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The role of the phyllosphere microbiome in plant health and function
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Annual Plant Reviews (2018) 1, 1–24 http://onlinelibrary.wiley.com
doi: 10.1002/9781119312994.apr0614
THE ROLE OF THE

PHYLLOSPHERE MICROBIOME
IN PLANT HEALTH AND
FUNCTION
Bram W. G. Stone, Eric A. Weingarten and
Colin R. Jackson
Department of Biology, University of Mississippi, University, MS, USA
Abstract: The above-ground surfaces of plants (the phyllosphere) harbour a

diverse variety of microorganisms, and this phyllosphere microbiome interacts
with the host plant affecting its health and function. Phyllosphere microorganisms,
predominantly bacteria and fungi, can act as mutualists promoting plant growth
and tolerance of environmental stressors, commensals using the leaf habitat for
their own growth and reproduction, or as antagonistic pathogens. Although
much of the literature has focused on plant–pathogen interactions and disease
mechanisms, we expand this discussion to the structural and functional dynamics
of the whole phyllosphere community, rather than single-species populations.
We highlight the particular challenges posed to microorganisms living on the
leaf surface, describe the structure of the phyllosphere microbiome, and discuss
how these microbial constituents interact with the plant with respect to stress
tolerance, growth promotion, nutrient acquisition, and disease resistance. Lastly,
we pose new directions for the field made possible by advances in sequencing
and computational technologies.
Keywords: bacteria, endophytes, leaf, microbial community, microbiome, phyl-

losphere, plant-associated bacteria
1 Introduction
The fact that macroorganisms harbour diverse communities of microorgan-

isms (their microbiome) is one of the emerging principles in biology, and we
are beginning to understand the role that the microbiome plays in the host
Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

© 2018 John Wiley & Sons, Ltd. Published 2018 by John Wiley & Sons, Ltd.
1
BWG Stone, EA Weingarten & CR Jackson
organism’s health and function (Turnbaugh et al., 2007; Blaser, 2014; Colston
and Jackson, 2016). The microbiomes of animals have been found to influence
host development, immunity, nutrition, and even behaviour (Kau et al., 2011;
Blaser, 2014; Thaiss et al., 2016); and this has led to calls for increased efforts to
understand the roles of microbiomes of other environments, including soils,
waters, and plants (Alivisatos et al., 2015; Dubilier et al., 2015).
Microorganisms have long been recognised as being associated with
plants, and early research focused on interactions between agricultural
plants and microorganisms in the soil or rhizosphere (Sapp, 2004). This
research was expanded to include above-ground interactions with studies
of microorganisms on the leaf surface or phyllosphere (Last, 1955; Ruinen,
1956). These studies focused on agricultural pathogens, and this remained
the main focus of phyllosphere studies for years (Sapp, 2004). Pathogens
inhabiting the phyllosphere can have dramatic, often systemic, effects on
plant health, and can spread more rapidly than soil-borne diseases (Hirano
and Upper, 1991; Pedgley, 1991). Consequently, much subsequent effort
was directed at understanding the dispersal and establishment of microbial
pathogens. However, the diversity of non-pathogenic microorganisms on
leaves may play a protective role against plant disease (Balint-Kurti et al.,
2010), and understanding the ecology of the overall microbiome is an impor-
tant component of phyllosphere research (Meyer and Leveau, 2012). The
factors that influence the development of this community, and the roles that
this community may play in plant health and function are now beginning to
be understood.
2 The Leaf Surface as a Habitat for Microbial Growth
Environmental conditions at the leaf surface exert a tremendous influence

on microbial populations in the phyllosphere, which in turn determines the
interactions that can occur between the plant and its microbiome. Growth
on the leaf surface is frequently limited by both water and nutrients, as
well as exposure to high levels of ultraviolet (UV) radiation (Vorholt, 2012).
Variation in the physical and chemical landscape of the leaf itself (Neinhuis
and Barthlott, 1997; Reisberg et al., 2013) and patchiness of nutrients on the
leaf surface impose additional constraints for colonising microorganisms
(Remus-Emsermann et al., 2012). Leaf topography changes as the leaf ages,
so that plant–microbial interactions are dependent on time as well as the
specific characteristics of the host plant (Kinkel, 1997). Most leaf-associated
microorganisms occur in areas that are somewhat protected from abiotic
stresses and in areas that foster closer interactions with the host plant.
Denser populations of bacteria are found in the grooves between plant
cells, at the base of trichomes, and near leaf veins and stomatal openings

