CHAPTER 8

Interactions between Fungal Endophytes and

Bacterial Colonizers of Fescue Grass

Elizabeth Lewis Roberts and Christopher Mark Adamchek

CONTENTS

8.1 Introduction ................................................................................................................................................................ 109

8.2 Alkaloids..................................................................................................................................................................... 109
8.3 Bacterial Epiphytes ......................................................................................................................................................110
8.3.1 Phyllosphere.....................................................................................................................................................110
8.3.2 Rhizosphere .....................................................................................................................................................111
8.3.3 Seed Communities ...........................................................................................................................................111
8.4 Transfer of PGP Bacteria from Tall Fescue Seed to Rhizosphere...............................................................................111
8.5 Summary .....................................................................................................................................................................115
8.6 Acknowledgments........................................................................................................................................................115
References .............................................................................................................................................................................115

8.1 INTRODUCTION S. arundinaceus host has focused on the aboveground region

Endophytic clavicipitalean fungi (Ascomycota, Hypoc-
reales) are well known for their ability to increase fitness in
their C3 grass hosts (Poaceae). This relationship is defined
by the presence of asymptomatic hyphae that are mostly
observed in the intercellular spaces of the aboveground
tissues of the host plant. The endophytic fungus attains a
constant source of carbohydrates from the plant, and, in turn,
it produces secondary metabolites, which have been attrib-
uted to decreasing susceptibility of the host plant to abiotic
stresses (Clay 1990; Malinowski and Belesky 2000; Schardl
et al. 2004; Kuldau et al. 2008).
Additional benefits associated with endophyte infection
of tall fescue (Schedonorus arundinaceus) include decreased
infection by root-knot nematodes (Meloidogyne mary-
landi) and inhibited reproduction by migratory nematodes
(Pratylenchus scribneri) (Elmi et al. 2000; Kimmons et al.
1990). Endophyte infection is also attributed to increased
growth of the host plant, which is well documented but poorly
understood (Schardl et  al. 2004). Furthermore, researchers
have surmised unclear effects of fungal-produced plant hor-
mones on plant physiology (Clay 1990).
Research on the unique relationship between clavicipital-
ean fungi of the genus Epichloë (Fr.) Tul. & C. Tul. and their
of the plant, as the fungus primarily resides in the intercel-
lular spaces of the stems and leaf sheaths (White 1987; see
Figure 8.1). However, as asexual Epichloë is vertically trans-
mitted from mother plant to daughter plant, the endophyte
spends part of its life cycle within the seeds (Clay 1990).
8.2 ALKALOIDS
The mutualism between S. arundinaceus and Epichloë
coenophialum is due in part to the four classes of alkaloids,
which in the mature plant are known to limit mammalian
and insect herbivores (Bush et al. 1993; Wilkinson et  al.
2000; Ji et al. 2014). While the lolitrems ward off vertebrate
herbivores, the ergot alkaloids provide defense against both
vertebrate and invertebrates. Loline and peramine alka-
loids only decrease herbivory by invertebrates. The asexual
phase of Epichloë, formerly referred to as Neotyphodium, is
known to produce much higher levels of alkaloids than the
sexual phase (Schardl et al. 2012).
While these alkaloids accumulate in the aboveground
vegetative tissue, where the fungus resides, these beneficial
alkaloids are produced in the seeds by the vertically trans-
mitted endophyte. Further, alkaloid concentration varies

109
 110 THE FUNGAL COMMUNITY

Seed head

Blade

Phyllosphere
Endophyte (Epichloë)
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N-formylloline

Sheath

Rhizosphere
Alkaloid-catabolizing bacteria
Burkholderia ambifaria
Psuedomonas aureofaciens

Roots

Figure 8.1 Epichloë endophytes colonize the intercellular spaces of cool season grasses. The endophytes produce alkaloids such as
N-formylloline, which leach out onto leaves and exude into the rhizosphere. Bacterial colonizers that catabolize the alkaloid
have increased fitness in the phyllosphere and rhizosphere of tall fescue.

