hidden fungi, emergent properties: endophytes and...

PY49CH15-Bayman ARI 8 July 2011 9:17

Hidden Fungi, EmergentProperties: Endophytesand MicrobiomesAndrea Porras-Alfaro1,2 and Paul Bayman3

1Department of Biology, Western Illinois University, Macomb, IL 61455;email: [email protected] of Biology, University of New Mexico, Albuquerque, NM 871313Department of Biology, University of Puerto Rico-Rıo Piedras, San Juan, Puerto Rico00931-3360; email: [email protected]

Annu. Rev. Phytopathol. 2011. 49:291–315

The Annual Review of Phytopathology is online atphyto.annualreviews.org

This article’s doi:10.1146/annurev-phyto-080508-081831

Copyright c© 2011 by Annual Reviews.All rights reserved

0066-4286/11/0908/0291$20.00

Keywords

dark septate endophyte, latent pathogen, microbiome, mycobiome,mycorrhiza, systems biology

Abstract

Endophytes are microorganisms that live within plant tissues withoutcausing symptoms of disease. They are important components of plantmicrobiomes. Endophytes interact with, and overlap in function with,other core microbial groups that colonize plant tissues, e.g., mycorrhizalfungi, pathogens, epiphytes, and saprotrophs. Some fungal endophytesaffect plant growth and plant responses to pathogens, herbivores, andenvironmental change; others produce useful or interesting secondarymetabolites. Here, we focus on new techniques and approaches that canprovide an integrative understanding of the role of fungal endophytesin the plant microbiome. Clavicipitaceous endophytes of grasses arenot considered because they have unique properties distinct from otherendophytes. Hidden from view and often overlooked, endophytes areemerging as their diversity, importance for plant growth and survival,and interactions with other organisms are revealed.

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Endophyte:a symbiotic organism(usually a bacterium orfungus) that liveswithin plant tissueswithout causingsymptoms of disease

Systems biology:interdisciplinaryapproach to study thecomplex interactionsof biological systemsand emergentproperties that resultfrom them

INTRODUCTION

Our work as scientists is often reductionist. Totest a hypothesis about the pathogenicity of aparticular fungus on a particular plant, for ex-ample, we need an experiment in which the onlyvariables are the things we want to test. Otherfactors are carefully controlled, and if they can’tbe controlled, often ignored. This tight focus isnecessary to test our hypothesis, but it can makeus forget the tremendous complexity of biolog-ical systems.

We think of plants as organisms. However,all plant pathologists know that each plant is infact a complex community and that every plantin a natural or agricultural setting is colonizedby a diversity of microbes, both on its outerand inner surfaces. Endophytes, organisms thatlive inside plant tissues, are part of the microbialcommunity of every plant. It is not always clear,however, if and how these microbial communi-ties affect plant health and function.

Anton de Bary, the German botanist whois considered the father of plant pathology,coined the term endophyte in 1886 to describemicroorganisms that colonize internal tissues ofstems and leaves (169). This definition was laterrevised to specify that infections caused by en-dophytes are asymptomatic, that roots as well asshoots may be colonized, and that an endophytemay not remain an endophyte throughout its

Endophytefunctional groups

Dormantpathogens

DormantsaprobesMycorrhizal

Protectiveagents

Heat

Stress Insects

PathogensDrought

Figure 1The mycobiome. As part of a fungal community, endophytic fungi may haveone or multiple functional roles during their life cycles or in reponse to plant orenvironmental cues.

life cycle. This broad definition implies thatin addition to mutualistic and commensalisticsymbionts, endophytes could include latentpathogens, latent saprotrophs, and early stagesof colonization by mycorrhizal fungi and rhizo-bia (Figure 1). Functional mycorrhizal fungi,however, are explicitly excluded, as they arespecialized for nutrient transfer from sourcesoutside of the root (24) and are phylogeneti-cally distinct from most groups of endophytes(9, 123). The term endophyte is thus defined bylocation and does not address the nature of therelationship with the plant, unlike mycorrhiza,which specifies a functional relationship.

The potential importance of endophyticfungi became clear in 1975, when CharlesBacon discovered that endophytes of pasturegrasses in the family Clavicipitaceae were toxicto cattle (13). Subsequent work showed thatboth the endophytes and the associated toxicitysyndromes were widespread, with an estimatedcost of $600 million a year to the livestockindustry (77). Clavicipitaceous endophytes ofgrasses (i.e., systemic endophytes in the fam-ily Clavicipitaceae) are one of the most inter-esting and economically important examples ofplant-fungal interactions, and they have beenstudied from many perspectives. Although theyhave inspired much of the research on endo-phytes, they raise expectations of mutualism,functional significance, and coevolution that areoften unjustified when applied to other groupsof endophytes (14, 42, 124).

Plant-associated fungi are usually dividedinto five main functional groups: mycorrhizal,pathogenic, epiphytic, endophytic, and sapro-trophic fungi (Figure 1). Most studies focus ononly one of these groups, and few consider in-teractions among them, or between fungi andbacteria. In this review, we summarize exam-ples that show the functional importance of en-dophytes. We also argue for the urgent neces-sity to use more integral approaches to studyplant-associated microbial communities. Sys-tems biology approaches are emphasized be-cause they are providing dramatic new insightsinto microbial ecology. We focus on a simplequestion: Are fungal endophytes of sufficient

292 Porras-Alfaro · Bayman

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ITS: internaltranscribed spacer

CO1: cytochrome coxidase subunit I

BLAST: Basic LocalAlignment SearchTool

practical importance to warrant the attentionof plant pathologists, ecologists, and plant bi-ologists in general?

