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The diversity and distribution of endophytes across biomes, plant phylogeny, and host tissues—how far have we come and where do we go from here?

March 2020
Environmental Microbiology 22(6)

March 2020
22(6)

Authors:

Warren Wilson College

The interiors of plants are colonized by diverse microorganisms that are referred to as endo‐phytes. Endophytes have received much attention over the past few decades, yet many basic questions remain unanswered regarding patterns in their biodiversity at local to global scales. To characterize research effort to date, we synthesized results from ~600 published studies. Our survey revealed a global research interest and highlighted several gaps in knowledge. For instance, of the seventeen biomes encompassed by our survey, seven were understudied and together composed only 7% of the studies that we considered. We found that fungal endophyte diversity has been characterized in at least one host from 30% of embryophyte families, while bacterial endophytes have been surveyed in hosts from only 10.5% of families. We complimented our survey with a vote counting procedure to determine endophyte rich‐ness patterns among plant tissue types. We found that variation in endophyte assemblages in above‐ground tissues varied with host growth habit. Stems were the richest tissue in woody plants, whereas roots were the richest tissue in graminoids. For forbs, we found no consistent differences in relative tissue richness among studies. We propose future directions and guidelines to fill the gaps in knowledge we uncovered and inspire further research. This article is protected by copyright. All rights reserved.

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The diversity and distribution of endophytes across

biomes, plant phylogeny and host tissues: how far have

we come and where do we go from here?

Joshua G. Harrison

*and Eric A. Grifﬁn

Department of Botany, University of Wyoming, 3165,

1000 E. University Ave., Laramie, WY, 82071.

Department of Biology, New Mexico Highlands

University, Las Vegas, NM, 87701.

Summary

The interiors of plants are colonized by diverse micro-

organisms that are referred to as endophytes. Endo-

phytes have received much attention over the past few

decades, yet many questions remain unanswered

regarding patterns in their biodiversity at local to

global scales. To characterize research effort to date,

we synthesized results from ~600 published studies.

Our survey revealed a global research interest and

highlighted several gaps in knowledge. For instance,

of the 17 biomes encompassed by our survey, 7 were

understudied and together composed only 7% of the

studies that we considered. We found that fungal

endophyte diversity has been characterized in at least

one host from 30% of embryophyte families, while

bacterial endophytes have been surveyed in hosts

from only 10.5% of families. We complimented our

survey with a vote counting procedure to determine

endophyte richness patterns among plant tissue types.

We found that variation in endophyte assemblages

in above-ground tissues varied with host growth

habit. Stems were the richest tissue in woody plants,

whereas roots were the richest tissue in graminoids.

For forbs, we found no consistent differences in rela-

tive tissue richness among studies. We propose future

directions to ﬁll the gaps in knowledge we uncovered

and inspire further research.

Introduction

In 1887, Galippe reported that soil-derived microbes could

reside within the above-ground tissues of healthy plants. At

the time, this work was underappreciated, perhaps because

of the long-prevailing attitude that microbial assemblages

solely comprised deleterious pathogens (Compant et al.,

2012), this notwithstanding the work of Frank and others

demonstrating the mutualistic nature of the mycorrhizal–

host relationship (Frank, 1885, 2005; Trappe, 2005).

Nevertheless, Galippe’s observations set the stage for an

exploration of the non-pathogenic portion of the plant micro-

biome that took place from the late 1800s into the mid-

1900s (Laurent, 1889; Janse, 1897; Rayner, 1915; Auret,

1930; Hardoim et al., 2015). During those decades, knowl-

edge began to accumulate regarding the diversity, preva-

lence and ecological roles of the so-called ‘endophytes’

(Box 1; Campbell, 1908; Hyde and Soytong, 2008), with

much early work focused on the fungi living within grasses

(e.g. Sampson, 1937; Neill, 1940). Seminal research in the

1970s and 1980s led to widespread acknowledgement of

the ubiquitous nature of non-pathogenic fungi and bacteria

in plant tissues, particularly within leaves (Carroll and

Carroll, 1978; Carroll, 1988; Petrini, 1991). These studies

have inspired an evergrowing interest from microbial ecolo-

gists (Fig. 1), yet answers to many basic questions regard-

ing the natural history, biogeography, ecology and evolution

of endophytes remain elusive.

Box 1. What, exactly, is an endophyte?

The term ‘endophyte’is believed to have originated

with de Bary (1866), who so dubbed pathogenic,

plant-inhabiting microbes because of their habitat

(also see Link, 1809). Since then, the term endo-

phyte has been expanded to invoke both a habitat

and a non-pathogenic lifestyle (at least in some hosts

and life history stages) and encompasses fungal

(Petrini, 1991; Rodriguez et al., 2009), bacterial

Received 17 October, 2019; revised 24 February, 2020; accepted 27

February, 2020. *For correspondence. E-mail joshua.harrison@

uwyo.edu; Tel. 1-307-766-2384; Fax 1-307-766-2851

Environmental Microbiology (2020) 00(00), 00–00 doi:10.1111/1462-2920.14968

(Ryan et al., 2008; Grifﬁn and Carson, 2015) and

archael taxa (Müller et al., 2015; Moissl-Eichinger

et al., 2018). The term endophyte can be used sensu

lato to refer to those taxa that live inside of plant tis-

sues, either inside of or between host cells. However,

in our experience, contemporary microbial ecologists

most often use the term sensu stricto to refer to

those taxa, which over some portion of their life his-

tory do not cause obvious harm to their hosts, such

as inducing a hypersensitive response (Petrini, 1991;

Wilson, 1995; Stone et al., 2000). The lack of preci-

sion in this deﬁnition is somewhat unsatisfying, but

does hint at the complex life histories of many endo-

phytic taxa (Rodriguez et al., 2009). Indeed, for per-

haps the majority of endophytic taxa, individuals are

horizontally transmitted among hosts and, conse-

quently, may exist outside of the plant corpus for

some time, for instance as spores or endospores,

free living cells or colonies, or as epiphytic fruiting

bodies on decaying tissue (Malloch and Blackwell,

1992; Rodriguez et al., 2009). The term endophyte is

particularly strained by the mycorrhizal fungi, which

possess a mycelium that grows externally to the host

and also penetrates the root epidermis (Jumpponen,

2001; Schulz and Boyle, 2006). The categorization of

these fungi as endophytes seems to be on an

author-by-author basis (Schulz and Boyle, 2006).

These examples illustrate how the term endophyte is

useful for communication, but not biologically well

delineated.

