent of the host, being also responsive to changes in en- examples of studies addressing the functional roles of
vironmental (biotic and abiotic) conditions, is important these communities in plant health and development.
to a better understanding of the most important drivers
of the composition of plant microbiomes. In order to un- Plant selection for the rhizosphere microbial com-
derstand the factors that influence this assembly and the munities
dynamics from a phylogenetic and functional perspec- The rhizosphere is defined as the soil region under
tive, recent studies have targeted different fractions of the influence of the roots (Hiltner, 1904, as cited by Hart-
the plant microbiome separately. Partitioning the plant mann et al., 2008; Philippot et al., 2013). The microbial
microbiome considers three major compartments where community residing in this niche is structured differen-
microbial cells can establish and develop: the so-called tially from that found in the bulk soil, which is a differ-
rhizosphere, endosphere and phyllosphere (Hardoim et ence that is driven by two types of selection: the direct
al., 2008; Hirsch and Mauchline, 2012) (Figure 1). Al- effect of the presence of root exudates, leading to the
though the rhizosphere is still a soil portion, it presents high availability of nutrients; and the effect of increased
a community in part influenced by plant metabolism microbial biomass, which change the environmental
(Bulgarelli et al., 2013; Philippot et al., 2013), the endo- conditions in the rhizosphere.

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As regards the root exudates, the chemical com- mechanisms related to the in vitro inhibition of sugar-
ponents released in the vicinity of the plant roots are cane pathogen growth, the solubilization of phosphorus,
described as belonging to the major groups of carbo- and the production of indole-acetic acid (Luvizotto et al.,
hydrates, proteins, lipids, phenolic compounds, organic 2010). However, the combined activity of rhizosphere
acids and other cellular components (Nguyen, 2003; Di- members is more important to plant development than
ni-Andreote and Elsas, 2013). Among these molecules, the role of specific groups in the rhizosphere.
some are related to the activation of major fractions Plant protection against pathogens is one of the
of microbial communities (commonly metabolized by most important and least recognized features of the rhi-
most of soil organisms, e.g., glucose), but other com- zosphere microbial communities. The term ‘suppressive
pounds released are able to activate specific groups of rhizosphere’ refers to the microbial community that is
organisms (those related to signaling and chemotaxis, selected in the rhizosphere and is able to limit the devel-
e.g., flavonoids) (Nguyen, 2003; Jones et al., 2004). opment of pathogens, even in the presence of the host
These molecules represent the major source of carbon, plant. The inability of pathogens to survive is an effect
a nutrient available in abundance to plants through promoted by the biological fraction of the soil (Weller et
photosynthesis, that is commonly found in limited al., 2002), and the suppressiveness is related to a combi-
quantities in the soil environment (when comparing natory activity of several components of the rhizosphere
the forms available). (Mendes et al., 2011). Mendes et al. (2011) demonstrated
Based on the offering of specific carbon sources, that the stimulation of antibiotic-producing bacteria in
plants trigger a search for organisms that are able to com- the sugar beet rhizosphere is a major process respon-
plement the use of carbon sources released from their sible for the foundation of suppressive soils, exemplified
roots with other nutrients, which are obtained from a va- in an experiment where the suppressive soil inhibited