Extensive literature is available on the biol-ogy and diversity of endophytes. In this review,we try (as much as possible) to avoid repeat-ing topics covered in previous review articles.Clavicipitaceous endophytes of grasses are ex-cluded from this review because they have spe-cial characteristics and have been reviewed ex-tensively in multiple papers and books (19, 31,130, 153).

METHODS: CULTURINGVERSUS DIRECTAMPLIFICATIONAND DETECTION OFENDOPHYTIC FUNGI

Until recently, most studies on endophytes in-volved first isolating organisms into pure cul-ture in order to identify them. This means thatspecies that do not grow or grow very slowly inculture media were overlooked, and species thatgrow well in culture were over-represented.This bias can be corrected by direct ampli-fication of DNA from surface-sterilized plantmaterial [also called environmental PCR (poly-merase chain reaction)]. However, unlike bac-teria, where only one percent of species in somecommunities are culturable (45), it appears thata relatively high proportion of fungi can begrown in culture. In a study designed to test thedifferences between culturing and direct ampli-fication, more species of endophytes were re-vealed by direct amplification, but more ordi-nal level groups were revealed by culturing (9).Some taxa appeared more diverse with directamplification, but others appeared more diversewith culturing. Direct amplification studies willprobably reveal major new lineages of fungi, butthe best strategy is to use a combination of bothmethods (18).

For both culturing and direct amplification,a number of methodological issues make it dif-ficult to compare results among studies. Mor-photypes are often used as a proxy for species,but this method may overestimate diversity:

Sphaeropsis sapinea, an endophyte of Pinus sp.,has more than five different morphotypes inculture (26, 132). Methodological factors in-cluding surface sterilization, sample size, andtime of collection can all affect which endo-phytes are isolated. Also, many studies are im-precise about sampling strategies in terms of thenumber of plants sampled and number and sizeof samples per plant (18, 53).

For DNA-based approaches, primer and ex-traction methods can introduce bias, and thereis still no consensus on defining a universal bar-code region for fungal diversity studies. Theinternal transcribed spacer (ITS) of nuclear ri-bosomal DNA (rDNA) is likely to become theofficial barcoding region for fungi (107), butother regions, such as CO1 (cytochrome c ox-idase subunit I) and multilocus barcodes, arestill being investigated (131, 141). Other unre-solved issues include defining cut-off percent-ages for BLAST (Basic Local Alignment SearchTool) searches or methods for identificationat the species level (7), and how to controlfor misidentified sequences in public databases(108). Lack of cohesion in the research com-munity has prevented a consensus on these is-sues, another reason why an integrated pictureof endophyte diversity and distribution remainselusive.

Quantifying fungal biomass in plant tissuesis also problematic. Real-time PCR techniquesvary greatly depending on the type of fungus aswell as cell size, number, and type, and requireextensive calibration for each species using purecultures (158). They usually focus on one or afew taxa and are unwieldy for studies of micro-bial communities. Concentration of ergosterol,a sterol characteristic of fungal membranes, isanother way to measure fungal biomass in planttissues, but it does not distinguish among fungaltaxa (110).

METHODS: MICROBIOMES ANDSYSTEMS BIOLOGY APPLIED TOENDOPHYTIC FUNGI

Next-generation sequencing technologies andsystems biology allow simultaneous exploration

www.annualreviews.org • Endophytes and Microbiomes 293

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Plant-associated microbiomes(systems biology approach)

Plant-microbiomeinteractions

RNAi, Qdots, andmicroarrays formodel systems

‘Omics approaches to studymicrobial community functions

Metagenomics,transcriptomics, proteomics,

and metabolomics

Diversity and changes incommunity structure

Targeted studies of ITS rDNAfor fungi, 16S for bacteria, or

specific functional genes

Models that predict response of plant-fungalsystems to environmental change and the

roles of endophytic functional cores on planthealth and function

Figure 2A strategy for more inclusive and integrative studies of plant microbiomes.

Metagenomics: thestudy of nucleic acidsextracted fromenvironmental DNAsamples, including allorganisms therein

of all members of microbial communities andtheir interactions, not just interactions betweenpairs of organisms (40) (Figure 2). Most studieson plant microbiomes have focused on a singlegroup (e.g., endophytic or epiphytic fungi,endophytic or epiphytic bacteria, pathogenicfungi or bacteria, mycorrhizal fungi or rhi-zobacteria) and ignored others (136), so thisintegrative approach is needed. A symbiotic mi-crobiome is the microbial consortium of a par-ticular host, including all genes and metaboliccapacities. The members of this consortiuminteract with the host, among themselves, andwith other organisms. Metagenomics has beenused widely to study bacterial componentsof the microbiomes of animals, particularlyhumans (94, 114, 161). These studies show thatvarious aspects of host health may depend on(and affect) the composition of the microbialflora. A few studies have explored the myco-biomes (or fungal microbiomes) of vertebratesystems (58). In plants, comprehensive diver-sity studies of bacteria and fungi are becomingmore common. These include functional ge-nomics studies (5, 38, 41, 78), studies on effectsof fungal endophytes on plant hosts (92, 100),and potential roles of endophytes in plant com-munity structure and ecosystem functioning(62, 131).

Systems biology uses a multidisciplinaryapproach to study the multiple, complexinteractions of and between organisms. It isproviding new insights about the role of plantmicrobiomes in plant adaptation, evolution,and response to global climate change (81,102). Systems biology approaches are alsoshowing how plant microbiomes can interactwith herbivores and insects (43, 75, 111).