What is clear, however, is that fungal and bacterial

endophytes are important –even critical –components of

the world’s ecosystems. Endophytes can affect plant

phenotype, including decreasing disease susceptibility

(Arnold et al., 2003; Compant et al., 2005; Herre et al.,

2007; Busby et al., 2016; Christian et al., 2017), increas-

ing resistance to abiotic stressors (Redman et al., 2002;

Márquez et al., 2007; Rodriguez et al., 2008), shaping

phytochemical proﬁles (Kusari et al., 2012; Panaccione

et al., 2014) and mediating plant functional trait expres-

sion (Friesen et al., 2011; Grifﬁnet al., 2016). Recent

work has demonstrated how these various effects of

endophytes can inﬂuence whole ecosystem level pro-

cesses (Clay and Holah, 1999; Kivlin et al., 2013; Grifﬁn

et al., 2017; Laforest-Lapointe et al., 2017b; Christian

et al., 2019). Importantly, endophytes are often errone-

ously assumed to have predominantly mutualistic associ-

ations with their hosts. Reality is much more complex

and the inﬂuence of endophyte taxa is highly context

dependent (Carroll, 1988; Rodriguez et al., 2009), with

interactions between hosts and endophytes ranging

from mutualism through commensalism to latent or mild

antagonism (Saikkonen et al., 1998; Schulz and Boyle,

2005; Hardoim et al., 2008).

Much of the focus on endophytes has been driven by

the desire to harness these taxa to manipulate plant phe-

notype (e.g. increase growth, Doty, 2011) and prevent

pathogen colonization of crops (Busby et al., 2017).

Endophytes have also attracted attention from natural

products chemists who survey the world’s organisms for

useful compounds (Strobel and Daisy, 2003; Aly et al.,

2010). This is motivated by the capacity of various endo-

phytes to synthesize an impressive array of bioactive

small molecules (Newman et al., 2003; Strobel et al.,

2004; Verma et al., 2009). Indeed, a number of

endophyte-synthesized compounds are of medicinal

value (Strobel et al., 1996; Kharwar et al., 2011).

Both basic and applied research regarding endophytes

have been hampered by a lack of knowledge regarding

the distribution of endophyte biodiversity at any spatial

scale –from global, interbiome scales to among the tis-

sues of individual host plants. Similarly, almost nothing is

known regarding how endophyte biodiversity maps onto

the plant phylogeny. Characterizing such broad patterns

in endophyte biodiversity is extremely logistically challeng-

ing because of the outlay of effort required for large cultur-

ing and sequencing projects (Arnold and Engelbrecht,

2007; Nilsson et al., 2019; Carini, 2019). Moreover, deter-

mining the causes of patterns in endophyte diversity is

difﬁcult because they result from the interplay of many

forcings, including both contemporary and historical eco-

logical drivers (i.e. niche determination, ecological drift,

dispersal limitation) and, at longer timescales, evolutionary

processes (i.e. divergence and extinction, Hanson et al.,

2012; Wiens and Donoghue, 2004).

Further complicating matters is the disconnection

between the spatial scale of sampling endophyte assem-

blages, as dictated by logistical constraints, and the size

of the focal organisms. This problem was well illustrated

by Remus-Emsermann and Schlechter (2018) who

Year

Num. of studies

100

150

200

250

300

100

150

200

250

300

1978

1980

1990

2000

2010

2016

Fungal endophytes

Bacterial endophytes

Fig. 1. The number of studies characterizing endophyte biodiversity

published each year since the late 1970s. Studies are parsed by tax-

onomy with fungal studies in grey and bacterial studies in black.

2J. G. Harrison and E. A. Grifﬁn

pointed out that the disparity in size between a single

bacterium of 2 μm

and a leaf mirrors the ratio of sizes

between a person and a mid-sized country. Indeed, using

traditional culturing and sequencing methodologies, we

can only sample what are in effect whole regions of

endophytes that may include multiple assemblages that

never directly interact, that have been shaped by differing

community assembly processes and that may even have

divergent evolutionary histories. This complicates the

study of endophyte biogeography and community ecol-

ogy because the scale of sampling is so much larger than

many covariates that may affect the membership of endo-

phytes in a particular assemblage. For instance, micro-

habitat variation within leaves (such as proximity to upper

or lower leaf surfaces, veins) may have effects on endo-

phyte assemblages akin to those of shifting elevation

across a mountainside on forest composition, and those

forcings are unavailable for study when the unit of repli-

cation is an entire leaf or even a leaf section (Lodge

et al., 1996; Herre et al., 2007; Vacher et al., 2016;

Remus-Emsermann and Schlechter, 2018). Adding

further complexity, some bacterial endophytes can live

inside endophytic fungi (Shaffer et al., 2016); thus, for

these bacteria, the habitat covariates most relevant for

explaining interassemblage variation may be the traits of

the host fungus, not the traits of the host plant.

Although we have much to learn regarding the distribu-

tion of endophyte biodiversity, patterns observed so far

generally follow the predictions of community ecology

theory and are similar to those observed for metazoan

and plant assemblages (Nemergut et al., 2013; Christian

et al., 2015). For instance, sampling of endophyte assem-

blages recapitulates the positive species–area relation-

ship observed in so many natural systems –as one

samples a larger area, one encounters more taxa

(e.g. Suryanarayanan et al., 2002). A necessary correlate

of this observation is that the similarity among endophyte

assemblages declines with distance, which also has

been demonstrated numerous times (e.g. Davis and Jon-

athan Shaw, 2008; Nemergut et al., 2013; Higgins et al.,

2014; Vacher et al., 2016). Although its causes are multi-

farious and poorly understood (Martiny et al., 2006;

Vellend, 2010), the existence of distance decay suggests

that endophytic microbes are inﬂuenced not only by

deterministic forcings, but also by what are typically

regarded as neutral processes, such as dispersal limita-

tion and ecological drift (Hubbell, 2001; MacArthur and

Wilson, 2001; Nemergut et al., 2013). Also following what

is known for most large, multicellular organisms, foliar

fungal endophyte biodiversity seems to follow a latitudinal

gradient, with a higher diversity at lower latitudes, as

shown by Arnold and Lutzoni (2007). The reasons

for this pattern remain unknown, but likely include both

contemporary and historical drivers (Pianka, 1966;

Mittelbach et al., 2007). Importantly, it is unclear if this

pattern holds for non-fungal taxa and if non-foliar tissues

harbour higher fungal endophyte richness at lower

latitudes. Indeed, ectomycorrhizal fungi appear to be at

their richest in temperate zones (Tedersoo et al., 2014),

which suggests the possibility that other root-associated

microbes may be the richest at intermediate latitudes

as well.