within different plant tissues (Spiering et al. 2005). Of the
several loline alkaloids produced by Epichloë endophytes,
N-formylloline (NFL) is typically found in the highest con-
centrations (Justus et al. 1997). In some cases, the total con-
centration of lolines exceeds 2% of the dry weight of the
grass (Blankenship et al. 2001).
8.3 BACTERIAL EPIPHYTES
8.3.1 Phyllosphere
The surfaces of the aboveground tissues of plants
(phyllosphere) are populated by bacteria, fungi, and proto-
zoans. Carbohydrates, amino acids, and other organic com-
pounds, which passively leach onto the leaf surface, are
considered the major source of carbon compounds for epi-
phytic microbes. However, leachates account for less than
10 μg/g of plant tissue and therefore are not abundant nutrient
sources (Mercier and Lindow 2000). Thus, many epiphytic
microbes are limited by the amount of nutrients that escape
onto the plant surface.
N-formylloline exits from the plant interior and onto
the leaf surface via guttation fluid and wounding, where it
becomes available for consumption by epiphytes (Koulman
et al. 2007). In the phyllosphere of tall fescue, the presence of
NFL increases the fitness of bacteria that are able to catabo-
lize the alkaloid, and these bacteria make up the majority
of the phyllosphere microbial community of endophyte-
infected grasses (Roberts and Lindow 2014). 16S rRNA
sequencing of NFL-enrichment cultures from leaf surface
samples identified Burkholderia ambifaria, Pseudomonas
fluorescens, Stenotrophomonas maltophilia, and Serratia
proteamaculans as the dominant culturable phyllosphere
bacteria. Additional analysis showed that the ability to catab-
olize NFL is a trait only found in bacteria associated with
loline-producing endophyte-infected turfgrasses. Coyote
bush (Baccharis pilularis) and black sage (Salvia mellifera)
 INTERACTIONS BETWEEN FUNGAL ENDOPHYTES AND BACTERIAL COLONIZERS OF FESCUE GRASS
plants, growing in the California chaparral, which is devoid of
tall fescue, harbor no loline-catabolizing bacterial epiphytes
(Roberts and Lindow 2014). Therefore, the presence of par-
ticular bacteria on tall fescue plants can be attributed to NFL.
8.3.2 Rhizosphere
Rhizosphere-dwelling microorganisms experience more
stability in abiotic stresses and have greater access to nutri-
ents than their phyllosphere counterparts. A continuous
supply of carbohydrates and mucilage are secreted into the
rhizosphere by plant roots (Bais et  al. 2006). In clavicipi-
talean fungal infections of grasses, the endophyte mostly
resides in the aerial parts of the plant, but the protective
alkaloids that they produce are translocated to the roots
(Kimmons et  al. 1990). Furthermore, Epichloë mycelium
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and loline alkaloids have been observed in tall fescue roots
(Schardl and Moon 2003; Nagabhyru et al. 2013). In addi-
tion, in meadow fescue, 1937  μg/g of loline alkaloids has
been observed in the roots (Patchett et al. 2008). Thus, NFL
is likely secreted in rhizosphere exudates.
Next-generation sequencing of total DNA from rhizo-
planes showed that bacterial community composition varies
between endophyte-infected (E+) and endophyte-free (E–)
tall fescue rhizospheres. Several beneficial plant-growth-
promoting bacteria were found in greater abundance in
the rhizospheres of E+ plants than in the rhizospheres of
E– plants (Roberts and Ferraro 2015). Similar to the phyl-
losphere dwellers, loline-catabolizing rhizosphere bacteria
have increased fitness over bacteria that are not able to use
the alkaloid as a nutrient source (Roberts and Ferraro 2015).
In addition, seeding the E+ rhizospheres with loline-
catabolizing strain B. ambifaria increased the population
sizes of beneficial Bacillus strains by 15% as compared
with controls (Roberts and Ferraro 2015). Plant-growth-
promoting Bacillus strains produce auxin, siderophores,
ammonium, and proteases and are known for inorganic
phosphate solubilization (Hayat et  al. 2010). The increase
in plant-growth-promoting bacteria (PGPB) could be quite
beneficial to the fescue plant, and this result indicates a clear
influence of the loline-catabolizing strain on tall fescue rhi-
zosphere community composition.
8.3.3 Seed Communities
Studies of the microbial communities on seeds are
limited, with most of the literature focusing on seed-borne
plant pathogens (Baker and Smith 1966; Darrasse et  al.
2010). Some plants have been shown to harbor specific bac-
teria on seeds that later colonize the seedling (Ferreira et al.
2008). Transmission from seed to seedling is not guaran-
teed, as seed-borne microorganisms must compete with soil
microbes for the nutrients released from emerging seedlings
during germination (Nelson 2004). However, Buyer et  al.
(1999) found that seed exudates played a minimal role in
111
bacterial community structure. Their analysis showed that
there was little variation in the microbial communities of
corn, cucumber, radish, and soybean seeds 96  hours after
sowing, despite significantly different carbohydrate and
amino acid exudate production. Similarly, pyrosequencing
of seed washes from Brassica and Triticum showed that nei-
ther epiphytic bacterial load nor community richness was
different between the two seed types (Links et  al. 2014).
However, the investigators used only a fragment of chapero-
nin 60 (cpn60) as their molecular marker. More appropri-
ately, Barret et al. (2015) utilized the V4 region of 16S rRNA
and a portion of gyrB for bacterial taxa as well as ITS1 for
identification of fungal taxa to examine seed microbiomes
of different Brassicaceae plants. They concluded that host
species affect fungal community composition but have no
effect on bacterial seed communities.
While the presence of seed-borne bacteria on cool
season grasses has been previously examined, the studies
focused only on culturable bacteria (White et al. 2012; White
et al. 2015). By using culture-free methods, we analyzed the
differences in bacteria from endophyte-infected (E+) and
endophyte-free (E–) tall fescue seeds. Because Epichloë
coenophiala is vertically transmitted, we hypothesized that
the E+ tall fescue seeds would have unique microbiota.
Illumina sequencing of the V4  region of 16S rRNA
illustrated that the diversity of bacteria is higher (Shannon
Diversity index = 3.7) on endophyte-infected tall fescue
seeds than on endophyte-free seeds (Shannon Diversity
index = 1.53) and that the E+ seeds have a distinct micro-
flora from the E– seeds (Figure 8.2) (Adamchek and
Roberts 2015). Furthermore, the E+ bacterial communi-
ties from seed surfaces and seed interiors have a higher
relative abundance of plant-growth-promoting bacte-
ria (Figure 8.3, Table 8.1). While Pseudomonas tolaasii
dominated the interiors of E+ seeds, the seed surface had
several equally distributed strains, with Rhizobium sp.,
Pedobacter sp., Pantoea agglomerans, Agrobacterium sp.
and Enterobacter cowanii making up the majority of the
community (Figure 8.3).
8.4 TRANSFER OF PGP BACTERIA FROM
TALL FESCUE SEED TO RHIZOSPHERE
Seed-borne bacteria of agricultural plants have been
shown to be sources of bacteria in host tissues (Hallmann
et al. 1997). Illumina sequencing of E+ seed coats and rhizo-
spheres demonstrated a 44% similarity in bacterial commu-
nity composition (Figure 8.4). The most abundant phylum in
common from before planting (seed surface) to later growth
stages was Proteobacteria, with 68% washed from seed sur-
faces, 62% in the rhizospheres of 3-week-old plants, and 67%
by 6 weeks (Figure 8.5) (Adamchek and Roberts 2015).
Table 8.1  highlights the plant-growth-promoting prop-
erties of the dominant bacterial epiphytes found from tall
 112 THE FUNGAL COMMUNITY