2
The role of the Phyllosphere Microbiome in Plant Health and Function
(Kinkel, 1997; Baldatto and Olivares, 2008). Even within a plant species,
leaf traits can vary between cultivars (Jenks et al., 1995; Hunter et al., 2010)
and even between leaves on the same plant (Beattie, 2002; Cordier et al.,
2012), further complicating how the surface interacts with phyllosphere
microorganisms.
Moisture availability is a key limitation to microbial growth on the leaf sur-
face (Beattie, 2002). The cuticle prevents moisture from leaving the inside of
the leaf and limits how much water remains on the leaf surface (Holloway,
1970; Rentschler, 1971; Neinhuis and Barthlott, 1997). To overcome this chal-
lenge, bacteria may form aggregates and biofilms, producing extracellular
polymeric substances (EPS), which can resist desiccation (Wilson and Lin-
dow, 1994a; Ophir and Gutnick, 1994; Morris et al., 2002). Other bacteria pro-
duce surfactants to increase the wettability of the leaf and lessen the ability of
the cuticle to limit water accumulation (Knoll and Schreiber, 2000; Schreiber
et al., 2005). In addition to these strategies, the leaf surface has a boundary
layer with a microclimate that typically has higher humidity than the broader
phyllosphere, and this likely mitigates some of the desiccation pressure for
microbiota that are in that layer (Burrage, 1971). Microbial populations typ-
ically increase following precipitation (Last, 1955; Hirano et al., 1996), when
there can be substantial changes in the diversity and composition of the phyl-
losphere microbiome (Jackson et al., 2006; Copeland et al., 2015). The effect
of moisture from dew on the leaf community has not been explored, but it is
assumed to act similarly to rain (Lindow, 2006).
Although phyllosphere microorganisms have evolved strategies to mit-
igate potential moisture limitation, the nutrient-poor nature of the leaf
surface means that growth of these microorganisms is still limited by avail-
able nutrients, primarily carbon and nitrogen (Wilson and Lindow, 1994;
Mercier and Lindow, 2000). Microorganisms on the leaf surface are generally
oligotrophs that can tolerate low-nutrient conditions or are microorganisms
that can interact with the host plant to obtain more nutrients (Beattie
and Lindow, 1999). Although cuticular waxes are generally resistant to
chemical movement, some plant metabolites can move to the leaf surface,
supporting microbial growth (Tukey, 1966; Mercier and Lindow, 2000).
These compounds may arrive on the leaf surface by excretion from leaf cells,
or due to osmotic pressure when the leaf is wet (Tukey, 1970). Plants also
release volatile organic compounds, which support specific populations
of microorganisms; for example, methylotrophic bacteria that metabolise
plant-derived single-carbon compounds are abundant constituents of the
phyllosphere of many plant species (Omer et al., 2004; Delmotte et al., 2009).
Phyllosphere microorganisms may obtain nitrogen by way of plant-
produced amino acids, which leach to the leaf surface or by inorganic forms
of nitrogen that leach from the apoplast (Tejera et al., 2006). Nitrogen arrives
on the leaf surface through atmospheric deposition. Ammonia is typically
assimilated by the leaf microbiota, although chemoautotrophic ammonia

3
oxidizers can also be present in the phyllosphere (Bowatte et al., 2015;

Watanabe et al., 2016). Oxidised nitrogen species (nitrate and nitrite) are
water soluble, and their availability changes during rain events (Papen et al.,
2002; Guerrieri et al., 2015). Bacterial nitrogen fixation can occur on the leaf
surface, likely in pockets of moisture because of the anaerobic constraints of
the fixation process (Ruinen, 1965; Jones, 1970; Holland, 2011).
Exposure to UV radiation poses a particular challenge to leaf epiphytes,
and bacterial and fungal populations that have been isolated from the
phyllosphere are typically more pigmented than those from soil (Stout, 1960;
Sundin, 2002). This pigmentation can increase survival in the phyllosphere
environment (Sundin and Jacobs, 1999; Jacobs et al., 2005). Phyllosphere
microorganisms can also express enzymes to handle reactive oxygen species
generated from solar radiation, as well as produce DNA protection proteins
(Delmotte et al., 2009). Rapid expression of DNA repair mechanisms fol-
lowing UV exposure may be a crucial determinant of phyllosphere survival
(Sundin, 2002). However, most of the information on the influence of UV
radiation comes from studies at the organismal or population level, and little
is known of the effects of UV radiation on the collective microbial community.
UV radiation has been shown to increase phyllosphere bacterial diversity
(Kadivar and Stapleton, 2003) but also to cause no change (Truchado et al.,
2017). Because the influence of solar radiation occurs on a diurnal cycle,
day length can also relate to the growth and abundance of certain microor-
ganisms (Sundin and Jacobs, 1999). Thus, growth of microorganisms on
the leaf surface may be affected by day lengths that change on a seasonal
level; however, no investigations have sufficiently disentangled such effects
from other variables that also follow seasonal trends (i.e., temperature and
relative humidity). In addition, because most phyllosphere studies focus
on agricultural systems, many studies are concluded at the time of harvest
or at the end of the growing season – before seasonal trends may become
pronounced.
3 The Nature and Composition of the Phyllosphere