Much of what is known regarding the patterns of endo-

phyte biodiversity demonstrates the inﬂuence of contem-

porary ecological contingencies at either regional or local

spatial scales (i.e. niche determinism). For instance,

Zimmerman and Vitousek (2012) reported greater fungal

endophyte richness at wetter, low elevation sites on a

Hawaiian mountainside, and Bowman and Arnold (2018)

found that Pinus ponderosa hosted more diverse foliar

fungal endophyte communities at mid-to-high elevations

compared with lower elevations in southwestern Arizona

(also see Giauque and Hawkes, 2013; Glynou et al.,

2016; Lau et al., 2013). Furthermore, it is clear that endo-

phyte assemblages shift among coexisting host species

although the effect of host on endophyte assemblage

divergence can be quite modest in some cases (Redford

et al., 2010; Vincent et al., 2016; Grifﬁnet al., 2019).

Although evidence reported to date suggests that many

cultivable endophytes are host generalists (e.g. Arnold

and Lutzoni, 2007; Suryanarayanan et al., 2018), special-

ist endophytes do exist, as demonstrated by the ﬁdelity

of vertically transmitted (seed-borne) Epichloë fungi to

the members of Poaceae (Clay and Schardl, 2002;

Rudgers et al., 2009) and of swainsonine-producing

Alternaria fungi to certain Fabaceous taxa (Cook et al.,

2014; Panaccione et al., 2014). However, the host range

of the myriad endophytes that occur at low relative abun-

dance is unknown (Arnold and Lutzoni, 2007) –an impor-

tant gap in knowledge given that these taxa likely

comprise the bulk of endophyte biodiversity (Arnold and

Lutzoni, 2007; Lynch and Neufeld, 2015).

Even within an individual plant, niche determinism can

shape endophyte assemblages as many studies have

conﬁrmed that endophyte assemblages vary among tis-

sue types (e.g. the endophyte assemblages in roots often

differ from those in leaves; Coleman-Derr et al., 2016;

Haruna et al., 2018; Massoni et al., 2019), though gen-

eral patterns in endophyte richness among tissue types

have not been described.

Niche determinism is not the only force affecting endo-

phyte biodiversity within a particular substrate, though it

is likely the best studied. For instance, it is clear from

research within non-endophytic taxa that microbes can

be dispersal limited, and therefore the longstanding Baas

Becking hypothesis for microbial biogeography, namely

that ‘everything is everywhere, but the environment

selects’(Baas Becking, 1934) is too simplistic (Martiny

Endophyte diversity and distribution 3

et al., 2006; Vellend, 2010; Hanson et al., 2012; Nemergut

et al., 2013). It is still unclear, however, how dispersal limi-

tation and ecological drift (stochastic changes in commu-

nity membership due to aggregated life history events)

shape endophyte community assembly. Similarly, little is

understood regarding the inﬂuence of historical factors,

including divergence and extinction, on endophyte bioge-

ography, though it seems likely that these factors will man-

ifest in differences in endophyte assemblages across

biomes and geographical regions, just as they do for other

taxa (Mittelbach et al., 2007). How often these forces act

at what are, to our sensibilities, small spatial scales, such

as within a forest or even a single-long-lived tree, remains

unknown.

Aﬁnal challenge to the study of endophyte distribution

is the likelihood that most patterns in biodiversity will be

taxon speciﬁc, because taxa respond differently to eco-

logical contingencies and are on varying evolutionary tra-

jectories. For example, Coleman-Derr and colleagues

(2016) suggest that prokaryote taxa are more inﬂuenced

by plant tissue type than fungal taxa, which are affected

more by host habitat and biogeography. At the order

level, Jumpponen and colleagues (2017) suggested that

Helotiales fungal root endophytes are most abundant in

forested ecosystems and Pleosporales fungi are more

common in grasslands. Studies such as these are very

rare; little is known regarding the geographical or host

ranges of endophytes at any level of the biological hierar-

chy –from phylum to subspecies.

Although daunting, the study of endophyte biogeogra-

phy and community assembly will likely provide important

beneﬁts for both basic and applied research. An exem-

plar is provided by Higginbotham and colleagues (2013)

who isolated over 3000 endophytic fungi from numerous

tropical angiosperms and ferns and tested these cultures

against common diseases, including malaria, Chagas

disease and cancer. They report that 30% of the fungi

showed strong activity against at least one of the focal

diseases and that bioactivity against a speciﬁc target was

non-randomly distributed across the fungal phylogeny.

Intriguingly, they also reported a generally higher degree

of bioactivity in taxa sourced from cloud forests compared

with lowland tropical forests –thus providing a biogeo-

graphic road map for natural product discovery in tropical

forests that demonstrates an important role of both biome

and host phylogeny (also see Schulz et al., 2002).

The ﬁrst step towards a working knowledge of endo-

phyte distributions across spatial scales is the description

of broad patterns in their biodiversity. To understand the

scope of relevant research, we scoured the literature and

extracted basic metadata from 596 studies characterizing

endophyte assemblages. Our goal was to synthesize the

metadata from representative studies, with the hopes of

highlighting particular portions of the plant phylogeny and

speciﬁc biomes that need further exploration and to deter-

mine how information could be shared among studies.

Additionally, we paired our survey with a vote-counting

procedure where we compared patterns of endophyte rich-

ness among tissue types. The synthesis process illus-

trated the challenges of pooling information among studies

and, consequently, we offer speciﬁc guidelines for data

sharing and research reproducibility moving forward. For

our purposes in this article, we did not consider obligate

pathogens, epiphytes or mycorrhizae; nor did we include a

review of the large body of literature examining Rhizobia

and their associations with legumes, as others have

already done so (e.g. Peter et al., 1996; Willems, 2006).

Methods

We searched Google Scholar and Web of Science for

the term ‘endophyte’in conjunction with ‘fungal’,‘bacte-

rial’,‘diversity’or ‘community’. All publications in which

the authors characterized endophyte assemblage biodi-

versity were collated. As we were primarily interested in

studies characterizing endophyte biodiversity, we did not

consider research involving manipulative experiments

where no survey of microbial diversity was conducted.