100%

ACETOBACTERACEAE
ACIDIMICROBIACEAE
ALCALIGENACEAE
90% AURANTIMONADACEAE
BACILLACEAE
BRADYRHIZOBIACEAE
CAMPYLOBACTERACEAE
80% CARNOBACTERIACEAE
CAULOBACTERACEAE
COMAMONADACEAE
CYTOPHAGACEAE
ENTEROBACTERIACEAE
70%
FLAVOBACTERIACEAE
GEODERMATOPHILACEAE
HALOMONADACEAE
HYPHOMICROBIACEAE
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60% KINEOSPORIACEAE
MARINILABILIACEAE
Relative abundance

METHYLOBACTERIACEAE
METHYLOPHILACEAE
MICROBACTERIACEAE
50%
MICROCOCCACEAE
MORAXELLACEAE
NAKAMURELLACEAE
NOCARDIACEAE
40% NOCARDIOIDACEAE
OXALOBACTERACEAE
PAENIBACILLACEAE
PHYLLOBACTERIACEAE
30% PORPHYROMONADACEAE
PROMICROMONOSPORACEAE
PSEUDOMONADACEAE
PSEUDONOCARDIACEAE
RHIZOBIACEAE
20% RHODOCYCLACEAE
RHODOSPIRILLACEAE
SANGUIBACTERACEAE
SPHINGOBACTERIACEAE
10% SPHINGOMONADACEAE
STREPTOCOCCACEAE
STREPTOMYCETACEAE
STREPTOSPORANGIACEAE
XANTHOMONADACEAE
0%
E+ seed coat E− seed coat

Figure 8.2 (See color insert.) Comparison of bacterial families washed from endophyte-infected (E+) and endophyte-free (E–) tall
fescue seeds.