riety of metabolic processes found in microbial groups. the growth of the root pathogen Rhizoctonia solani. This
An example of this need for “metabolic complementa- ability to select beneficial organisms in the rhizosphere
tion” is the selection of nitrogen-fixing organisms in the is believed to be a common feature among plant species,
rhizosphere. As a highly competitive environment, the indicating that throughout their evolutionary history,
rhizosphere is a nitrogen-limited niche, that renders those plants have evolved to protect themselves by building
organisms that are able to capture gaseous nitrogen highly their own rhizosphere communities (Cook et al., 1995).
adapted to becoming established and thrive in this niche This inherent evolutionary capacity was crucial for the
(Raymond et al., 2004). The availability of nutrients in the establishment of the primitive plant in a terrestrial envi-
rhizosphere results in its colonization by a more abun- ronment, which has a still undeveloped (adapted to wa-
dant microbial community than that found in the bulk ter system) root structure (as revised by Mendes et al.,
soil (Philippot et al., 2013; Prashar et al., 2014). 2013 and Philippot et al., 2013).
Secondary selection in the rhizosphere is promot- Regarding the selection exerted in the rhizosphere,
ed by the presence of a higher abundance of microbial a question that needs to be robustly addressed remains
cells in this niche compared to the bulk soil. The in- concerning the selection of the taxonomical affiliation
crease in the number of cells per gram of soil leads to of rhizosphere organisms (see Box 1) or their ability
variation in local environmental conditions, thereby for to perform specific roles when closely associated with
example, promoting a decrease in oxygen availability as plant roots. Lundberg et al. (2012) targeted this issue and
it is rapidly consumed by the higher microbial biomass found that the rhizosphere composition varied for the
(Philippot et al., 2013). This scenario means that oth- same plant species, according to the available source of
er local parameters can also vary, for example, the pH microbes in each soil, possibly indicating that the func-
(commonly lower in the rhizosphere), the organic carbon tioning of the rhizosphere components drives the selec-
content (commonly higher in the rhizosphere), and the tion of the organisms. However, considering the possi-
activity of enzymes produced by microbial cells (Shi et bility of high rates of gene transfer in the rhizosphere
al., 2011). (check Box 1), it remains to be described how microbial
In summary, taking these effects together, plants cells that strive under the rhizosphere conditions easily
have evolved to allow the rhizosphere to attract specific acquire important function-related features.
microbes, which support plant development (Mendes et
al., 2011; Prashar et al., 2014). This concept is based on Endosphere – a niche for intimate friends
the fact that local conditions found in the rhizosphere The presence of microbial cells in the inner tis-
are interpreted as being optimum environments for the sues of plants was long interpreted as being synonymous
replication of organisms that present features related to with plant disease. At that time, the microorganisms
the promotion of plant growth, such as uptake of nu- found inside plant tissues were those able to infect the
trients from non-trivial sources (nitrogen fixation, phos- plant, leading to losses in plant yield and disturbance
phorus solubilization) or inhibition of pathogen growth of its development. Possibly, this connection was caused
(Mendes et al., 2011). As an example of these features, by the availability of methods for microbial detection,
one study isolated several Burkholderia spp. strains from which were only able to identify an abundance of or
the rhizosphere of sugarcane and observed efficient easy-to-cultivate microorganisms.