We also made the choice to omit studies that did not dis-

tinguish between epiphytes and endophytes through per-

forming some form of surface sterilization. Searches

were performed periodically from 2016 to 2018, and addi-

tional studies were added to our database as we became

aware of them until the beginning of 2019. We apologize

to those authors whose work we missed and to those

who have published their work in non-English language

journals, which typically did not appear in our searches

and were inaccessible to us because of our linguistic

backgrounds.

From each study, we collected information on host

organism(s) studied, research location(s), tissue type(s)

surveyed and various metadata describing the nature of

the survey conducted –for instance, if the endophyte

assemblage was characterized via sequencing or cultur-

ing, if spatial or temporal replication was employed, host

and culture vouchers deposited, and data made avail-

able. We considered studies spatially replicated if they

involved two or more sampling locations separated by

≥1 km. We chose this threshold because of work by

Higgins and colleagues (2014) who reported rapid dis-

tance decay in endophyte assemblage similarity within

tropical grasses within 1 km. It is likely that the strength

of distance decay depends upon biome, host plant, endo-

phyte taxon and other ecological conditions, thus deter-

mining what constitutes sufﬁcient spatial replication is

challenging and study dependent. We usea1kmthresh-

old here because most studies that were replicated at a

smaller spatial scale were within a single ﬁeld, forest or

4J. G. Harrison and E. A. Grifﬁn

greenhouse and thus were likely exposed to similar

endophyte inoculum, at least over longer timescales. If

the study location was not explicitly provided, we extrapo-

lated an estimate based on the city or country reported

by the authors. We assigned studies to biomes following

the nomenclature of Olson and colleagues (2001). Host

plants collected from urban, agricultural or areas that

were otherwise managed were classiﬁed as coming from

‘cultivated’landscapes and counted independently from

those studies that occurred in unmanaged landscapes

within the same biome. We chose this approach because

managed areas experience ecological contingencies

divergent from their surroundings (e.g. irrigation). We

considered studies of ‘stems’as those involving sampling

of woody branches, twigs or grass shoots. Studies of

‘roots’included any survey of below-ground plant tissue,

but excluded rhizosphere soil surveys and studies, that

did not attempt to surface sterilize roots. We considered

studies of ‘leaves’to be those sampling leaf sections or

whole leaves/leaﬂets (including needles) and did not con-

sider studies that combined petioles with leaf blade

tissue.

To understand the phylogenetic breadth of host plants

surveyed, we calculated the total number of hosts exam-

ined for each plant family and plotted this information on

a phylogeny of the Embryophyta (algal endophyte hosts

were thus omitted from this portion of our analysis)

generated using phyloT (online software accessible

at https://phylot.biobyte.de/). The National Center for Bio-

technology Information taxonomy database was used to

generate the tree (database accessed March 15, 2019;

Federhen, 2012). iTOL v4.3.2 was used for tree visualiza-

tion (Letunic and Bork, 2016). Manipulation of all data

was performed in the R statistical computing environment

(R Core Team, 2019).

Vote counting to determine patterns in relative tissue

richness

In addition, we asked how endophyte richness shifted

among tissue types for both fungi and bacteria. We

attempted two approaches to address this question –afor-

mal meta-analysis and a simple vote-counting approach.

Because few studies used the same methods, comparing

the effect of tissue type on richness among studies was

inappropriate (this limitation also precluded comparison of

richness among taxa or across biomes, unfortunately).

Thus, we only examined those studies that compared rich-

ness among multiple tissue types, and all comparisons

were made within studies.

Unfortunately, very few studies provided data sufﬁcient

for a quantitatively rigorous meta-analysis (see Methods

and Results in Data S1; Viechtbauer, 2010), so we con-

ducted a simple vote-counting procedure where we

considered each study independently and ranked tissue

types by the relative richness reported in that study. We

only considered those studies that examined multiple tis-

sues and that standardized sampling effort among tis-

sues. In total, we examined 243 studies: 182 studies of

fungal endophytes and 61 studies of bacterial endo-

phytes. After ranking tissues by relative richness sepa-

rately for each study, we calculated, across studies, the

proportion of times one tissue type had higher richness

than another tissue (e.g. for what proportion of studies

did leaves have higher richness than roots) and calcu-

lated the probabilities of these proportions using a bino-

mial sign test (Cooper and Hedges, 1993). This test is

simply the probability of observing a particular number, or

more, of positive outcomes (in our case, one tissue type

having higher richness than another), given a certain

number of trials and assuming equal probability of posi-

tive and negative outcomes. For this vote-counting

approach, we focused on richness because fewer studies

reported diversity metrics and, when not explicitly

reported by authors, relative richness was simpler to cal-

culate and extract from published summary tables and

ﬁgures than were diversity entropies. To test how growth

habit inﬂuenced relative microbial richness among tis-

sues, we conducted vote counting separately for studies

of hosts with the following growth habits: woody-stemmed

trees and shrubs, forbs and graminoids.

Results

Our survey highlighted the breadth of the endophyte bio-

diversity literature, as we extracted data from 596 unique

publications. We report that interest in endophyte diver-

sity is on the rise, with a sharp increase in studies per

year since 2010 (Fig. 1). Fungi have received compara-

tively more attention than bacteria, though this disparity

is diminishing (Figs. 1 and 2E). The majority of studies

were of foliar endophytes (1694 unique combinations of

study and host species), followed by root (577 combina-

tions) and stem (540 combinations) endophytes. By com-

parison, ﬂoral tissues (39 combinations) and plant

propagules were understudied (172 combinations; Fig. 2).

Multiple host studies were not the norm –approximately

66% of studies focused on a single host taxon.

The global extent of endophyte biodiversity research

The geographical range encompassed by the studies we

considered was global; endophytes, both fungal and bac-

terial, have been recovered from hosts across all major

biomes (Fig. 3). Temperate mixed coniferous and decidu-

ous forests were the best studied with 96 studies (16% of

total). However, the most unique combinations of host

and study were reported from tropical and subtropical

Endophyte diversity and distribution 5

wet forests (471, 21% of total). This was due to several

studies that surveyed many hosts within these forests

(e.g. Rojas-Jimenez et al., 2016 with 92 hosts and

Suryanarayanan et al., 2011 with 70 hosts). In terms of

unique studies, research in tropical and subtropical for-

ests composed a more modest 13% of studies in our sur-

vey. Many biomes were quite understudied. For instance,

50 or fewer studies (in terms of unique host by study

(a)

(c)

(d) (e)

(b)

Fig. 2. Summary of 596 publications characterizing endophyte biodiversity. Because many studies surveyed multiple hosts, we report both the

number of studies and number of unique host by study combinations.