Microbiome
Phyllosphere microbiota represent a diverse array of microorganisms, but

they are typically dominated by bacteria. Phyllosphere bacterial assemblages
are generally less species rich than the rhizosphere or soil (Knief et al., 2012).
Alphaproteobacteria are particularly well represented on the leaf surface,
and these bacteria play many ecological roles (Ruinen, 1965; Innerebner
et al., 2011). Gammaproteobacteria have also commonly been reported
in surveys of phyllosphere bacterial community composition (Redford
et al., 2010; Vorholt, 2012). Proteobacteria are metabolically diverse, and the

4
phyllosphere bacteria that carry out methyltrophy, nitrification, nitrogen

fixation, or anoxygenic photosynthesis are typically representatives of this
phylum (Corpe and Rheem, 1989; Fürnkranz et al., 2008; Atamna-Ismaeel
et al., 2012a; Watanabe et al., 2016). Bacteroidetes and Actinobacteria are
generally the next most dominant bacterial lineages in phyllosphere commu-
nities, and both of these phyla are also well represented in the rhizosphere
(Lauber et al., 2009; Philippot et al., 2013). Bacteroidetes in the phyllosphere
tend to be from families such as the Cytophagaceae or Chitinophagaceae
(Vorholt, 2012; Stone and Jackson, 2016). These organisms are often aerobic
and pigmented (Yasuyoshi, 2011; Krieg et al., 2011), suggesting that they
are well adapted to the leaf surface. The phylum Actinobacteria includes
members that are plant pathogens, nitrogen-fixing symbionts, and fungal
antagonists, as well as decomposers (Qin et al., 2011; Palaniyandi et al.,
2013). Many of these roles have not been explored in the phyllosphere
environment, but the Actinobacteria Corynebacterium has been used as a
foliar-applied plant growth promoter (Giri and Pati, 2004). Less is known
about the presence and distribution of archaea in the phyllosphere as they
appear to constitute a minor portion of the microbial community (Delmotte
et al., 2009; Knief et al., 2012; Vorholt, 2012).
Fungi are an important component of the phyllosphere microbiota, an
aspect that has been recognised for years because of pathogenic fungal
species (Keen, 2000). The fungal community is composed of organisms
with a wide variety of ecological roles whose population sizes fluctuate in
distinct seasonal trends based on the growing season and, ultimately, leaf
senescence (Kinkel, 1991). Moulds belonging to the Ascomycota are often
the dominant fungi on the leaf surface before senescence (Thompson et al.,
1993; Abdelfattah et al., 2015). Other important fungi are yeasts belonging to
the Ascomycota and Basidiomycota (Last, 1955; Dickinson, 1976). Following
leaf senescence, the fungal microbiome becomes dominated by filamentous
fungi (Voříšková and Baldrian, 2013). The distribution and role of other
microbial eukaryotes (protists) on plant leaves have not been well examined,
but as with other systems, these organisms largely act as predators on the
bacterial community (Bamforth, 1973; Flues et al., 2017).
Next-generation sequencing of community metagenomes has shown
highly redundant functionality throughout phyllosphere microorganisms,
suggesting that environmental conditions (low nutrients, high UV, changing
temperature, and humidity) select for consistent biological traits, and
low functional diversity at the community level (Delmotte et al., 2009;
Lambais et al., 2017). Generally, the phyllosphere is dominated by aerobic
organoheterotrophs, and metabolic diversity exists primarily in the context
of utilisable carbon compounds. Interestingly, proteorhodopsin genes related
to anoxygenic photosynthesis were found to be taxonomically widespread
in the tamarisk salt cedar (Tamarix nilotica) phyllosphere (Atamna-Ismaeel
et al., 2012a,b). Proteorhodopsins are light-activated proton pumps that have

5
been implicated as starvation prevention mechanisms in oligotrophic marine

environments (Akram et al., 2013). Such adaptations seem particularly
useful in the phyllosphere, although more studies are needed to address this
phenomenon.
Plant species identity appears to be the predominant factor influencing
the composition of the phyllosphere microbial community, although there is
substantial variability in microbiome composition even within a single plant
species (Hunter et al., 2010; Redford et al., 2010; Laforest-Lapointe et al.,
2016). Temporal variation in phyllosphere composition likely represents
a combination of leaf age and succession, coupled with environmental
variation (Kinkel, 1997), and changes in the microbial composition of the
atmosphere (Pedgley, 1991). This variation can be dramatic, and phyllo-
sphere communities differ significantly on seasonal time scales, even on
evergreen plants that might be expected to show less influence of leaf age
(Jackson and Denney, 2011). Spatial differences in the phyllosphere of indi-
vidual plant species are less well studied, and the extent to which dispersal
limitation or environmental gradients drive phyllosphere composition is
unclear (Redford et al., 2010; Finkel et al., 2012; Stone and Jackson, 2016).
4 Interactions Between the Leaf Microbiome and the Plant