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The presence of other (non-pathogenic) organisms

Box 1 − DNA mobile elements enhancing the inside plants was first described by De Bary (1866), who
genetic drift of features related to plant-associ- observed that microbial cells are present in microscopi-
ated microorganisms cally analyzed plant tissues. This observation remained
unexplored until the definition of endophytes arose at
The traditional view of the link between the the end of the last century. The most common definition
taxonomic and functional affiliation of organisms of endophytes is based on the ability to detect the micro-
has long been used to target the components and bial cells from previously surface-sterilized plant tissues
functions of microbial communities in different (Halmann et al., 1997). However, this definition says,
environments. However, due to their cellular and in the main, that these organisms are not epiphytes. A
genomic organization, it seems that microbes (espe- working definition for endophytes was provided by Pe-
cially bacteria) are much more genotypically unsta- trini (1991), as “organisms that at some part of their life
ble than previously believed. The increasing num- cycle, colonize internal plant tissues without causing ap-
ber of complete and draft genome sequences [more parent harm to the host.” A more detailed analysis of
than 35,000 genomes as of May 2014 – GOLD data- endophytes has divided the endophytic communities
base (www.genomesonline.org)] is revealing unique into subgroups, named ‘obligate’ or ‘facultative’ by the
metabolic mechanisms and high genomic variabil- authors. Hardoim et al. (2008) classify as obligate those
ity even within the same “species.” This suggests endophytes that depend on plant metabolism for their
that microbial genomic information is a result of survival, being spread amongst plants by vertical trans-
complex interactions, occurring constantly through mission or by the activity of vectors. The facultative
evolution and also possibly imposed by the local endophytes are those living outside the host during a
environmental conditions, where they must strive certain stage of their life cycle, that are recruited by the
to survive and multiply (Philippot et al., 2010; Dini- plant from adjacent communities, such as the bulk soil,
Andreote et al., 2012). mainly through the rhizosphere.
Most systems described as hotspots for hori- Endophytes are described as being present in ev-
zontal gene transfer (HGT) are active zones of in- ery single plant because it is thought that no plant is
teractions between different organisms, including free from the presence of such organisms in their in-
both the donor and recipient cells. However, it might ner tissues (Rosenblueth and Martinez-Romero, 2006).
be true that the interaction between plants and mi- The presence of endophytes has even been described in
crobes can also lie in genome re-structuring, in a sys- plants maintained in vitro, where these organisms seems
tem where the host can impose local conditions that to be intimately associated with plants not in terms of
ultimately select those organisms more susceptible colonizing the culture medium but preferring to live in-
to genetic rearrangement and further acquisition of side the plant tissues (Almeida et al., 2009, Abreu-Taraz-
novel metabolic features. The “easy” occurrence of zi et al., 2010). However, several issues still remain to
rearrangements might be linked to the high com- be better addressed, concerning the roles of endophytes
plexity of microbial communities in the plant board- in plant development, and also in understanding the
ers (rhizosphere and phyllosphere), where the high mechanisms governing the transmission of such organ-
abundance of viruses, plasmids and other mobile isms between plants.
entities would supply a series of “new weapons” for Endophytes are likely to be involved in controlling
those microbes to interact with the host plant. plant pathogens and promoting plant growth. Mendes et
There is evidence that these interactive mech- al. (2007) have shown the ability of endophytic Burkhold-
anisms are present and active within the plant mi- eria spp. to control the growth of the pathogen Fusarium
crobiome, as well as in different niches in the soil. moniliforme. Ferrara et al. (2012) observed that the endo-
The first piece of evidence is the high occurrence of phytic diazotrophs from sugarcane roots are able to pro-
transmissible plasmids in the mycosphere (soil re- duce plant growth-promoting substances and to secrete
gion influenced by the fungal hyphae), which carry higher amounts of amino acids that might facilitate plant
genes that enable the recipient bacteria to colonize nutrition. Quecine et al. (2014) described the capacity of
the fungal-driven environment (Zhang et al., 2014). genetically engineered endophytes producing the heter-
It is likely that something similar is present in the ologous protein cry1Ac7 to control the sugarcane pest
rhizosphere that, furthermore, supplies microbial Diatraea saccharalis. However, although several individ-
resources for the host colonization, as evidenced in ual capacities are described in endophytes, it might be
the manuscript by Tauch et al. (2002) for the cryp- suggested that, acting as a community, these organisms
tic plasmid pIPO2. Possibly, these observations and are able to perform many other functions not detectable
future studies on this issue will identify the genes when each microbial group is studied separately. As an
(and their derivative organizations) as the units example, Araújo et al. (2002) indicated the interactions
where the selection occurs for the composition of occurring between the endophytic microbial community
plant-associated microbiomes. and the pathogen Xylella fastidiosa in citrus plants. Araú-
jo et al. (2002) claim that the entire endophytic com-