These interactions may result in emergentproperties that arise from the interplay of genes,proteins, organelles, multiple microbial species,the host plant, and the environment. Thermo-tolerance is an example of an emergent propertythat results from interactions among a virus, anendophyte, and plant roots. A virus infectingthe endophyte Curvularia protuberata appearsto be necessary for thermotolerance to Dichan-thelium lanuginosum (panic grass) in geother-mal soils of Yellowstone National Park; neitherthe plant nor the endophyte can survive tem-peratures above 38◦C, but together they cansurvive intermittent temperatures of 65◦C for10 days (101, 126). Similarly, tomato and panicgrass plants colonized by Fusarium sp. surviveat 65◦C, whereas neither partner alone survivestemperatures above 40◦C (129).

The use of microbiosensors, quantum dots(Q-dots), and microarrays is also providing new


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insights about function and response of micro-biomes (Figure 2). Microbiosensors are mi-crobes that have been genetically engineeredto express reporter genes, either continuouslyor in response to a particular stimulus. The ex-pression of these reporter genes (e.g., nitrate-or carbon-sensitive reporter genes) can be mon-itored in situ (50) and can facilitate long-termmonitoring of microbiomes using specific or-ganisms. Q-dots are nanoscale semiconduc-tors that fluoresce in different colors depend-ing on their size and can be linked to organiccompounds to track their movement. Thesenanoparticles show promise for studying therole of endophytic fungi in nutrient uptake andtranslocation. Q-dots were used to demonstratethe uptake of organic nitrogen by a saprotrophand its transfer by mycorrhizal fungi to annualbluegrass (171).

Comparative genomics, metagenomics,transcriptomics, and proteomics are changingour perception of plant-microbial interac-tions (41, 140). Next-generation sequencingtechnologies are becoming more accessiblein terms of cost, allowing in-depth surveysof microbiomes. A study of epiphytic andendophytic communities in Quercus leavesusing 454 sequencing (18,020 sequences)revealed a community dominated by Ascomy-cota (93.4% of the sequences) and more than700 fungi (84). Microarrays for the grassendophytes Neotyphodium and Epichloe andthe plant pathogen Fusarium graminearumare allowing high-throughput transcriptomestudies to evaluate expression of specificgenes of plants and fungi. They also facilitatediscovery of novel genes and mechanismsof interaction among host plants and fungalsymbionts (44, 65). These technologies willprovide fundamental information that can beused not only with model systems, but otherplant symbionts as well. Another technology ofgreat potential is the use of RNAi knockdownmutants to study function of particular genesin the establishment of symbiotic associations.Transformants of the endophyte Piriformosporaindica made using RNAi showed a direct link

between phosphate transporters and improvedplant nutrition (173).

In addition, a growing number of genomesare available for plants and mycorrhizal and en-dophytic microbes. Genomic studies in Popu-lus (poplar trees) have demonstrated that fungalendophytes respond to genetic differences in in-dividual plants and plant responses to environ-mental cues. The production of condensed tan-nins in Populus is regulated at the genetic leveland affects directly fungal endophytic infectionsdepending on the ontogenic differences in indi-vidual plants, tissue types, and the phenotypicplant responses to environmental factors (15).Genomic analysis of bacteria from poplar rootsreveals potential roles in drought resistance andplant protection in poplar (164).

The availability of fungal genomes, includ-ing mycorrhizal fungi such as Laccaria bicolorand Glomus intraradices, plant pathogens such asMagnaporthe grisea, Ustilago maydis, F. gramin-earum, and Stagonospora nodorum, and the al-most completed genome of the clavicipitaceousendophyte Neotyphodium lolii is invaluable forunderstanding the role of mycobiomes in plantsurvival, establishment, and response to globalclimate change. However, the majority of fun-gal genomes available represent human or plantpathogens or fungi with industrial or biofuelpotential, and there is a clear necessity to prior-itize genomes to advance endophytic research.Comparative genomics, metagenomics, tran-scriptomics, and proteomics will help to unravelthe complexity of plant-microbial interactions(140).

Still, a number of technical challenges arepending. Fungal metagenome studies are lim-ited because with current technologies plantDNA cannot be separated from fungal DNA;the high concentration of host plant DNAmakes the much larger but much more dilutefungal metagenome difficult to sequence withadequate coverage. We are also limited by ourcapacity to manage large datasets and to con-duct automated classification, and by insuffi-cient functional gene annotations for currentgenomes. More quantitative proteomics and


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metabolomics approaches also need to be im-plemented for fungi.

ENDOPHYTES ANDFUNGAL DIVERSITY

Although less than 100,000 fungal species havebeen described, there are probably many more,perhaps 1,500,000 (48, 71). Some mycologistshave argued that endophytes comprise a large,although hidden, component of fungal biodi-versity (6, 10, 130). Every plant species has acommunity of endophytes—perhaps 90 speciesin a single tropical tree leaf (18) and more than50 different genera associated with roots of anarid grassland species (123). Colonization ratesvary: from <1% to 41% of 2 mm2 leaf pieces inthree major plant lineages in boreal and arcticecosystems (74) to 90% in leaves in tropical for-est trees (98). However, some endophytes arerestricted to single cells and tissues in the leaf;endophytes in different tissues may not interact(152). This potential goldmine of undescribedbiodiversity has kept mycologists interested inendophytes and the issue of host specificity, par-ticularly in tropical plants.

Fungal endophyte communities in manyplants are dominated by various classes, in-cluding Dothideomycetes, Sordariomycetes,Leotiomycetes, Eurotiomycetes, and Pezi-zomycetes (74, 84). Zygomycota and Basid-iomycota fungi also occur as endophytes, withAgaricales common in grasses (73, 88, 123),and Russulales, Polyporales, and Agaricalescommon in woody tissues and roots (146).