Host
4.1 The Role of Phyllosphere Microorganisms in Plant Nutrient

Acquisition
In contrast to the recognised importance of rhizosphere microorganisms to
plant nutrient acquisition, the phyllosphere microbiome has generally been
viewed as being relatively inert, with little role in providing nutrients to
the host plant. The presence of nitrogen-fixing bacteria has been reported
in surveys of phyllosphere community composition (Ruinen, 1965; Jones,
1970; Sattelmacher et al., 1998; Delmotte et al., 2009; Holland, 2011), but
mechanistic studies of plant-phyllosphere nitrogen dynamics are generally
lacking. In temperate environments, nitrogen fixation typically occurs in the
interior tissue of the leaf rather than on the leaf surface (Sattelmacher et al.,
1998), presumably allowing nitrogenous end products to diffuse freely into
plant cells. In tropical environments, however, nitrogen fixation occurs in the
phyllosphere, potentially because higher moisture availability at the leaf sur-
face allow nitrogen-fixing bacteria to be active (Fürnkranz et al., 2008). The
transfer of nitrogenous compounds from nitrogen-fixing microorganisms in
the phyllosphere to the host plant has been observed (Bentley and Carpenter,
1984), although most studies report indirect evidence for phyllosphere
nitrogen fixation, and the mechanisms for microbe–host nitrogen transfer are
unclear. Tropical epiphytes in the canopies of higher plants show nitrogen

6
fixation in their phyllosphere, and this likely provides a substantial amount

of their nitrogen requirements. These plants have been found to retain the
majority of the microbially fixed nitrogen that they obtain, passing little to
the larger host plant whose canopy they inhabit (Hietz et al., 2002).
Application of nitrogen-fixing microorganisms to leaves can promote plant
growth and increase the nitrogen content of plants (Giri and Pati, 2004). How-
ever, this could represent internalisation of those applied bacteria, rather than
actual phyllosphere nitrogen fixation. Such experimental studies on foliar
applications demonstrate the potential for leaf uptake of nitrogen, as foliar
application of chemical fertilizers increases the nutrient content and yield of
plants (Yildrim et al., 2007; Scagel et al., 2008). Thus, while direct mechanistic
demonstrations of the importance of nitrogen-fixing phyllosphere microor-
ganisms to plant health are lacking, there is certainly the potential for this to
be an important source of nutrients to the plant.
Interestingly, in areas subject to pollution from elevated levels of nitrogen,
phyllosphere microorganisms may play a protective role by oxidising ammo-
nia to nitrate through nitrification (Papen et al., 2002; Krupa, 2003; Guerri-
eri et al., 2015). Chemoautotrophic nitrifiers, especially archaea, have been
identified in the phyllosphere of various plant species (Bowatte et al., 2015;
Watanabe et al., 2016), so the ability of the phyllosphere to mitigate effects
of ammonia pollution may be widespread but not necessarily driven by bac-
teria. Interactions between phyllosphere microbiota and the plants’ nutrient
acquisition may also occur indirectly. For example, foliar application of fer-
tiliser can result in increased bacterial growth and production of cytokinins
that can be bioactive within the plant (Holland, 2011). These can influence
overall plant metabolism, including belowground nutrient acquisition strate-
gies. In such cases, the phyllosphere microbiome may influence the ability of
the overall plant, rather than just the foliage, to acquire nutrients.
4.2 The Inﬂuence of the Phyllosphere Microbiome on Host Stress

Tolerance
Plant growth-promoting (PGPR) bacteria are those that promote a robust
plant stress response and stimulate growth. Root-associated microorganisms
can confer increased drought resistance to the overlying plant (Sandhya
et al., 2009; Ortiz et al., 2015). The rhizosphere microbiome also plays a role
in resistance to temperature extremes (McLellan et al., 2007; Selvakumar
et al., 2008; Grover et al., 2011; Meena et al., 2015). Fewer studies have
examined how phyllosphere microorganisms alter the plants’ ability to
tolerate environmental stressors, with more known about the impacts of
such stressors as drought and temperature extremes on the phyllosphere
microbiota alone. It is possible that bacterial EPS could provide some
protection to the plant itself, both from desiccation and from damaging UV
radiation. Laboratory studies of aquatic Pseudomonas aeruginosa biofilms have