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munity is affected by the presence of the pathogen and protecting plants against invading pathogens and biosyn-
suggest that disease occurrence (in this case, citrus varie- thesizing phytohormones (Jones, 1970; Freiberg, 1998;
gated chlorosis) is a result of the interaction between the Brandl et al., 2001; Kishore et al., 2005). It makes them
pathogen X. fastidiosa and the endophytic community important pieces of global processes, such as carbon se-
and not only with the host plant. questration (Bulgarelli et al., 2013), and they can be used
The ecology of endophytes is a gap in our knowl- as potential sources for the development of sustainable
edge of plant-associated microbes. Several attempts have agricultural practices.
been made to track the origin of endophytic organisms The phyllosphere community is composed of
(Hallmann et al., 1997; Saikkonen et al., 1998; Mitter fungi (filamentous and yeasts), bacteria, algae, and, at
et al., 2013). Researchers commonly choose the rhizo- lower frequencies, protozoa and nematodes (Lindow
sphere (and consequently the soil) or the seed-born mi- and Brandl, 2003). The most abundant group amongst
crobial communities as the major sources. Their origin these is the bacterial community, presented in the phyl-
is strictly linked to the strategy of maintenance inside losphere at numbers between 105 and 107 cells per cm2
the plants, which determines the dissemination of en- (Beattie et al., 1995; Andrews and Harris, 2000). Phyllo-
dophytes between plants. One indicator of the way that sphere-living organisms are able to thrive and live under
specific endophytes interact with plants and evidence of particular and harsh environmental conditions, char-
their strategy of survival and transmission is provided acterized as an oligotrophic environment, where there
by their genome organization. are a limited availability of nutrients and variable con-
Dini-Andreote et al. (2012) reviewed several ge- ditions of humidity, UV radiation, pH and temperature
nome sizes and origins, including those of endophytes. (Andrews and Harris, 2000).
These authors correlated the genome size with the life- Another issue of this theme is the origin of the
style of bacteria, detecting the variation in environmen- microbial cells that make up the microbial communities
tal conditions as a major driver of genome expansion or in the phyllosphere. The location of such communities
shrinking. They suggested that bacteria living in stable is far from the soil (the main source of plant-associated
environments, such as endosymbionts, commonly have microbes) and is subjected to high rates of inoculation,
more compact genomes. On the other hand, bacteria liv- promoted in the main, by the activity of vectors and
ing in niches where environmental conditions are con- wind (Bullgarelli et al., 2013). Considering these pos-
stantly shifting, such as soils, would need to harbor a sibilities, together with the limiting and shifting condi-
more replete arsenal of genes to thrive under distinct tions that occur in the phyllosphere, some studies have
environmental conditions, leading to the prevalence of investigated the major sources of microbial communities
bigger genomes. At first glance, endophytes seem to fit in the phyllosphere. Bullgarelli et al. (2013) recently sug-
the first part of this hypothesis because they live inside gested that air and its aerosols, soil and water are the
plants, where the environment is more stable over time most important sources for microbial cells that make up
compared to the bulk soil. However, considering their the communities in the phyllosphere.
origin and transmissions systems, it is possible that some It is possible that the assemblage of microbial com-
endophytes must address distinct environments dur- munities in the phyllosphere is modulated by the interac-
ing part of the life cycle when they are not hosted by tion of distinct environmental factors. Variations in these
the plant. In fact, Mitter et al. (2013) observed a great conditions might promote the heterogeneity in abun-
variation in the size of genomes of bacterial endophytes. dance and structure of the phyllosphere microbial com-
These results suggest that the endophytic community is munities in distinct plant species. In tropical (Lambais et
made up of organisms from distinct origins, with those al., 2006) and temperate forests (Redford et al., 2010), the
with larger genomes likely to live in soils (variable en- plant genotype is a major driver of the composition of
vironment) and those with smaller genomes likely to be the bacterial communities in the phyllosphere. Redford
vertically transmitted (stable environment). et al. (2010) claim that distinct plant species harbor spe-
cific bacterial communities, mainly due to the generation
Microbial groups living in the phyllosphere of specific niches and local conditions, which are driven
A third component of the plant microbiome is by the genetic, and consequently, the functional metabo-
made of organisms colonizing the external area of aerial lism of the plant. The specificity of the phyllosphere com-
plant tissues, the phyllosphere. Although this term can munity was also observed in plants used in agriculture,
be used for any external surface of plants, it is common- with changes observed in the abundance and structure of
ly applied when describing the leaf surface (Vorholt, bacterial communities when comparing beans, cucumber,
2012). The phyllosphere is an enormous environment grasses, lettuce and maize (O’Brien et al., 1989; Kinkel et
on Earth that is estimated to reach an area of 6.4 × 108 al., 2000; Rastogi et al., 2012). Geographical distance is
km2 and is densely colonized by microorganisms (Morris also an important player in the structuring of bacterial
and Kinkel, 2002). communities in the phyllosphere (Bokulich et al., 2014).
The microbial communities found in the phyllo- These authors showed that grapevines harbor distinct
sphere have essential roles in processes related to plant bacterial communities, which could influence the final
development, for example, performing nitrogen fixation, quality of the wine produced.