A–C. The number of studies surveying each plant compartment (A), biome (B) and host life history category (C; values in parentheses are unique

hosts).

D. Information pertaining to study design and reproducibility.

E. The endophytic taxon characterized and the methodology employed.

6J. G. Harrison and E. A. Grifﬁn

combinations) were conducted in 7 of the 17 biomes that

we considered (Fig. 2B). Overall, studies from these

biomes composed only 7% of those surveyed.

Across biomes, we found comparatively few studies of

hosts growing in obvious wilderness, far from human

development. Indeed, 33% of studies relied on hosts

grown in cultivated environments, including urban loca-

tions, agricultural landscapes and greenhouses (with uni-

versity campuses being particularly well sampled). This

estimate may be conservative as for some studies the

exact collection location was difﬁcult to determine and so

we did not include them in the ‘cultivated’category, but

sampling was likely not far from human development.

Much of the host phylogeny remains unsampled

The studies we surveyed encompassed 1702 unique taxa

from 254 plant families. Poaceae was by far the most well-

studied family (189 hosts studied), followed by Fabaceae

(98 hosts), Pinaceae (82 hosts) and Asteraceae (79 hosts;

Fig. 4). In the studies we examined, fungal endophytes

have been surveyed in hosts from 30% of plant families

listed in the NCBI taxonomy database for Embryophyta.

By comparison, bacterial endophytes have been charac-

terized in only 10.5% of plant families. Of particular note,

very few observations of foliar microbiota have been made

among bryophyte and pteridophyte families (Fig. 4; Davis

and Jonathan Shaw, 2008; Alessandro et al., 2013). Addi-

tionally, we observed a mismatch between host family

species richness and sampling effort. For instance, only

39 Orchidaceae species have been surveyed out of the

approximately 28,000 accepted orchid taxa occurring

worldwide (Chase et al., 2015; Kew and Missouri Botani-

cal Gardens, 2019).

Replication and reproducibility could be improved

We also characterized details for each study regarding

sampling scheme and reproducibility (Fig. 2D and E).

We found that just over half of studies were spatially

replicated (sampling areas were separated by at least a

kilometre) and fewer than a quarter of studies were tem-

porally replicated. The majority of studies (~74%) relied

on culturing; however, only about a third of these studies

reported accessioning cultures (Fig. 2E). By compari-

son, 72% of studies that relied on sequence data pro-

vided clear instructions for downloading raw data,

though only 23% of these studies provided processed

data [such as an operational taxonomic unit (OTU)

table]. Surprisingly, fewer than 20% of studies men-

tioned accessioning host vouchers. For cultivated plants,

we considered a description of the cultivar as equivalent

to an accessioned voucher.

Mangroves

Trop. dry forests

Flooded grasslands

Temp. coniferous

Trop. wet forests

Desert

Trop. grasslands

Montane grass/shrublands

Temp. decidous/mixed forests

Temp. grasslands

Boreal forests

Tundra

Ice

Meditteranean

Freshwater

Uncultivated

Cultivated

Fig. 3. Locations of studies considered. An interactive, zoomable version of this map can be found at https://jharrisonecoevo.github.io/

EndophyteMap/. Black points represent studies of cultivated crops and managed landscapes, purple points represent studies of uncultivated

plants in unmanaged settings. Biomes are colour coded and delineated in accordance with Olson and colleagues (2001). In some cases, multi-

ple, proximal locations were surveyed and a single point was used to graphically represent these locations. If a study did not provide exact loca-

tion information, then study location was approximated.

Endophyte diversity and distribution 7

The effects of tissue type on endophyte richness and

diversity

We performed vote counting to compare the relative rich-

ness and diversity of fungal endophyte assemblages in

varying tissue types across plant taxa. We resorted to

vote-counting procedure because data were insufﬁcient

for a robust meta-analysis (see Methods and Results in

Data S1). We found that relative tissue richness was

dependent upon host growth habit. For instance, stems

had richer fungal endophyte assemblages than leaves for

woody-stemmed hosts, but this pattern was not observed

for either forbs or graminoids (Table S1). By comparison,

for graminoids, roots had richer fungal and bacterial

endophyte assemblages than stems (Table S3). For

forbs, no tissue type was clearly richer, on average, than

other tissues (Table S2). Additionally, for fungal endo-

phytes, we found that reproductive structures, including

ﬂowers and propagules, were relatively species poor,

while bark was species rich (Tables S1 and S2), though

these results are quite tentative given the few studies that

compared endophyte assemblages in these tissues to

those in other portions of the plant corpus.

Discussion

We report that endophyte biodiversity has been studied

within all major biomes and continents (even Antarctica,

if one counts King George Island; Fig. 3; Rosa et al.,

2009). Given that widespread interest in endophytes did

not occur until the 1970s, progress has been rapid. How-

ever, great swathes of the globe still remain unsurveyed.

Certain biomes have been particularly understudied –

either due to their high biodiversity, which makes thor-

ough sampling exceptionally difﬁcult (i.e. tropical

rainforests); large geographical area (e.g. the boreal for-

est); or because they are geographically restricted and

simply have not received much attention. For instance,

we found few studies from coastal dunes, ﬂooded grass-

lands and mangrove forests. These habitats are chal-

lenging for plants due to salinity, short intervals between

disturbances and the presence of anoxic soil. Surveys of

understudied biomes will help deﬁne the scope of endo-

phyte biodiversity and functional traits. In particular, we

suggest that surveys in ﬂooded grasslands and man-

groves may improve our understanding of archael endo-

phyte biodiversity (Moissl-Eichinger et al., 2018), as this

120

100

Hornworts

(307 ,44)

(73 ,16)

(234,92)

(159,27)

(73,86)

(33,3)

(136,53)

(154,51)

(19,1)

(2,3)

Number of unique hosts surveyed

Bacterial endophytes Fungal endophytes

Bar length proportional to number of hosts.

Concentric rings at intervals of 20 hosts.

Pinaceae

Poaceae

Fabaceae

100

120

Lycophytes

Gymnosperms

Asteraceae

(27,0)

(1684,325)

(100,0)

(26,1)

(27,1)

(108,8)

(1396,315)

Fig. 4. Survey effort across Embryophyta. Number of studies surveying fungal (blue) and bacterial (red) endophytes are shown extending out-

wards from the tips of the phylogeny. Tips are families. Notable taxa within Embryophyta are labelled and colour coded.