Some endophytes are host-specific. Assum-ing that the number of host-specific speciesis constant, the total number of endophyticspecies can be extrapolated from the number ofplant species (21, 71). Given that plant diversityis highest in the tropics, endophyte diversitymight also be highest in the tropics. A recentmeta-analysis found that leaf endophytes areindeed more species-rich in the tropics than intemperate regions (7). However, a recent studyshowed a different pattern in which diversity ofroot endophytes of a single plant, Bouteloua gra-cilis, increased with latitude in North America(73) (Figure 3). This indicates the need formore extensive surveys of plant organs to eval-uate distribution patterns and diversity of en-dophytic fungi across large geographical scales.

GrasslandH = 3.6

Wind caveH = 3.5

KonzaH = 3.0

SevilletaH = 2.6

JanosH = 2.8

OjuelosH = 2.3

Pleosporales

Agaricales

Sordariales

Hypocreales

Xylariales

Other

Ordersrepresented:

a

d d a f

a

a

a

a b b b g

c f

a a c c f g g

a b f fe e

a a c

Figure 3Continental scale distribution of fungal endophytes in a widely distributed host. Bars show the fungal community in roots of the grassBouteloua gracilis at sites ranging from Jalisco, Mexico, to Saskatchewan, Canada. Bars are labeled with site name and Shannon index ofdiversity (H). Identifications were based on 795 cloned internal transcribed spacer sequences. Data from Herrera et al. (73).


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VARIABILITY OF ENDOPHYTESIN SPACE, TIME, AND FUNCTION

Communities of endophytic fungi can varygreatly in a single host species in differentsites, climates, seasons, and environments (29,53, 97, 127, 170). Mycobiome compositionmay depend on multiple factors, includingplant host, plant density, nutrient availabil-ity, environmental conditions, and interactionswith external microbiomes (e.g., soil fungi andbacteria).

Variation can be observed at all levels. Dif-ferences in endophytic communities in a singlehost species can increase with distance (8) orshow no significant variation (73, 88). Leaves,roots, and woody stems of a single plant oftendiffer greatly in the dominant members of theirendophytic communities (reproductive struc-tures have been less widely studied) and mayeven show functional differences (30, 57, 73,119). For example, leaves, stems, and roots ofalfalfa plants are colonized by distinct fungi thatproduce different ranges of secondary metabo-lites (Figure 4) (166). These differences in en-dophytes between roots, stems, and leaves mayreflect differences in external environment asmuch as biological differences among organsand tissues: In epiphytic orchids (genus Lep-anthes) in which leaves and roots are equallyexposed to air and light, significant differenceswere not observed in their endophytic commu-nities (20). Even within a single plant, differ-ent leaves or roots may differ significantly incommunity composition (52, 98). Single leavesof a tropical forest tree, Manilkara bidentata,showed fine scale variation of endophyte iso-lation rates and identity (Figure 5). In this re-spect, plants are genetic mosaics, because eachorgan may have a unique combination of genesin its microbiome (72). More studies are neededon seasonal variation and succession to deter-mine functional importance of changes in themycobiome of the plant.

In the following sections, we discuss howendophytes overlap and interact with mycor-rhizal fungi, pathogens, saprobes, and mutu-alistic symbionts that offer protection against

drought, heat, pathogens, and herbivores, andinteractions among guilds.

ENDOPHYTES VERSUSEPIPHYTES

Endophytes are often contrasted with epi-phytes, which live on external plant surfaces(136). In practice, the distinction is that epi-phytes can be washed off plant surfaces or beinactivated by surface sterilization, usually withsodium hypochlorite and ethanol to break sur-face tension, whereas endophytes cannot. Thus,an epiphyte that survives surface sterilizationand grows in culture might be assumed to be anendophyte (9). Although there are few studiescomparing phylloplane and endophytic fungalcommunities of the same leaves, comparisonswithin pine and coffee leaves indicate that endo-phytic communities are distinct from epiphyticones, even though they may live less than a mil-limeter apart (93, 136).

Temporally as well as practically, the dis-tinction between endophytes and epiphytes isoften arbitrary. Many horizontally transmittedendophytes presumably start growing on thesurface of the leaf before penetration. Also, en-dophytes may become epiphytes when internaltissues are exposed, and may help protect theexposed tissues from the environment. In shoottip–derived tissue cultures of Pinus sylvestris,calli were found to be covered by hyphae of theendophytes Hormonema dematioides, Rhodotorulaminuta, and associated biofilms (117). How suchendophytes coordinate function, interact withother microbiome biofilm components, and af-fect plant fitness needs further exploration.

ROOT ENDOPHYTES ANDINTERACTIONS WITHMYCORRHIZAE

Root endophytes colonize healthy plant rootswithout the nutrient transfer interfaces com-monly observed in mycorrhizae (25, 137). Rootendophytes are common, but they have beenneglected for many years in comparison with


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Endophyte

Phomemedicaginis

54% Brefelcin A

Alternaria sp. 12% (not yet identified)

Cercospora sp. 11% (not yet identified)

Epicoccum sp. 11% (not yet identified)

Colletotrichumtrifolli

40% Mevinolin

Fusarium spp. 69% Lateritin

2-(3,4-dihydroxy-phenyl)ethanol

Frequency Antifungal metabolites

H O

H

HO CH3

OO

OO

NN

O

O

OH

OH

OH

H

H

H

O

OO

OO

OHOH

Figure 4Differences in most common endophytes among leaves, roots, and shoots of alfalfa (Medicago lupulina or Medicago sativa). Shown fromleft to right, plant organs, common endophytes, frequency, and secondary metabolites with antifungal activity. Metabolites weredetected in vitro and not in planta. Nonetheless, organs of a single plant may differ in both fungal endophytes and bioactive secondarymetabolites. Adapted from Weber & Anke (166).