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In a more detailed view, it is possible to observe which can also account for changes observed in plants
the occurrence of intra-specific variations in the compo- from distinct genotypes within the same species (i.e., va-
sition of the microbial community in the phyllosphere. rieties, cultivars). Based on that, the differential selec-
Such variations are driven, in the main, by the nutri- tion driven by plant genotype has been extensively used
tional heterogeneity observed in regions on the leaf sur- to track the safety issues for the cultivation of transgenic
face, where the carbon sources (e.g., glucose, fructose plants (Rasche et al., 2006; Cotta et al., 2013; Arpaia et
and sucrose) are spatially heterogeneous, leading to dis- al., 2014), with many studies indicating limited or low
tinct microbial assemblages on the leaf veins, which are effects of the exogenous genes on the plant-associated
regions near the stomata and surface appendages (Lin- communities. In contrast to these observations, differ-
dow and Brandl, 2003; Vorholt, 2012). In some cases, ences in the composition of microbial communities in
this heterogeneity is promoted by the organization of the rhizosphere of Arabidopsis thaliana are likely to be
microbial cells in biofilms, which are a common feature determined by soil type, rather than a unique selection
of organisms in the phyllosphere, acting as an aggregator by plant genotype (Lundberg et al., 2012). Along the
and protector of the microbial cells under the frequently same lines, Yergeau et al. (2014) demonstrated that soil
inhospitable conditions (Davey and O'Toole, 2000; Lin- contamination that leads to shifts in community com-
dow and Brandl, 2003). position ultimately influences the composition of as-
Despite these distinctions, it is possible to observe sembled communities in the rhizosphere of willows. In
a “core” for the phyllosphere bacterial community colo- the phyllosphere, which is a niche less subjected to the
nizing plants, which is composed of organisms belonging high density of organism inoculum from soil, the plant
to the phyla Proteobacteria, Actinobacteria, Bacteroide- genotype seems to exert a stronger selective influence, as
tes and Firmicutes (Redford et al., 2010; Vorholt, 2012). observed in specific microbial communities in the phyl-
It is worth noting that these phyla (Proteobacteria, Acti- losphere of plants living in mangroves (Dias et al., 2012;
nobacteria, Bacteroidetes and Firmicutes) are composed Rigonato et al., 2012).
of the most abundant and well-studied microorganisms, As regards the plant developmental stages, shifts
which indicates that further studies concerning this is- observed in plant-associated microbial communities are
sue should be designed to evaluate taxonomic ranks be- likely to be related to changes in plant metabolism dur-
low phylum. Hence, this core is believed to be composed ing the life cycle (Overbeek, L.; Elsas, J.D. 2008; Chap-
of members presenting a co-evolutionary history with arro et al., 2014). For instance, the developmental stage
plant species, with the host physiology being comple- of maize plants is a stronger driver of the bacterial com-
mentary to the features found within the microbial cells. munity composition in the rhizosphere than the soil type
It remains to be described how this microbial resource and plant genotype (Cotta et al., 2013). Andreote et al.
can be used for the development of agricultural prac- (2010) studied the roles of bacterial inoculation, plant
tices that promote the activity and singular or synergistic genotype and the developmental stage of the coloniza-
relationships that might stimulate plant growth and/or tion of plant roots (in both rhizosphere and endosphere)
protection against pathogen invasion. by bacterial communities and found the composition of
bacterial communities in potato to be mostly driven by
Drivers of plant-associated microbial communities the plant genotype (it differed according to the use of
Although the plant microbiome can be disentan- distinct varieties) and plant developmental stage (from
gled into groups of organisms to be studied separately, vegetative to senescent stages). Andreote et al. (2010)
these distinct groups of organisms respond in similar also observed that specific fractions of bacterial assem-
ways to the drivers underpinning their composition blages, such as the class Alphaproteobacteria and Paeni-
and functioning. Both biotic and abiotic factors impose bacillus communities, were influenced, in the main, by
strong selection on microbial community composition. the exogenous inoculation of bacterial components into
Special attention has been given to the plant genotype, its composition.
the phenological stage of the plant, and the use of spe- Moreover, agricultural practices are also often cor-
cific agricultural practices, which ultimately affect the related with changes in the structure of microbial com-
soil physicochemical characteristics. munities associated with plants. That influence occurs
The plant genotype influences the composition of based on physical and chemical changes promoted in
microbial communities associated with plants through the soil matrix, ultimately influencing the way by which
specific metabolic processes (Garbeva et al., 2008; plants exert the selection of their microbiome. In sugar-
Philippot et al., 2013). A comparative analysis between cane (Saccharum officinarum), soil chemical fertilization
the endophytic microbial communities of Atriplex cane- alters the composition of bacterial communities in culti-
scens and A. torreyi, two halophilic plants used as for- vated fields (Wallis et al., 2010). The adoption of distinct
age in North America, revealed the presence of distinct agricultural practices was also related to these shifts,
communities between the two species, mostly differing where the sugarcane harvesting strategy (burning-based
in the prevalence of diazotrophic bacteria (Lucero et al., vs mechanical) seems to determine the microbial com-
2011). That finding was directly related to the metabolic munities that are selected in soils. Rachid et al. (2013)
differences observed between the two plant genotypes, correlated the differential selection due to the presence