fescue seeds and rhizospheres. Of the 15 most abundant
bacteria, only two of the most abundant strains on the seeds
(Chryseobacterium indologenes and Chryseobacterium
spp.) have no published data that indicate plant growth pro-
motion. Notably, Pedobacter sp., which makes up 7% of
the seed surface microbiome, has been shown to suppress
the growth of the fungal pathogen Rhizoctonia solani, when
combined with Pseudomonas sp. (Yin et al. 2013). Similarly,
volatile organic compounds produced by Xanthomonas vesi-
catoria have been shown to inhibit the growth of R. solani
(Weise et al. 2012). Although this bacterium is less abundant
in the seed bacterial community, perhaps the presence of
X. vesicatoria is responsible for the reduction of Rhizoctonia,
observed in endophyte-infected tall fescue (Gwinn and
 INTERACTIONS BETWEEN FUNGAL ENDOPHYTES AND BACTERIAL COLONIZERS OF FESCUE GRASS 113

Seed interior Seed surface

sp. (9 rium
%)

%)
bacte
(8
p.
as

Agro
ell
Dy
%)
(10
a n toeaerans
P lom
agg Rhizobium sp. (8%)

En
co tero

)
wa b

%
ni act

agglomerans (9%)
(7
Pseudomonas tolaasii (58%) i ( er

.
8%

sp
)

r
cte
ba

Pantoea
do
Pe
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Figure 8.3 Bacterial communities of tall fescue seed interiors and seed surfaces are dominated by plant-growth-promoting species.

Table 8.1 Plant-Growth-Promoting and Protection Properties of the Dominant Bacteria Found in the Rhizosphere and Seed
Surface of Tall Fescue Plants
Phosphate-
Rhizosphere Auxin Siderophore Solubilizing Ammonium Chitinase
Bacillus sp. + + + + +
Stenotrophomonas sp. + + + + +
Burkholderia sp. + + +   −
Pseudomonas sp. + + + + +
Acidobacterium spp. − + − − −
Variovorax spp. − + − − −
Lysobacter spp. − − − − +
Nitrosomonas spp. − − + − −
Bradyrhizobium spp. − − − + −

Phosphate-
Seed Surface Auxin Siderophore Solubilizing Ammonium Chitinase
Agrobacterium tumefaciens + + − − −
Brevundimonas vesicularis − + − − −
Chryseobacterium indologenes − − − − −
Chryseobacterium spp. − − − − −
Enterobacter cowanii − − − − +
Frigoribacterium spp. + + − − −
Hymenobacter spp. − − − − −
Massilia timonae + + − − +
Pantoea agglomerans + − − + −
Pedobacter aurantiacus − − − − −
Pseudomonas spp. + + + − −
Rhizobium spp. − − − + −
Rhodococcus fascians + − − − −
Sphingomonas spp. − − − + −
Xanthomonas vesicatoria − − − − +
 114 THE FUNGAL COMMUNITY

100%

90%

ACIDOBACTERIA
80%
ACTINOBACTERIA
BACTEROIDETES
70% CHLOROGI
CHLOROFLEXI
60% FIRMICUTES
Relative abundance

GEMMATIMONADETES

50% NITROSPIRAE
PLANCTOMYCETES
PROTEOBACTERIA
40%
SBR1093 (CANDIDATE DIVISION)
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SPAM (CANDIDATE DIVISION)

30%
TM6 (CANDIDATE DIVISION)
TM7 (CANDIDATE DIVISION)
20% VERRUCOMICROBIA
OTHER
10%

0%
Seed wash 3 wk rhizosphere 6 wk rhizosphere

Figure 8.4 (See color insert.) Relative abundance of the major bacterial phylum from seed surfaces, rhizospheres of 3-week-old E+ tall
fescue, and rhizospheres of 6-week-old (E+) tall fescue plants.

ACETOBACTERIACEAE
AURANTIMONADACEAE
BURKHOLDERIACEAE
COMAMONADACEAE
CYTOPHAGACEAE

RHIZOSPHERE FLAVOBACTERIACEAE
(Total 59435) GEODERMATOPHILACEAE
MICROBACTERIACEAE
NOCARDIACEAE
OXALOBACTERACEAE
SC
(Total 44835) PSEUDOMONADACEAE
Sl
(Total 20642) RHIZOBIACEAE
SPHINGOBACTERIACEAE
SHINGOMONADACEAE
XANTHOMONADACEAE