DSE: dark septateendophyte

AMF: arbuscularmycorrhizal fungi

mycorrhizae; only recently have they been con-sidered fundamental components of ecosystemmodels (35, 62). Because some important rootendophytes do not sporulate in culture, theuse of molecular techniques has been impor-tant for identification (123, 163) and has con-firmed that many of these endophytes coexistwith other functional groups in the microbiome(Figure 6). For example, dark septate endo-phytes (DSEs) occur in mycorrhizal roots ofPinus halapensis and Rosmarinus officinalis, along

with ectomycorrhizal and arbuscular mycor-rhizal fungi (AMF), respectively (61), and withAMF in Pedicularis roots (95).

Because of problems with taxonomy andidentification, some root endophytes are com-monly described in the literature using genericnames: DSEs, hyphomycetes-endophytes, orhyaline hyphal endophytes. However, theseterms are based on morphological character-istics and colonization patterns, and grouptogether phylogenetically diverse fungal taxa.


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Here, we provide a short summary of bothgroups.

DSEs are common, widely distributed anddiverse endophytes, found in 600 phylogenet-ically diverse host species and including fungifrom different phyla (82). One DSE group,the Phialocephala fortinii s.l.–Acephala applanataspecies complex, colonizes roots in multipleplant hosts in Europe and North America (63,64, 86, 106).

DSEs are easily distinguished from mycor-rhizal fungi because their hyphae are darkly pig-mented due to the presence of melanin. Theycoexist with mycorrhizal fungi, pathogens, andother endophytes (Figure 6) (61, 82, 85, 122,123).

DSEs are commonly observed in roots ofplants in stressful and nutrient-limited environ-ments (17, 70, 88, 95, 123), which suggests theymay facilitate plant establishment and survival.Their broad geographic and host distributionsindicate low specificity. For example, P. fortiniihas been found in mutualistic association withplants from Pinaceae, Cyperaceae, Ericaceae,Salicaceae, and Rosaceae (82).

An increase in nutrient content and growthwas observed for Carex, Pinus contorta, andVulpia ciliata plants that were inoculated withDSEs (70, 85, 106). The DSE Heteroconiumchaetospira forms a functional mycorrhizal sym-biosis with Brassica campestris (Chinese cab-bage); the fungus can transfer nitrogen to andreceive carbon from the plant (162). The Brassi-caceae are usually described as nonmycorrhizal,so this association with DSE suggests that myc-orrhizae are too narrowly defined. The mecha-nisms of how these fungi contribute to acquisi-tion of nutrients, protection, and plant growthare still not well understood, but the ability ofDSEs to decompose complex organic matter in-dicates that some may act as satrotrophs (28).

Hyaline hyphal endophytes and hy-phomycetes are also common in plant roots(23, 165). Aquatic hyphomycetes are com-monly found in riparian and coastal ecosystems.For example, multiple species of aquatic hy-phomycetes were isolated from roots from ri-parian plants including grasses, pteridophytes,

Arthrinium sacchari

Chaetomium sphaerale

Colletotrichum crassipes

Coniothyrium fuckelii

Fusarium cf. avenaceum

Fusarium decemcellulare

Fusarium solani

Glomerella cingulata

Khuskia oryzae (Nigrospora)

Penicillium glabrum

Pestalotiopsis versicolor

Phomatospora sp.

Phomopsis manilkarae

Phyllosticta sapotae

Trichoderma koningii

Xylaria cf. adscendens

Xylaria cf. mellisii/arbuscula

Xylaria cf. multiplex

Zygosporium echinosporum

Sterile mycelium 2

Sterile mycelium 4

Sterile mycelium 51

Sterile mycelium X

No fungus isolated, zero

20 mm

2 m

mLe

af 1

1 2 3 4

Pe

tio

le 1

Leaf

2

1 2 3 4

Pe

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Figure 5Fine-scale distribution of fungal endophytes at the level of individual leaves.Each row shows a leaf of Manilkara bidentata cut into 1 × 2 mm pieces. Resultsshow a high level of endophytic colonization (>90% of leaf pieces), a highdiversity of fungi in a single leaf, and marked differences in communitiesamong individual leaves in a single population. Adapted from Lodge et al. (98).

and Cupressaceae trees (148). Like DSEs,hyphomycetes coexist with other types ofendophytes, mycorrhizae, and other fungithat are normally associated with marine andfreshwater environments (4), but less is knownabout their roles.

Some endophytes may form mycorrhiza-like structures. Roots of the orchid Dendrobiumnobile inoculated with an endophyte, Lepton-tidium, formed structures similar to pelotonsand showed increases in plant height, biomass,and stem diameter, all characteristic of the


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a b

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Figure 6Dark septate endophytes (DSEs). (a) Stained root section of the grass Bouteloua gracilis showing internal andextraradical hyphae; (b) DSE hyphae encircling a mycorrhizal vesicle (AMF) in a Geum rossii root; (c) hyphalproliferation in plant cells; and (d ) germinating DSE spore in G. rossii root. (Photos courtesy of J. Herreraand A. Porras-Alfaro.)

recognized mycorrhizal interactions in orchids(76). Work with model systems has suggestedthat root endophytes activate specific metabolicpathways that facilitate transfer of nutrients.For example, the external hyphae of P. indicain corn roots express a phosphate trans-porter [propylisopropyltryptamine (PiPT)](173).

Functions that overlap with those of myc-orrhizal fungi (e.g., nutrient transfer, protec-tion, internal-external colonization) show theneed to integrate endophytic and mycorrhizalfungal research. In many mycorrhizal stud-ies, endophytes are ignored or reported ascontaminants.

ARE SOME ENDOPHYTESLATENT PATHOGENS?