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Andreote et al. Plant-associated microbial communities

(or not) of plant residues in the soil, which drastically gest that such stimulation of gene transfer could drive,
modulate the degradation of organic matter and other at least partially, the functional redundancy of soil mi-
chemical characteristics of the living soil. crobiome.
In addition to these major drivers, many other
environmental conditions can change the composition Studies based on plant microbiomes
of plant-associated microbial communities. One of the Although plant microbiomes are a broadly stud-
most promising issues in this field is the mechanism ied topic, a holistic view of the microbial groups as-
involved in the interaction of the plant microbiome sociated with the entire plant is a recent perspective
with pathogens. The presence of pathogens can alter and still an active area of research. The importance
the composition of microbial communities in the rhi- of this subject is evidenced by the growing number of
zosphere (Mendes et al., 2011) and in the endosphere scientific publications on this topic in recent years, as
(Araújo et al., 2002). Future studies on these topics can well as research focusing on specific niches of plants
lead to information of essential components of plant and how they modulate their specific microbial com-
microbiomes or specific stimuli for beneficial groups munities (Table 1, Figure 2). However, as observed for
that are able to suppress the development of pathogens specific microbial assemblages, it is likely that plant
in plants. microbiomes vary according to plant species and en-
Many researchers have confirmed shifts in micro- vironmental conditions. In this sense, key questions
bial communities as being attributable to changes in en- about how plants acquire their microbiomes, whether
vironmental conditions. However, an open issue is the certain microorganisms are passed down generation to
validation of these inferences made in the taxonomical generation or are recruited from the environment, and
aspects of plant-associated microbes. The evaluation of the possible composition of the minimal microbiome
changes in the structure of microbial communities is one remain to be answered.
level where variations might happen. Another issue to Despite the clear importance of microorganisms in
consider is related to the specific response of each mi- soil nutrient cycling and promotion of plant growth, we
crobial group in the face of distinct environmental con- still need more comprehensive studies on the interac-
ditions. These responses are related to possible changes tions between microbial communities that make up the
in microbial fitness, metabolic response, and even re- microbiomes of plants. Such an effort would allow for
arrangements at the genomic level. The last possibility a better understanding of the effects of different envi-
most likely constitutes the next barrier to understanding ronmental conditions and agricultural practices on the
how microbes respond to shifting environmental condi- proper functioning of plant microbiomes.
tions. This statement is in line with the description of Most studies are still to some extent very descrip-
the microbiome by Boon et al. (2014), who considered tive or even link the response of the microbiome to
a set of genes and not a set of organisms to be the best shifts in environmental conditions (Table 1). For ex-
microbiome concept given that these genes might drift ample, Pinto et al. (2014) reported the microbiome of
between distinct members of the taxonomical compo- grape in a vineyard landscape through a culture-inde-
nents of the microbiome (Box 1). It is reasonable to sug- pendent approach, indicating the occurrence of highly

Figure 2 − Numbers of scientific publications on the topics of “plant microbiome,” “rhizosphere,” “endosphere” and “phyllosphere” in the last 20
years. The small panel (upper-left) represents the number of appearances of each term. Searches were performed in the Scopus database
on May 23, 2014.