7
shown the gel-like EPS matrix to resist the diffusion of water, oxygen, and
nutrients (Costerton et al., 1994). Biofilms in the phyllosphere may be even
resistant to desiccation than those found in water. For example, Pseudomonas
putida biofilms grown in air retained their morphology better after drying
than biofilms grown in liquid medium (Auerbach et al., 2000). Pseudomonas
spp. are often dominant constituents of the phyllosphere suggesting that
naturally occurring biofilms may limit the loss of water and exposure to
UV radiation. Plants are necessarily exposed to high levels of UV radiation
and can suffer developmental and genetic damage (Jansen et al., 1998).
Pigmented bacteria are more UV resistant, and the phyllosphere microbiome
as a whole becomes more UV tolerant towards the end of the growing season
(Jacobs and Sundin, 2001). It is possible that phyllosphere microorganisms
may provide some UV protection to the plant host through EPS production
and UV-absorbing pigmentation, but neither of these mechanisms has been
investigated experimentally.
Phyllosphere bacteria might also provide desiccation tolerance through
other mechanisms, although these have been explored more thoroughly
for microorganisms in the rhizosphere. PGPR rhizobacteria confer drought
resistance through hormonal growth stimulation (Glick et al., 2007), pro-
duction of EPS that adheres soil to roots (Sandhya et al., 2009), or increased
salt tolerance (Chakraborty et al., 2013). Wheat cultivars primed with
PGPR bacteria show better survival and greater dry weight under drought
conditions than unprimed plants, likely through bacterial stimulation of root
growth, and the same mechanism might also increase the plants’ tolerance to
salinity (Kasim et al., 2013). Whether some of the benefits of PGPR bacteria
that are typically associated with the rhizosphere can also occur when
those bacteria are present in the phyllosphere has not been explored. Arid
conditions generally result in increased C:N in leaves, suggesting that one of
the secondary effects of drought is nitrogen limitation. Drought can increase
the richness and diversity of nitrogen-fixing members of the phyllosphere
(Rico et al., 2014), suggesting a potential role of the phyllosphere microbiome
in reducing nitrogen limitation triggered by drought.
Along with drought tolerance, the plant microbiome may play a role in
heat tolerance. Wheat plants containing fungal endophytes show better yield
and seed germination success when stressed by heat than non-inoculated
plants (Hubbard et al., 2014). The mechanisms by which this heat tolerance
is conferred has been hypothesised to be the dissipation of heat by the fungi
cell walls, or the triggering of a generalised host stress response that helps
with thermal tolerance (Redman et al., 2002). Heat shock proteins associated
with temperature responses are found across plants, bacteria, and fungi
(Queitsch et al., 2000) and have such functional conservation that yeast genes
can be replaced by those from Arabidopsis and the yeast retains heat tolerance
(Schirmer et al., 1994). This gene-level homology and interaction are a likely
avenue for future explorations of plant–microbial interactions, particularly

8
if increased thermal resistance can be promoted by bacteria on the surface of

plants as well as those within plant tissues.
A well-documented role of phyllosphere bacteria is in frost formation
(Lindow et al., 1982a,b; Wisniewski et al., 1997; Attard et al., 2012). Several
species of phyllosphere bacteria such as Pantoea agglomerans and Pseudomonas
syringae possess cell surface protein complexes that can raise the temperature
at which ice crystals form (Lindow et al., 1982a,b; Attard et al., 2012). This ice
nucleation activity (INA) is generated by bacterial cell wall proteins, which
have a structure resembling that of an ice crystal. When supercooled water
droplets contact these proteins, they can spontaneously freeze (Zachariassen
and Kristiansen, 2000), and plants treated with P. syringae or P. agglomerans
become coated with frost up to 8 ∘ C warmer than untreated plants (Lindow
et al., 1982a). INA bacteria benefit from ice damage to the plant that allows
nutrients to become more accessible (Zachariassen and Kristiansen, 2000;
Pearce, 2001).
However, INA-induced frost damage does not always occur, likely because
of two other mechanisms that can occur in the phyllosphere microbiome.
First, other species of bacteria produce thermal hysteresis (antifreeze) pro-
teins that have an antagonistic effect relative to INA proteins by lowering the
freezing point of water (Duman and Olsen, 1993). These proteins have been
observed in bacterial strains obtained from the phyllosphere (Romanovskaya
et al., 2001). More broadly, ice-nucleating bacteria may not be competitive
members of the phyllosphere under non-freezing conditions and are thus
excluded from the community through selection processes. For example, the
biopesticide BlightBan A506 (a strain of Pseudomonas fluorescens) reduces frost
damage of treated plants by 40% through the competitive exclusion of P.
syringae (Lindow et al., 1996; Stockwell and Stack, 2007). Phyllosphere bac-
teria may also increase cold tolerance by the plant itself. For example, strains
of Burkholderia phytofirmans can upregulate the plants’ photosynthetic rate,
sugar uptake, root enlargement, and production of proline and phenolics
while under cold stress (Barka et al., 2006).
Remediation of chemical pollutants is another mechanism by which
bacteria may alter a plant’s stress tolerance. Rhizobacteria can reduce plant
uptake of polycyclic aromatic hydrocarbons by promoting deep-growing
roots (Huang et al., 2004a; Parrish et al., 2005) and by limiting transport to the
aerial portions of the plant, where toxic effects are more pronounced (Huang
et al., 2004b; Vilchez and Manzanera, 2011). Phyllosphere bacteria associated
with aquatic plants can oxidise arsenite, preventing its accumulation and
reducing toxicity (Xie et al., 2014), and the phyllosphere microbiome may
be a major contributor to aquatic arsenic cycling. Similarly, bacteria in the
terrestrial phyllosphere may remediate airborne pollutants. Pseudomonas
strains can accumulate phenol on the leaves of bean plants at concentrations
10-fold higher than in the ambient air, and use that phenol metabolically
as a source of both energy and carbon (Sandhu et al., 2007). This likely