A common theme in discussions of endo-phytes is that they could be latent or quiescentpathogens. A change in the host or environmentmay trigger pathogenicity in an endophyte thatwas previously asymptomatic. Whether or notan interaction becomes pathogenic dependspartly on the time scale in which it is observed;even mutualisms can be viewed as series of brief,reciprocal, antagonistic interactions (138, 139).

Part of the difficulty in distinguishing endo-phytes from pathogens is that many endophytesare closely related to pathogens. In many cases,


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morphological comparisons do not provide suf-ficient resolution (e.g., Colletotrichum gloespori-oides), but the use of multiple gene sequenceanalysis has facilitated the differentiation of re-lated endophytes and pathogens (132). For ex-ample, a common, nonpathogenic endophytewas subject to quarantine because of its rela-tionship to Guignardia citricarpa, causal agentof citrus black spot (12).

A rigorous study concluded that endophytesare not simply latent pathogens: When endo-phytes of western white pine (Pinus monticola)were isolated and identified by ITS sequenc-ing, many were in the same families and generaas important pathogens (especially Rhytismat-aceae and Mycosphaerellaceae) (54). However,the most similar sequence to each endophytenever came from a pathogen of P. monticola. In-stead, many endophytes were most closely re-lated to, but distinct from, pathogens of otherspecies of pine. These endophytes may be sep-arate, less-pathogenic lineages derived frompathogens or pathogens of other hosts thatlanded on a nonhost plant. The authors pre-ferred the first explanation.

The hypothesis that some endophytes arenot pathogens, but derived from pathogens,is supported by experimental work onColletotrichum magna. This fungus is anotherexample of a pathogen of one group of plants(cucurbits) that can be an endophyte of otherplants. A pathogenic strain was convertedto a nonpathogenic strain by mutation of asingle gene, and some of the mutants even hadmutualistic effects (125, 128). Also, isolates ofColletotrichum from Panama and China showa large range of activities from endophytic topathogenic (8, 72, 132).

The reverse is also true: Pathogens can arisefrom endophytes. Arabidopsis plants colonizedby single gene mutants of P. indica grew moreslowly and produced fewer seeds than uncolo-nized plants or plants colonized with the wildtype (80). External factors, such as changes inplant gene expression, habitat, nutrient status,or stress, can also make nonpathogenic endo-phytes pathogenic (80).

However, other examples suggest that someendophytes are indeed latent pathogens. Forexample, some of the most common endo-phytes in asymptomatic wheat leaves werewheat pathogens, suggesting latency (90). En-dophytes of weeds may be pathogens of nearbycrops, complicating control of the pathogens(145) and establishment of quarantine guide-lines. Similarly, a DSE from pine was alsoa root pathogen of curcubits (61). Relativesof pathogens may be found as endophytes indifferent ecosystems: Moniliophthora sp. wasisolated and amplified directly many timesfrom healthy roots in a dominant grasslandin New Mexico, and was related to one ofthe most devastating pathogens of cacao (73,88, 123). In Musa acuminata only a few en-dophytes were pathogenic in leaf pathogenic-ity assays, but those were closely related toknown pathogens (116). A shift in host may alsotrigger pathogenicity: Colletrotrichum tropicale, acommon endophytic in Panamanian trees, hasalso been isolated as a pathogen in old leavesof Persea americana and from Annona muricatafruits (132). The lack of a clear distinction be-tween endophytes and pathogens complicatesefforts to inoculate plants with endophytes inthe field (see section on Field Applications).

BIOCONTROL OF PATHOGENSAND INSECT PESTS BYENDOPHYTIC FUNGI

Control of insects and fungal pathogens canbe accomplished by different mechanisms: byantagonism, including competition, parasitism,or production of secondary metabolites; byinduction of host defenses; or by stimulation ofhost growth and vigor (2). These mechanismsoverlap, and a single endophyte may employseveral of them. Most studies have proposedthe induction of host defenses, specificallymechanisms of systemic acquired resistance(SAR). SAR is often mediated by productionof salicylic acid, jasmonic acid, ethylene, anda variety of pathogenesis-related (PR) proteins(160). Endophytes may also produce secondary


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metabolites that directly inhibit insects orpathogens, or produce elicitors that stimulatethe plant to produce secondary metabolites.Furthermore, a single endophyte may offerprotection from both fungal pathogens and in-sects. For example, Beauveria bassiana inhibitsboth fungal pathogens and insects, mostlyby production of secondary metabolites, andLecanicillium spp. and Trichoderma spp. are bothmycoparasites and insect parasites, althoughthey also produce inhibitory metabolites(68, 112).

Pathogens

Endophytic fungi are effective biologicalcontrol agents against a variety of fungalpathogens. In most of the following examples,the endophyte is inoculated before exposure tothe pathogen (11). The control is endophyte-free plants; these can be difficult to generateand maintain, especially in trees, becauseinfection by air- and rain-borne inoculum mustbe prevented. In cacao, multiple studies havedemonstrated that endophytic fungi can reducedamage by important pathogens, includingPhytophthora palmivora, Moniliophtora roreri,and Moniliophtora perniciosa (8, 11, 104). The en-dophyte Gliocladium catenulatum can reduce upto 70% the incidence of witches’ broom diseasein cacao (133). In wild banana (M. acuminata),two endophytes (Cordana sp. and Nodulisporiumsp., out of a total of 723 cultures) showed poten-tial activity against Colletrotrichum, evaluatedas a reduction in radial growth of the pathogenand growth inhibition by the production ofsecondary metabolites (109). Protection byendophytes in nonhost plants has been demon-strated in barley plants infected with the rootpathogen Gaeumannomyces graminis var. tritici(100). Mixtures of endophytes decreased mor-tality of P. monticola seedlings exposed to whitepine blister rust (55). Fusarium verticillioides, acommon endophyte in corn, provides signif-icant reduction in the infection by U. maydis(smut disease) and causes an increase in plantgrowth when the endophyte is inoculated atthe same time as the pathogen (92).