Numbers in parentheses denote unique hosts surveyed. Very few surveys of bacterial endophytes have been conducted in bryophyte hosts;

therefore, this portion of the ﬁgure has been abbreviated to aid visualization. An interactive, zoomable version of this phylogeny can be found at

https://itol.embl.de/shared/harrisonjg.

8J. G. Harrison and E. A. Grifﬁn

branch of life includes numerous halophiles and other

extremophiles that may be able to cope with the abiotic

conditions characteristic of those locations. Similarly, stud-

ies in desert and alpine biomes may uncover endophytes

with unique mechanisms for coping with the severe ultravi-

olet exposure, temperature swings and desiccation that

occurs in such harsh habitats (see e.g. Lopez et al., 2011;

Massimo et al., 2015; Sangamesh et al. 2018).

We also reported a lack of studies from Africa, west

and north Asia, and the interiors of Australia and South

America (Fig. 3). These areas hold some of the most bio-

diverse and charismatic landscapes on the planet; for

instance, the Congo basin is the second largest tropical

rainforest in the world, with thousands of endemic plant

taxa (Brenan, 1978; Linder, 2001), and it has historically

experienced less deforestation than other rainforests

(Koenig, 2008). Similarly, the Cape Floristic province in

Africa has some of the highest levels of plant endemism

in the world. Because these regions have evolutionary

histories that have facilitated endemism, it seems likely

that they harbour unique endophyte taxa and would be

prime locations to study coevolution and codivergence

between plants and endophytes. More generally, the lack

of sampling outside of North American, Europe and por-

tions of Asia precludes a robust knowledge of endophyte

biogeography.

The inﬂuence of human development on endophyte

biodiversity

We acknowledge the logistical challenges of sampling the

remote locations that remain understudied. Indeed, we

report an imprint of this challenge in even relatively well-

studied regions, where we found that most studies were

conducted near roadways, townships and other human

development. The lack of sampling in wilderness areas

likely biases our nascent understanding of endophyte biodi-

versity. Human development is associated with pollution,

habitat fragmentation, ecosystem disturbance frequency

and the abundance of introduced hosts (Dietz et al., 2007;

Crowl et al., 2008) –all of which likely affect plant

microbiomes. Evidence for this hypothesis is sparse; how-

ever, Laforest-Lapointe and colleagues (2017a) reported

many phyllosphere bacterial taxa shift in relative abundance

along an urbanization gradient, with an overall decline in

dominant Alphaproteobacteria with more urbanization. Simi-

larly, Lappalainen and colleagues (1999) reported a decline

in endophyte colonization of Betula trees with proximity to

a copper–nickel smelter. Variation in heavy metal concen-

trations (Jurc et al., 1996; Tóth et al., 2009), acid rain

(Helander et al., 1994) and air pollution (Wolfe et al., 2018)

have all been associated with shifts in endophyte assem-

blages –thus, it seems likely that the effects of pollution

and urbanization are multifarious and have effects that

depend upon the endophytic taxon examined and the eco-

logical context.

In addition to pollution, habitat fragmentation also

increases in proximity to human development. Very little

is known regarding how habitat fragmentation affects micro-

bial assemblages or, more generally, how metacommunity

processes manifest within microbiomes (Christian et al.,

2015). However, classic island biogeography theory

(MacArthur and Wilson, 2001) suggests that human-caused

habitat fragmentation likely shapes endophyte assem-

blages through determining proximity to inoculum sources.

In a survey spanning islands of various sizes, Helander

and colleagues (2007) reported that endophyte colonization

of Betula spp. trees was greater on larger islands and

islands closer to the mainland (also see Oono et al., 2017).

This result, coupled with work documenting dispersal limita-

tion in non-endophytic microbial systems (Andrews et al.,

1987; Peay et al., 2007; 2010; Golan and Pringle, 2017),

suggests that it is reasonable to expect variation in

endophyte assemblages routinely follows the predictions of

island biogeography, regardless of whether habitat frag-

mentation and patch size are caused by geological pro-

cesses or human inﬂuence.

Another way in which endophyte assemblages may be

affected by proximity to human development is through the

inﬂuence of invasive plant taxa, which are often much more

abundant near development than in wilderness areas.

Invasive host taxa could inﬂuence endophytes in a variety

of ways –from changing the inoculum pool within an area

(i.e. ‘neighbourhood’effects; Moeller et al., 2015), bringing

along endophyte taxa or genotypes from the ancestral

range of the host (Dickie et al., 2017), or affecting many

other aspects of the local ecology [e.g. shifting ﬁre regimes

(Brooks et al., 2004), determining litter deposition rate and

elemental composition (Allison and Vitousek, 2004),

inﬂuencing herbivore assemblages (Forister, 2009), etc.].

Interestingly, the few studies we encountered that

surveyed endophytic microbiomes of invasive plants in

both their native and invaded ranges found that endophyte

assemblages differed between ranges. For instance, Lu-

Irving and colleagues (2019) report reduced richness in

phyllosphere and endophytic root bacteria in the invaded

portion of the range of Centaurea solstitialis compared

with the native range. Similarly, Shipunov and colleagues

(2008) report a wholesale shift in the fungal endophyte

assemblage within the leaves of Centaurea stoebe in

invaded versus native portions of its range. Thus, the biodi-

versity of endophytes within widespread, invasive plants is

also inﬂuenced by host invasion history (also see Gundale

et al., 2016; Sikes et al., 2016; Taylor et al., 1999).

All of these anecdotes support the idea that endophyte

assemblages in relatively undisturbed areas, such as

portions of the Amazon or the Siberian forest, are likely

to be different from those in conspeciﬁc hosts growing

Endophyte diversity and distribution 9

near human habitation or that are being actively culti-

vated and thus remote locations should be the focus of

further study. Even if different microbial taxa are not

observed in less disturbed environments, the study of the

shifts in relative abundances among endophyte assem-

blages along urbanization and pollution gradients could

provide insight into how endophytes interact and commu-

nities assemble (e.g. Gazis and Chaverri, 2015).

Much of the host phylogeny remains unexplored: what

might we be missing?

We found that members of about a third of plant families

have been surveyed for fungal endophytes and only

about a tenth of plant families are represented among

studies characterizing bacterial endophyte assemblages.