9
provides some protection to the plant from airborne phenolics. The presence
of bacterial genes coding for catechol 2,3-dioxygenase, which degrades
many aromatic compounds, has also been attributed to enhanced plant
survival (Yang et al., 2011). Phenanthrene-degrading bacteria have been
found to colonise the leaves of plants in polluted environments and can
remove a substantial amount of this polyaromatic hydrocarbon (Waight
et al., 2007). Other bacteria can utilise pesticides as sources of phosphorous
(Ning et al., 2012), and so may provide some degree of protection from those
chemicals. The extent to which phyllosphere bacteria carrying out pollutant
remediation activity interact with the host plant is still largely unknown,
as is whether conferred increases in plant tolerance are a mechanism for
increased remediation.
There may also be microbially conferred plant tolerance to other envi-
ronmental stressors. Amending soils with salt-tolerant bacteria can increase
plant growth in saline soils, and seeds treated with salt-tolerant bacteria
show increased germination rates (Mayak et al., 2004; Siddikee et al.,
2011). Whether phyllosphere bacteria show the same benefits has yet to be
studied directly, but halophytic Salicornioideae plants have phyllosphere
microbiomes that consist of bacteria ranging from halotolerant to extreme
halophiles (del Rocío Mora-Ruiz et al., 2015), suggesting a possible role of
the phyllosphere in salt tolerance. The most immediate consequences of
global climate change – greater air and soil temperature, elevated carbon
dioxide concentration, and more frequent drought occurrence – will likely
have significant effects on plant–microbial interactions, but little research
has been devoted to this area (Compant et al., 2010; Kardol et al., 2010). The
phyllosphere microbiome is likely to be more affected by climate change than
endophytic or rhizosphere microbial communities because the leaf surface
is directly exposed to ambient environmental conditions. Ultimately, despite
strong correlations between constituents of the phyllosphere microbiome
and plant stress tolerance, the mechanisms underlying potential interactions
have rarely been studied, and it is often unclear which members of a complex
microbial community confer increased tolerance traits.
4.3 Interactions Between the Phyllosphere Microbiome and Plant

Hormones
The hormonally induced contributions of the phyllosphere microbiome to the
host plant are almost certainly less than those of the rhizosphere (Yang et al.,
2009; Liu et al., 2013; Abd El-Daim et al., 2014); however, knowledge from
rhizosphere and seed-treatment studies (Mahmood et al., 2016) will likely
provide the foundation for future research in above-ground plant tissues.
In most plants, the functions of auxins (predominantly indole-3-acetic acid,
IAA) and cytokinins (CKs) overlap and interact, controlling a well-described
system of plant growth in response to light and nutrients (Skoog and Miller,

10
1957; Schaller et al., 2015). Many of the microorganisms that have been
isolated from the phyllosphere have the ability to synthesise IAA, and do
so in either a plant-growth promoting or pathogenic capacity (Spaepen
et al., 2007). The influence of IAA-producing phyllosphere microorganisms
on plant growth has only recently been considered and evidence suggests
that they can increase plant productivity (Glick, 1995; Romero et al., 2016).
Microorganisms on the leaf can also produce CKs to stimulate nitrogen
transportation to above-ground plant tissues (Holland, 2011), potentially
increasing above-ground plant biomass. However, low concentrations of
CKs produced by pathogenic microorganisms can inhibit salicylic acid (SA)
and interfere with the plant immune response (Ashby, 2000; Argueso et al.,
2012). In such cases, pathogens in the phyllosphere can hijack the cell growth
and immune-mediating functions of CKs.
Stomatal closure is controlled primarily by abscisic acids (ABAs), and
ABA-induced stomatal closure is a major mechanism that confers drought
tolerance to plants (Sussmilch and McAdam, 2017). Some phyllosphere
microorganisms can produce ABA, and this has been linked to attempts to
colonise the leaf interior and alter the plant immune response (Cao et al.,
2011). Microbial pathogens can antagonise the ABA-stomatal interaction in
order to preserve access to the leaf interior (Ton et al., 2009). Interestingly,
leaf endophytes have been found to increase endogenous concentrations of
ABAs to encourage stomatal closure (Forchetti et al., 2007), whereas IAA
and CKs are more commonly synthesised by epiphytic microorganisms
and may antagonise the ABA-controlled closure of stomata (Tanaka et al.,
2006). Under drought conditions, leaf epiphytes and endophytes likely
have opposing goals in regards to stomatal opening or closing, and how
these contrasting functions interact, or the extent to which leaf endophytes
and epiphytes hormonally mediate the plant stress response is poorly
studied.
4.4 The Role of the Phyllosphere Microbiome in Mediating