The root endophyte P. indica can mediateresistance to root and leaf pathogens in mul-tiple plant species. P. indica–Arabidopsis inter-actions have been used as a model to studyresponse mechanisms of plant-endophyte sys-tems to plant pathogens (142). This fungusis restricted to the root cortex but can in-duce resistance to leaf pathogens through asystemic signaling between plant and fungus.P. indica induces systemic resistance in Ara-bidopsis to Golovinomyces orontii, a powderymildew, by activating the jasmonate signalingpathways (150). A related endophyte, Sebacinavermifera, increased the growth of Nicotiana at-tenuata but increased the susceptibility to her-bivorous insects through the inhibition of ethy-lene synthesis and jasmonic acid pathways (16).

In other examples, P. indica uses sophisti-cated mechanisms to induce host cell deathin order to establish a mutualistic relationshipwith barley roots (39). The presence of P. in-dica attenuates the expression of a barley BAXinhibitor gene. This gene is known to inhibitplant cell death and fungal colonization was in-hibited in transgenic barley that expressed thegene.

Insect Pests

Horizontally transmitted endophytes arehighly variable in their effects on shoot-feedinginsects (69), but several studies have demon-strated potential in this area. Three of fiftyfoliar fungal endophytes isolated from Picearubens (red spruce) needles showed toxicityagainst Choristoneura fumiferana, the easternspruce budworm (156). Beauveria bassiana,Lecanicillium lecanii, and Aspergillus parasiticusare entomopathogens that have been identifiedas endophytes in various plants and can be suc-cessfully inoculated in the field (60). Positiveresults with B. bassiana and L. lecanii include adecrease in reproduction and leaf consumptionby the aphid Aphis gossypii and a decreasein the growth of nymphs of the Australianplague locust Chortoicetes terminifera followinginoculation with the fungi (67). Endophytescan also offer protection from other plant pests:


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Meira geulakonigii colonizes grapefruit peeland protects against mites (113). Inoculationwith Fusarium oxysporum reduced populationsof nematodes in roots of banana and tomatoplants (144).

Of course, unsuccessful attempts at biocon-trol are much less likely to be published thansuccessful ones. Although the cited studies showimpressive potential for using endophytes forbiocontrol in crop plants and forest trees, itshould not be assumed that all endophytes areeffective at plant protection (42).

Field Applications

The fluidity of lines between endophytes andother funcional groups, as shown in the previ-ous sections, raises questions about the safety offield applications of endophytes for biocontrol.Will changes in the environment (e.g., nutri-ent availability or gene expression in the host)shift the fungus from mutualistic to pathogenic?Will the endophyte be pathogenic in other,nearby plants? Will it harm beneficial insectsas well as pests? Will it produce mycotoxins?Because all of these actions have been shownto occur in some endophyte-host combinationsand not occur in others, these questions shouldbe considered for each particular application.For example, there are commercial formula-tions of clavicipitaceous endophytes of grassesthat protect turfgrasses from insect pests (33).These products would be undesirable when ap-plied to pasture grasses, however, because thesame secondary metabolites that deter insectsare toxic to livestock.

In some cases, inconsistency in pathogenic-ity versus mutualism could simply reflect poortaxonomic knowledge of the fungi (3, 82). InColletotrichum it can be difficult to distinguishColletotrichum theobromicola, which causes an-thracnose in leaves, from Colletotrichum igno-tum and C. tropicale, which infect leaves with-out causing disease but cause rot in ripe fruits(132). Comparisons between greenhouse andin vitro experiments also show inconsistent re-sults: When P. contorta was inoculated withP. fortinii, open pot culture experiments and

in vitro culture assays differed in response interms of biomass and foliar nutrient concentra-tion (86).

It is clear that more comprehensive surveysare needed to document relationships ofendophytes with congeneric saprotrophs andpathogens. In addition, the complexity ofinteractions among endophytes, pathogens,insects, and plants shows the difficulty ofpredicting outcomes for plant protection (59,79). Pilot studies on these interactions alsoneed to be scaled up to field experiments. Wethink advances in the biology of endophytes,combined with growing interest in biocontroland integrated pest management, will lead toa growing number of commercial applications.Another potential use of endophytes, at least inthe case of those endophytes that are verticallytransmitted, is vectors of genes intended to im-prove plant performance; transformation of theendophyte may be easier than transformationof the plant (33).

ENDOPHYTES AS SOURCES OFNOVEL SECONDARYMETABOLITES

Endophytes are fertile ground for drug discov-ery (149). The number of patents that use endo-phytes for the production of secondary metabo-lites or with biologically important activitieshas increased dramatically in the past 20 years(Figure 7) (118). Classes of bioactive metabo-lites obtained from endophytes include alka-loids, cytochalasins, polyketides, terpenoids,flavonoids, and steroids (66). Activity targets in-clude bacteria, fungi, and cancer cells; cellulartargets include cell division, glucose transport,HIV-1 protease, and the cytoskeleton (60, 71,151).

One of the best-known and most curiousexamples is that of paclitaxel, the first billiondollar anticancer drug (154). Paclitaxel was sosuccessful in the 1990s that the survival ofthe source plant, the yew Taxus brevifolia, wasthreatened by overharvesting. An endophyteof T. brevifolia, Taxomyces andreanae, was alsofound to produce paclitaxel, presumably the


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1990

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Figure 7Increase in number of U.S. patents awarded for bioactive secondarymetabolites from endophytic fungi. Redrawn from Priti et al. (118).

result of lateral gene transfer from host to fun-gus (151). Other examples of potentially usefulmetabolites from endophytes abound. Fusariumsubglutinans, an endophyte in stems of a peren-nial twining vine, Tripterygium wilfordii, pro-duces subglutinol A and diterpene pyrones withimmunosuppressive activity (91, 155). AnotherFusarium showed activity against intravascularthrombosis, a main cause of cardiovascular dis-eases (172). Endophytes clearly have potentialfor bioprospecting.