These results suggest we may be missing a large portion

of endophyte biodiversity. It is true that many cultivable

endophytic taxa are known to have broad host ranges

(e.g. Arnold and Lutzoni, 2007; Suryanarayanan et al.,

2018), thus one could argue that an understanding of

endophyte biodiversity does not hinge on thorough sam-

pling of potential host taxa. However, we note that, in the

majority of multivariate studies of endophyte biogeogra-

phy, host taxon is a supported predictor of assemblage

variation (Grifﬁnet al., 2019; Kivlin et al., 2019) –albeit a

sometimes modest one (Vincent et al., 2016). Moreover,

little is known regarding the host range of those rare

endophyte taxa that compose the bulk of most assem-

blages (Arnold and Lutzoni, 2007).

Studies delineating host range are desperately needed

to understand endophyte distributions and biodiversity;

however, given the daunting nature of the sampling

required, where then should we begin? We suggest

targeting those plant lineages with unique traits, such as

production of unusual secondary metabolites or prefer-

ences for restricted or harsh habitats (e.g. halophiles and

extremophiles). As an example, certain Astragalus taxa

can hyperaccumulate selenium, and recent research has

suggested that these plants may harbour unusual endo-

phytic taxa that could inﬂuence selenium uptake (Sura-de

Jong et al., 2015; Lindblom et al., 2018, 2013). Following

a similar rationale, we also suggest surveying those

plant families that are phylogenetically distinctive. If

coevolution or codivergence has occurred between hosts

and their endophytes, then unusual endophytic taxa

could occur in hosts from remote portions of the plant

phylogeny (Hassani et al., 2019). Non-vascular plants, in

particular, deserve more attention, as these plants have

different evolutionary histories, physiology, growth habits

and preferred habitats than vascular plants (Huang

et al., 2018).

An additional justiﬁcation for surveying broadly across

the plant phylogeny is the discovery of specialist

endophyte taxa. Surveys of seeds, in particular, could lead

to the discovery of more specialist vertically transmitted

endophytes (class I and II endophytes sensu Rodriguez

et al., 2009), which are particularly interesting because of

their capacity to inﬂuence their hosts during early ontogeny

(e.g. Hodgson et al., 2014; Truyens et al., 2015; Gundel

et al., 2017). An individual seed generally contains a very

species poor endophyte assemblage (e.g. in many cases

only a single fungus can be isolated from seeds, see,

Hodgson et al., 2014; Newcombe et al., 2018; Shipunov

et al., 2008), and relatively few instances of vertical trans-

mission of endophyte taxa have been documented. How-

ever, recent work by Hodgson and colleagues (2014)

provides evidence that vertical transmission of fungi may

occur much more often than previously suspected (also

see a review on bacterial seed endophytes by Truyens

et al., 2015). Indeed, while the well-known clavicipitaceous

endophytes seem to be limited to members of the Poaceae

(Rudgers et al., 2009), the occurrence of vertically transmit-

ted endophytes capable of systemic growth has been

documented from throughout the plant phylogeny, including

within members of the Asteraceae (Hodgson et al., 2014),

Araliaceae (Soares et al., 2016), Convulvulacea (Cook

et al., 2013), Ericaceae (Rayner, 1915), Fabaceae (includ-

ing members of Astragalus, Oxytropis and Swainsona,

Cook et al., 2009, 2014; Grum et al., 2013), Papaveraceae

(Hodgson et al., 2014) and Plantaginaceae (Hodgson

et al., 2014). This suggests that facultative vertical trans-

mission may occur in numerous plant hosts and across

many biomes. Cross-biome comparative studies of the

seed microbiome could determine whether vertical trans-

mission is more common in certain habitats, as might be

predicted if these endophytes interact mutualistically with

their hosts to ameliorate the negative effects of particular

abiotic conditions (Afkhami et al., 2014; Gundel et al.,

2017; Semmartin et al., 2015).

The effects of tissue type on endophyte assemblages

Our vote-counting approach suggested that in woody

plants stems had higher richness than other tissues for

both fungi and bacteria. However, for graminoids, roots

were the richest tissue, and for forbs, intertissue patterns

in richness were less clear (Tables S1–S3). These

results suggest that tissues with greater lifetime inocula

exposure have the highest richness across plant life

histories. This hypothesis is supported by several studies

that have demonstrated that older leaves typically har-

bour richer microbial assemblages than younger leaves,

presumably because of greater exposure to inoculum

and increased time for microbial growth (Ercolani, 1991;

Arnold et al., 2003). Stems and bark of woody plants are

exposed to inocula in air, water and dust year round and

have long lifespans (indeed much bark is dead and can

10 J. G. Harrison and E. A. Grifﬁn

remain on the trunk for a lengthy period of time), whereas

leaves, even for evergreen trees, do not persist for nearly

as long. Similarly, roots are the longest-lived tissues of

many perennial forbs and graminoids, as above-ground

tissues of these hosts often senesce annually. It is true

that roots of woody-stemmed plants can be quite long

lived; however, roots are primarily encountering inoculum

from the surrounding soil matrix, thus it is possible that

there is greater variation in the inoculum encountered by

stems than by roots over the lives of those tissues. Alter-

natively, perhaps the resources available to microbes

within stems of woody plants favour higher richness com-

pared to leaves, particularly of latent saprotrophs that

catabolize lignin or other structural carbohydrates (Oses

et al., 2006, 2008). These hypotheses are not mutually

exclusive and await experimental testing.

Our survey comes with several caveats. First, it is pos-

sible that the efﬁcacy of surface sterilization may vary

with tissue type; thus, for instance, the high fungal rich-

ness in bark that we report could be because it was more

difﬁcult to surface sterilize than other tissues. Also, while

we chose those studies that had the same sample size

(in terms of replicates) between each tissue type, it was

not always apparent that the same mass was used for

each sample. Additionally, both culture and sequence-

based surveys suffer from taxonomic biases (Nilsson

et al., 2019; Carini, 2019) and if those biases coincide

with taxonomic variation among tissue types, then rich-

ness estimates will be incorrect. Nevertheless, our analy-

sis demonstrates the existence of clear patterns in

richness among tissue types and suggests several

hypotheses for those patterns that deserve further study.

How can we best share information among studies?

We report several challenges that impede meta-analysis

and synthesis of the endophyte literature (e.g. Meiser

et al., 2014). Most importantly, raw and processed

sequence data were not always available. Moreover, it

was quite rare for sufﬁcient detail to be provided regard-

ing sequence processing –including options and ver-

sions for software used and date accessed for taxonomy

training databases, which are in constant ﬂux. Given the

challenge in reprocessing data and the inﬂuence different

bioinformatic pipelines can have on results (e.g. Pauvert

et al., 2019), we suggest that publication of polished data

and scripts should be considered to facilitate information

sharing among studies. Those data that would be most

amenable to meta-analysis include replicate by taxon

tables, sequences of OTUs or exact sequence variants,

and the taxonomic hypotheses for those sequences.