Plant–Pathogen Interactions
Pathogens can enter the leaves of plants through a variety of entry points,
including stomata, wounds, or hydathodes (Hugouvieux et al., 1998; Melotto
et al., 2008). Biological control of pathogens by other phyllosphere microor-
ganisms involves interactions between the host plant, the potential pathogen,
that pathogen’s competitors, and other members of the microbial commu-
nity on or in the leaf (Elad, 1996). Biological control can be accomplished
through the induction of a plant immune response by non-pathogenic
microorganisms, direct competition between non-pathogenic microor-
ganisms and pathogens, or through the production of antibiotics. Many
microorganisms produce avirulence gene products, which promote the
expression of the plant’s pathogen resistance genes and subsequent local and

11
global responses (Baker et al., 1997; Conrath et al., 2002). Type III secretion
systems are widespread among pathogenic bacteria, and flagellar molecules,
β-glucans, chitin fragments, and ergosterol (all of which could also be
present in non-pathogenic microorganisms) can also act as signals to the
plant to mount its defences (Lugtenber et al., 2002). Bacteria can promote the
expression of degradative enzymes such as chitinase, β-1,3-glucanase and
peroxidase activity by the host plant (Bargabus et al., 2002; Fernando et al.,
2007), which can reduce fungal infections, suggesting another mechanism
by which microorganisms can stimulate the plant to resist pathogens. The
advantage of biological control pathways that involve the plant’s own
immunity is that these defences can stay active even after the control agent
is no longer present (Fernando et al., 2007), potentially providing a longer
term benefit than might be expected.
Competitive exclusion of pathogens by the broader phyllosphere com-
munity also plays an important role in plant pathogen resistance (Zipfel
et al., 2004; Innerebner et al., 2011), although this may depend on specific
competitors for the pathogen being part of the leaf microbiome. For example,
Sphingomonas strains limit the plant pathogen P. syringae in Arabidopsis,
while Methylobacterium strains do not, likely because Sphingomonas is a
direct competitor with P. syringae for glucose, fructose, and sucrose, none
of which are metabolised by Methylobacterium (Innerebner et al., 2011).
Whether produced in response to competition or as a general metabolite, the
production of antibiotics by components of the phyllosphere microbiome
can also inhibit the colonisation of pathogens (Müller et al., 2016). Bacterially
produced antibiotics are often broad-spectrum, acting against a range of
microorganisms including both bacterial and fungal pathogens (Raaijmakers
et al., 2002).
Emergent properties of the collective leaf-associated microbial community
might also be important in mitigating the spread and intensity of plant dis-
eases, although the role of these ecological characteristics is still poorly under-
stood. Higher phyllosphere diversity has been associated with lower dis-
ease incidence and intensity (Balint-Kurti et al. 2010), and this pattern aligns
with the wider body of ecological literature linking greater species diversity
to reduced invasion of exotic species and overall ecosystem health (Naeem
and Li, 1997; Levine et al., 2004; van Elsas et al., 2012). An important driver
of this pattern is the selection effect, wherein increases in diversity lead to
a higher probability of an antagonist towards a pathogen or invader being
present in the community (Fargione and Tilman, 2005). This concept is rele-
vant towards agricultural research, where increased phyllosphere diversity
is less important than promoting the growth of a small subset of beneficial
microorganisms (Rastogi et al., 2012). Future work should explore the rela-
tionship between phyllosphere diversity and disease resistance in an experi-
mental context.

12
5 Future Directions
5.1 Omics Approaches and Phyllosphere Research

High-throughput sequencing and ‘omics’ techniques are beginning to enable
insights into the function and life histories of the phyllosphere microbiome
(Bell et al., 2014). Promising future research exists in understanding mech-
anisms of the microbe–plant and microbe–microbe interactions that deter-
mine the true functionality of the phyllosphere (Hunter et al., 2010). Meta-
transcriptomics has been used to show that the rhizosphere bacterial com-
munity upregulates stress tolerance genes after the introduction of fungal
pathogens, and this may stimulate the plant to express fungal antagonistic
genes (Chapelle et al., 2016). Understanding the molecular basis of similar
mutualistic defence mechanisms in the phyllosphere is a promising avenue
of future research. Fungal transcripts can be separated from those of the plant
based on sequence length and GC content (Delhomme et al., 2015), suggesting
the potential for co-analysis of both the host plant transcriptome and that of
its fungal community. Such approaches could be useful in elucidating inter-
actions between pathogens and host, as well as the broader microbiome. Also
of interest would be attempt to connect metagenomics, metatranscriptomics,
or metaproteomics with the emerging field of metabolomics, which charac-
terises the chemical outputs of cell metabolism (Aguiar-Pulido et al., 2016).
5.2 An Ecological Approach to Plant–Microbe