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Andreote et al. Plant-associated microbial communities

Table 1 – Short description of selected papers that represent important advances in the field of plant microbiomes.
Plant Main findings Reference
Sugar beet (Beta vulgaris L.) Microbiome-driven protection of plant against attack by a root fungal pathogen. Mendes et al. (2011)
Influence of the soil on bacterial community assembly in the rhizosphere and
Arabidopsis thaliana Lundberg et al. (2012)
phyllosphere compartments.
Arabidopsis thaliana Correlation between microbial genes and metabolites released by plant roots. Chaparro et al. (2013)
Microbiome selection exerted by plant-roots; enhancing plant photosynthetic activity
Pepper (Capsicum annuum L.) Marasco et al. (2012)
and biomass synthesis under drought stress.
Koopman and Carstens
Sarracenia alata Composition of plant microbiome similar to the gut microbiome of soil microfauna.
(2011)
Correlation between the abundance of Massilia and the effects of plant phenological
Cucumber (Cucumis sativus) Ofek et al. (2011)
stage on the root microbiome.
Balsam Poplar (Populus balsamifera) Differences in fungal microbiomes promoted by the poplar genotype. Bálint et al., 2013
Zygophyllum dumosum and Atriplex halimus Essential role of microbiomes for plant life in the desert. Kaplan et al. (2013)
Wheat (Triticum aestivum), oat (Avena
Distinct rhizosphere microbiomes even at high taxonomic rank. Turner et al. (2013b)
sativa) and pea (Pisum sativum)
Grapevine (Vitis vinifera L.) Dynamic response of plant microbiome to agrochemical applications. Pinto et al. (2014)

dynamic communities during the plant lifecycle, which Importantly, by combining these topics in an integrative
was also significantly responsible for the application of way, substantial understanding is gained for the explora-
agrochemicals. Amongst these studies, a number are tion and preservation of natural areas.
already investigating the roles of the associated micro- Considering the topic of the microbiome in the
biomes in plant physiology as when describing the mi- actual Brazilian research scenario, a recent initiative
crobiome associated with plants living in deserts, where aims to organize microbiome-derived data across differ-
the microbial communities are essential to the resistance ent Brazilian biomes. The Brazilian Microbiome Project
of the plant to the unhospitable environment (Kaplan et (BMP) (http://www.brmicrobiome.org/) is a group-based
al., 2013). Marasco et al. (2012) also described the micro- effort focused on standardizing the assessment of micro-
biome as an essential component of plant resistance to biomes in Brazilian resources (Pylro et al., 2014). In its
drought stresses. A more intimate interaction was shown first publication, the BMP listed the microbiome-based
in the study of Chaparro et al. (2013), where the micro- studies under development in Brazil, highlighting the
biome was responsible for the composition of exudates importance of soil microbiomes (in natural and agricul-
released by the plant roots. These examples raise the tural areas) and plant microbiomes, such as those found
possibility that the selection exerted in the rhizosphere in leguminous plants, sugarcane, and plants inhabiting
can be driven not only by the plant but, more precisely, natural areas, such as the Cereus jamacaru, in the Brazil-
by an integrated evolutionary mechanism governed by ian caatinga (Pylro et al., 2014).
the nature of the interaction between the host and the The results generated and organized by the BMP
associated microbiome. initiative are aimed to be further integrated into a major
consortium, named the Earth Microbiome Project (EMP)
State of the art in Brazil (http://www.earthmicrobiome.org/). This effort will give
Several Brazilian research groups are accomplished the Brazilian microbiomes the opportunity for wider ex-
in the study of plant-associated microbial communities, posure for comparative analyses and determination of
contributing to an important part of the recent litera- particularities in our claimed mega-biodiverse landscape.
ture on the topic (Figure 3). The Brazilian contribution to
plant-microbiome research accounts for 4 % of scientific Future perspectives
publications on the topic of the plant endosphere. On Although there is increasing information in the
the topic of the plant microbiome, Brazilian groups ac- literature about host microbiomes, the vast majority is
count for 3 % of the publications available in the field. related to the microbial groups in and the human body.
Lower percentages that are still significant in absolute The description of the microbiome composition of plants
numbers are attributed to studies on the rhizosphere and and their putative roles are ongoing themes in research.
the phyllosphere, with 2 % and 1 % of the literature fo- Several factors will certainly contribute to the ex-
cusing on these issues, respectively (Figure 3). pansion of this approach in the upcoming years. The
In a more detailed view, there is extensive lit- increasing quality of sampling strategies, DNA extrac-
erature generated by Brazilian groups on the topics of tions, amplifications of target genes from diverse com-
community ecology, microbial community structure and munities, amongst others, represent methodological
diversity, environmental functioning, and plant-associat- biases that will certainly diminish over the coming
ed communities and their implications for agriculture. years. Also, the wider access of sequence-based analyses