In many cases, meta-analysis will require substantial

reprocessing of the data, so raw data should also be

made available.

Additionally, we suggest that authors consider depositing

vouchers of host taxa studied, nucleic acids extracted or

cultures obtained in an herbarium whenever possible

(Fig. 2D). This suggestion is motivated, in part, by fascinat-

ing new work by Daru and colleagues (2019) who have

shown that endophytes within herbarium specimens can

be sequenced, and, in some cases, even cultured. Thus,

vouchers could act as ‘time capsules’that preserve endo-

phyte genotypes and could afford insight into endophyte

evolution and shifts in host and geographic range over

time. To best share information among vouchers, standard-

ized protocols (such as drying time and temperature) could

be helpful to adopt, though we acknowledge the challenge

of implementing such standards during ﬁeld collection.

Deposited cultures could provide many of the same bene-

ﬁts as host vouchers, but would also allow researchers

to grow endophytes of interest to meet various experimen-

tal goals (Huang et al., 2018; Suryanarayanan, 2019).

Finally, the plant taxonomy is ever-changing, thus as future

researchers interpret published work, they may wish to

examine accessions to determine the most current taxo-

nomic placement of the focal host or endophyte. In sum,

we see herbaria as tremendous resources for the study of

the plant microbiome, and consequently, we urge participa-

tion in their continued development.

Conclusions

To understand the evolutionary forces and ecological

pressures that shape endophyte assemblages, the delin-

eation of patterns in endophyte biodiversity across spatial

scales and the host phylogeny is required. The enthusi-

asm among microbial ecologists for endophyte biology

paired with the tools we now have at our collective dis-

posal suggests that description of such patterns is within

grasp. We hope that our survey inspires others to ﬁll the

gaps in knowledge that we report. To that end, we have

made the metadata from each study that we consider

available in hopes that other researchers mine them for

additional insights.

Acknowledgements

Thanks go to Lyra Beltran for assistance extracting data

from publications. This review was inspired by conversations

with Betsy Arnold, to whom we offer our thanks. We appreci-

ate comments from Leho Tedersoo and two anonymous

reviewers that led to a much improved manuscript. JGH was

supported by the National Science Foundation EPSCoR grant

1655726. EAG was supported by a Smithsonian Institution

Secretary’s Distinguished Research Fellowship, as well as

a Smithsonian Environmental Research Center Postdoc

Research Fellowship, the Maryland Native Plant Society, the

Washington Biologists Field Club and The New Mexico Idea

Network of Biomedical Research Excellence (NM-INBRE),

Endophyte diversity and distribution 11

and an Institutional Development Award (IDeA) from the

National Institute of General Medical Sciences of the National

Institutes of Health.

Author contributions

J.G.H. and E.A.G. conducted the literature survey and

wrote the manuscript.

Data availability

All scripts and processed data are available at: https://

bitbucket.org/harrisonjg/endophytereview/src/master/. For

collated metadata from examined studies see: https://

docs.google.com/spreadsheets/d/1hNzPz7Uteto7WiLoEd

FryonUMfa0nGU_7zNsejCWZPQ/edit?usp=sharing.

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Supporting Information

Additional Supporting Information may be found in the online

version of this article at the publisher’s web-site:

Fig. S1 Differences in fungal endophyte richness among

host tissues as determined through meta-analysis. Each

panel depicts pairwise comparisons between two tissue

types. Panel (a) depicts leaves versus roots, panel

(b) leaves versus stems and panel (c) roots versus stems.

Mean differences between tissues for each study are shown

in the right margins of each plot, with conﬁdence intervals.

No model was signiﬁcantly supported at p≤0.05. Results

were very similar for Shannon’s diversity, which can be seen

in Fig. S2. Richness for Unterseher et al. (2018) was higher

than the other studies because those authors relied on

sequencing data whereas the other studies considered relied

on culturing data. Two hosts were studied by Granzow and

colleagues (2017) and results from each host are denoted

by letters a and b.

Fig. S2 Differences in fungal endophyte diversity

(exponentiated Shannon’s entropy) among host tissues as

determined through meta-analysis. Each panel depicts

pairwise comparisons between two tissue types. Panel

(a) depicts leaves versus roots, panel (b) leaves versus

stems and panel (c) roots versus stems. Mean differences

between tissues for each study are shown in the right mar-

gins of each plot, with conﬁdence intervals. Results were

very similar for richness, which can be seen in Fig. S1.

Diversity for Unterseher and colleagues (2018) was higher

than the other studies because those authors relied on

sequencing data whereas the other studies considered relied

on culturing data. Two hosts were studied by Granzow and

colleagues (2017) and results from each host are denoted

by letters a and b.

Data S1 Meta-analysis methods and results

Table S1 Differences among host tissues in fungal (top

panel) and bacterial (bottom panel) endophyte richness in

woody plants. Each cell in the table provides the number of

times the tissue type on that row (the focal tissue) had

higher richness than the tissue type in that column (the com-

parison tissue) followed by the number of studies reviewed

for each comparison in parentheses. Signiﬁcance was deter-

mined using a binomial sign test. For results from herba-

ceous plants see Table S2, for results from graminoids see

2018Table S3

Table S2 Differences among host tissues in fungal (top

panel) and bacterial (bottom panel) endophyte richness in

herbaceous plants. Each cell in the table provides the num-

ber of times the tissue type on that row (the focal tissue) had

higher richness than the tissue type in that column (the com-

parison tissue) followed by the number of studies reviewed

for each comparison in parentheses. Signiﬁcance was deter-

mined using a binomial sign test. For results from woody

plants see Table 2017S1, for results from graminoids see

Table S3

Table S3 Differences among host tissues in fungal (top

panel) and bacterial (bottom panel) endophyte richness in

graminoids. Each cell in the table provides the number of

times the tissue type on that row (the focal tissue) had

higher richness than the tissue type in that column (the com-

parison tissue) followed by the number of studies reviewed

for each comparison in parentheses. Signiﬁcance was deter-

mined using a binomial sign test. For results from woody

plants see Table S1, for results from forbs see Table S2

Endophyte diversity and distribution 17

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Long-Distance Dispersal of Fungi

Chapter

Sep 2017

The diversity and distribution of endophytes across biomes, plant phylogeny, and host tissues—how far have we come and where do we go from here?

Abstract

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