and Microbe–Microbe Interactions
High-throughput molecular approaches should also enable better investiga-
tion of spatial and temporal phyllosphere dynamics, as well as exploration
of dominance and competition in microbial communities. The endophyte
Azospirillum brasilense improves rice yield 19% compared to controls (Pedraza
et al., 2009), but simultaneous treatment with two strains of A. brasilense
decreases yield below the control level. We have a very poor understand-
ing of why such interactions occur, and studies of such microbe–microbe
competition are also relevant to the success of biological pathogen control.
Exploring whether members of the phyllosphere act as ecosystem engineers
of the leaf surface, perhaps by modifying the cuticle or producing EPS,
or identifying whether particular microbial keystone species (Meyer and
Leveau, 2012) structure the phyllosphere microbiome could also be useful
applications of ecological concepts. The issue of scale is important, as phyllo-
sphere communities can vary as much at the very fine scales between leaves
as they do across biogeographic distances (Cordier et al., 2012). Such spatial
variability is conflated by temporal variation in phyllosphere structure as
immigration/emigration varies from scales of hours to seasons (Lindemann
and Upper, 1985; Penuelas et al., 2012; Copeland et al., 2015). Accurately

13
assessing this variability and how it influences the interactions between the
phyllosphere microbiome and the plant host are of critical importance.
5.3 Modelling and Prediction of the Phyllosphere

An emerging area of microbiome analysis is the use of theories developed
from social networks to construct maps of microbial co-occurrence and
interaction (Faust and Raes, 2012). These approaches can identify organisms
that function as network hubs, which are strong candidates for ecological
keystone species (Berry and Widder, 2014). Applying such approaches to
the phyllosphere microbiome could identify which of its components are
most critical for plant health and function and, when related to variability
in plant characteristics, might determine which microorganisms are most
closely associated with changes to the plant (Poudel et al., 2016). For
example, establishment of the oomycete pathogen Albugo in the Arabidopsis
phyllosphere not only reduced overall bacterial diversity, but also influenced
the interactions between bacteria and a variety of abiotic factors (Agler
et al., 2016). Modelling techniques can pare down complex microbiomes into
more tractable units that are amenable to the experimentation necessary to
accurately determine the role of plant-associated bacteria. Similarly, unsu-
pervised learning (i.e., machine learning) methods can be used to predict
single variables in response to non-parametric microbial and environmental
data. Plant microbiome research is likely to depend on increasingly complex
statistical computations, which will yield valuable insights into the dynamics
of the plant-phyllosphere system.
Related Articles
Microbial Communities in the Phyllosphere

Filamentous Fungi on Plant Surfaces
Plant–Microbe Interactions and Secondary Metabolites with Antibacterial,
Antifungal and Antiviral Properties
Metabolite Analysis and Metabolomics in the Study of Biotrophic Interac-
tions between Plants and Microbes
Plant-Microbe Interactions and Secondary Metabolites with Antiviral,
Antibacterial and Antifungal Properties
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The role of the phyllosphere microbiome in plant health and function

Article · August 2018

Bram Stone Eric Weingarten

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THE ROLE OF THE

Abstract: The above-ground surfaces of plants (the phyllosphere) harbour a

Keywords: bacteria, endophytes, leaf, microbial community, microbiome, phyl-

The fact that macroorganisms harbour diverse communities of microorgan-

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

2 The Leaf Surface as a Habitat for Microbial Growth

Environmental conditions at the leaf surface exert a tremendous influence

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

oxidizers can also be present in the phyllosphere (Bowatte et al., 2015;

3 The Nature and Composition of the Phyllosphere

Phyllosphere microbiota represent a diverse array of microorganisms, but

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

phyllosphere bacteria that carry out methyltrophy, nitrification, nitrogen

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

been implicated as starvation prevention mechanisms in oligotrophic marine

4 Interactions Between the Leaf Microbiome and the Plant

4.1 The Role of Phyllosphere Microorganisms in Plant Nutrient

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

fixation in their phyllosphere, and this likely provides a substantial amount

4.2 The Inﬂuence of the Phyllosphere Microbiome on Host Stress

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

if increased thermal resistance can be promoted by bacteria on the surface of

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

4.3 Interactions Between the Phyllosphere Microbiome and Plant

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

4.4 The Role of the Phyllosphere Microbiome in Mediating

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

5.1 Omics Approaches and Phyllosphere Research

5.2 An Ecological Approach to Plant–Microbe

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

5.3 Modelling and Prediction of the Phyllosphere

Microbial Communities in the Phyllosphere

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

Vilchez, S. and Manzanera, M. (2011). Biotechnological uses of desiccation-tolerant

Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.

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