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Andreote et al. Plant-associated microbial communities

Figure 3 − Distribution of the scientific literature across the most important countries involved in research on plant microbiomes (presenting
those with > 1 % of the production on each topic). Data were collected based on the last 20 years of research (i.e., 1994–2013), according
to the information available in the Scopus database on May 23, 2014.

allowed by recent advances in DNA sequencing tech- ganismal level to unveil the ecological strategies used by
niques is making possible the sequencing of nucleic ac- microorganisms to survive and thrive in the plant mi-
ids (DNA or RNA) from great numbers of samples. The crobiomes. In addition, by combining large amounts of
recent decrease in sequencing costs and the generation information provided by genomic and other sequence-
of enormous amounts of data (essential to a characteriza- based studies with new strategies to increase our abil-
tion of complex microbial communities) have supported ity to cultivate and study microbes in the laboratory, we
the emergence of studies on the microbiome, which is will attain a more detailed understanding of the behav-
also very dependent on the development of bioinfor- ior and functioning of microbiomes in nature.
matics and mathematical modeling. Such technological If plant microbiomes are better described and un-
advances have also provided a more robust description derstood, such information will be available for the de-
of microbial phylogenetic and taxonomic community velopment of new technologies, especially those that will
composition, thereby increasing the information avail- focus on a better exploration of the features triggered
able in public databases. These developments constitute by microbial cells in agricultural fields. More precisely,
a breakthrough in our ability to make ecological and it might be possible to alter the microbial community
functional inferences on microbes in nature (see Box 1). structure, for instance, by inoculation of specific exog-
These achievements will surely be complemented by enous organisms or by controlling environmental condi-
approaches based on more traditional microbiology, as tions so as to benefit specific sets of these microbiomes,
recently shown by Dini-Andreote and Elsas (2013), who leading to an increase in plant resistance or harnessing
indicated the need for ecophysiological insights at an or- of efficiency in the uptake of specific nutrients. In this

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Andreote et al. Plant-associated microbial communities

way, the development of so-called “microbiome-driven M.G.I.; Beiko, R.G. 2014. Interactions in the microbiome:
cropping systems” might result in the next revolution in communities of organisms and communities of genes. FEMS
agriculture, resulting in a more sustainable system for Microbiology Reviews 38: 90-118.
plant production. Bosch, T.C.; McFall-Ngai, M.J. 2011. Metaorganisms as the new
frontier. Zoology Review 114: 185-90.
Acknowledgments Brandl, M.T.; Quinones, B.; Lindow, S.E. 2001. Heterogeneous
transcription of an indoleacetic acid biosynthetic gene in
The authors would like to acknowledge Francisco Erwinia herbicola on plant surfaces. Proceedings of the National
Dini-Andreote for the critical and grammatical revision Academy of Science of the USA 98: 3454-3459.
of this manuscript and FAPESP (São Paulo Research Bulgarelli, D.; Spaepen, S.S.; Themaat, E.V.L.; Shulze-Lefert, P.
Foundation) for the financial support of the studies per- 2013. Structure and functions of the bacterial microbiota of
formed by the group and the grants of students (pro- plants. Annual Reviews in Plant Biology 64: 807-838.
cesses 2011/07343-5 and 2013/18529-8 for A.D and T.G., Chagnon, P.L.; Bradley, R.L.; Maherali, H.; Klironomos, J.N.
respectively). CNPq (The National Council for Scientific 2013. A trait-based framework to understand life history of
and Technological Development) is acknowledged for mycorrhizal fungi. Trends in Plant Science 18: 484-491.
the grant to F.D. Andreote (process 3030034/2011-4). Chaparro, J.M.; Badri, D.V.; Bakker, M.G.; Sugiyama, A.; Manter,
D.K.; Vivanco, J.M. 2013. Root exudation of phytochemicals in
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