Figure 8.5 (See color insert.) Overlap of three bacterial families from rhizosphere, seed interiors, and seed coats, based on operational
taxonomic units (OTU) (3% distance) and the taxonomic identities of the shared OTUs at the family level. The number in
parentheses represents the total OTUs for that community.
 INTERACTIONS BETWEEN FUNGAL ENDOPHYTES AND BACTERIAL COLONIZERS OF FESCUE GRASS
Gavin 1992). Pantoea agglomerans makes up 10% of the
bacterial community inside of seeds, and 9% of the seed
surface community has been shown to produce two antibi-
otics that control pathogenic Erwinia amylovora (Wright
et  al. 2001). In addition, P. agglomerans is known for
fixing nitrogen, limiting pathogenic infection, increasing
drought tolerance, and producing auxin (indole-3-acetic
acid [IAA]) on host plants (Lindow and Brandl 2003).
A  study by Rfaki et  al. (2014) found that Enterobacter
cowanii on legumes solubilize phosphate, produce IAA,
and have siderophores.
Loline catabolizer B. ambifaria is a common rhizosphere
strain that is used as a biological control agent against fun-
gal pathogens (Coenye and Vandamme 2003; Li et al. 2002).
It has been found to promote plant growth via auxin, sid-
erophore production, and nitrogen fixation (Parra-Cota et al.
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2014). In addition, this bacterium has been found to solubilize
phosphate (Walpola et al. 2012). Furthermore, B. ambifaria
outcompetes other bacteria in the rhizosphere, just as it does
on the phyllosphere (Roberts and Ferraro 2014; Roberts and
Lindow 2015). Although dominant in the phyllosphere and
rhizosphere, this strain was not isolated from seed samples.
8.5 SUMMARY
In many plants, the chemicals present in root exudates
can act as substrates or signaling molecules (Badri et al.
2013; Bais et  al. 2006; Neal et  al. 2012). Plant-growth-
promoting bacteria (PGPB) are known to inhabit rhizo-
spheres owing to the presence of particular exudates. These
bacteria benefit the plant host by warding off microbial
pathogens through niche exclusion, induced systemic resis-
tance (ISR), and the production of antimicrobial compounds
(Bais et  al. 2006). Plant-growth-promoting bacteria also
typically fix nitrogen, solubilize phosphorus, chelate iron,
and produce plant hormones (Kloepper 1997; Rengel 1999).
Above all, plant exudates are believed to be the underlying
reason that different plants harbor different microbial colo-
nizers (Haichar et al. 2008; Chaparro et al. 2014).
As Epichloë infection and loline production have been
noted in the roots of tall fescue (Schardl and Moon 2003),
it is likely that lolines are released into the rhizosphere
and that N-formylloline acts as a nutrient source for some
rhizosphere-dwelling microorganisms. In fact, the E+
rhizosphere is dominated by PGPB, which are further influ-
enced by the presence of loline-catabolizing B. ambifaria
(Roberts and Ferraro 2015). Thus, NFL produced by Epichloë
endophytes shapes the phyllosphere and rhizosphere com-
munities in the way that other chemical stimulants secreted
by plants recruit and activate PGPB (Roberts and Lindow
2014; Roberts and Ferraro 2015; Berendsen et  al. 2012).
If bacterial colonizers are able to catabolize ergot or pera-
mine alkaloids, as some do the lolines, the presence of these
115
alkaloids may also act in recruitment of beneficial bacteria
to the fescue host.
Similarly, the microbial community of tall fescue seeds
appears to be influenced by the presence of the endophyte
as well. Further analysis will need to be conducted to bet-
ter understand the role of NFL on seed-colonizing bacteria.
However, as almost half of the PGPB that dominate tall fes-
cue seed also make up the majority of the rhizosphere com-
munity, we surmise that plant-growth-promoting bacteria
are vertically transmitted in tall fescue.
As illustrated in Table 8.1, many of the plant-growth-
promoting bacteria associated with tall fescue solubilize
phosphorus and fix nitrogen. Conversely, while there is
an increase in alkaloid production with greater nitrogen
and phosphorus availability, fungal biomass decreases
(Malinowski  et  al. 1998; Rasmussen et  al. 2007). This is
perhaps an area where bacterial colonizers directly influ-
ence the fungal endophyte, either by making those nutrients
more available or by consuming the alkaloids and thus mak-
ing a sink for the excess nutrients.
8.6 ACKNOWLEDGMENTS
We would like to thank Jacqueline Desrosier and
Brendan Mormile for their diligent help in reviewing this
manuscript. Funding in support of this work was awarded
to Elizabeth Lewis Roberts through the SCSU Minority
Retention and Recruitment Committee and the Connecticut
State University Grants program.
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