Interesting and important examples of en-dophyte secondary metabolism are still beingdiscovered. Several groups of Convolvulaceae,including common Ipomoea species and culti-vars (e.g., morning glories), are notorious forthe ergot alkaloids in their seeds, compoundsrelated to LSD (115). It has recently been dis-covered that these alkaloids are produced by en-dophytic fungi in the Clavicipitaceae (89). Thefungi are unculturable, but their presence is re-vealed by direct sequencing. The endophytesare vertically transmitted through the seed, andfungicide-treated plants have neither the funginor the alkaloids (1). The proportion of theplant metabolome derived from or affected byendophytes is unknown.

ARE SOME ENDOPHYTESLATENT SAPROTROPHS?

Many authors have proposed that some endo-phytes are latent saprotrophs that get a headstart, becoming active on the death of the hostorgan. A saprotroph able to colonize living tis-sues will be able to start growing as soon as thetissue senesces, gaining a competitive advantageover other saprotrophs that arrive later. In theinitial stages of decomposition, the fungi willhave rapid access to sugars and other nutrientseasy to assimilate that will not be available tolater arrivals. In addition, senescent plants couldprovide stimuli or opportunities for sporulationabsent from living plant tissues. On a commu-nity level, there are diffuse benefits to this head-start saprophytism: It allows rapid turnover ofnutrients (85).

This hypothesis of endophytes as latentpathogens was supported by a phylogeneticstudy that compared relationships of endo-phytes and saprotrophs isolated, respectively,from healthy and decaying leaves and twigs ofMagnolia liliifera (120). In the common endo-phyte genera Colletotrichum/Glomerella, Fusar-ium/Nectria, Phomopsis/Diaporthe, Guignardia,and Corynespora, endophytic and saprotrophicisolates are closely related, supporting the hy-pothesis of latent saprotrophism. No sapro-trophic Xylaria was isolated, thus for Xylaria thehypothesis could not be evaluated. In the caseof Xylaria, endophytic and saprotrophic speciesin the same area, and even on the same host,may be distinct (96).

Other studies also support the saprotrophhead-start concept. Over 20% of root endo-phytes in blue grama were close relatives ofsaprotrophic and coprophilous fungi (123). Infungal communities in litter of Pinus edulis, Ju-niperus monosperma, and Populus deltoides in NewMexico, several clades showed high similaritywith endophytic fungi reported for arid grass-lands and other environments (51, 123, 121). Inthis case, it is possible that endophytes repre-sent saprotrophs that landed in nontarget hosts,as discussed above for pathogens. The three lit-ter types differed significantly in composition


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of their fungal communities, suggestingspecificity.

Metabolic activity typical of saprotrophshas been demonstrated in several groups ofendophytes. The endophyte Hymenoscyphusericae produces extracellular enzymes withcellulolytic, hemicellulolytic, pectinolytic, andligninolytic activity in vitro, able to penetrateplant cell walls to access complex humicclusters (27). The capacity to degrade complexorganic molecules can be viewed as indirectevidence of latent saprotrophism.

Dual roles as endophyte and saprotrophhave also been observed for Phoma medicaginis,a dominant endophyte in alfalfa plants (Med-icago lupulina and Medicago sativa) that acceler-ates growth and sporulation after death of thehost. In addition, the fungus produces brefeldinA, a metabolite that shows antifungal activ-ity against other fungi, facilitating the transi-tion from an endophytic to saprotrophic lifestyle (Figure 4) (167). Similar adaptations weredemonstrated for Phomopsis: In Australia, Pho-mopsis leptostromiformis can colonize lupins asan endophyte but grows extensively as a sapro-troph after plant death (168). P. leptostromiformisis also known to produce a large number of my-cotoxins that facilitate its establishment. Theability of the fungus to compete for the sub-strate in early decomposition stages facilitatesits reproduction and sporulation (30, 65).

The contrary case, facilitation by endo-phytes of saprotrophic fungi, has also beendemonstrated. Leaves of Camellia japonica col-onized by the endophytic fungus Coccomyces sp.are more accessible to other decomposers thanleaves without it (111). Similarly, interactionsamong endophytes (Phomopsis and Xylaria) andtwo saprotrophic fungi (Mycena polygramma andPhanerochaete) affect the decay rate of twigs ofJapanese beech (47). These studies reveal endo-phytes as important elements in decomposition.However, little is known about how much over-lap exists between saprotrophic and endophyticcommunities, the mechanisms that trigger thetransition from endophytic to saprotrophic lifestyles in a senescent plant or in litter, and theregulatory pathways that control expression of

the enzymes during decomposition versus en-dophytic or pathogenic colonization.

ENDOPHYTES INPHYTOREMEDIATION

Bacterial endophytes can make plants more ef-fective at tolerating and degrading xenobioticcompounds in the soil. For example, plantsin soil contaminated with petroleum had en-dophyte communities with higher frequen-cies of hydrocarbon-degrading bacteria thanplants on uncontaminated soil (143). Plantsinoculated with VM1330, an engineered en-dophytic bacterium, showed increased toler-ance to toluene and decreased transpiration oftoluene to the atmosphere (105). Festuca grassesinfected with endophytic clavicipitaceous fungiremoved more polycyclic aromatic hydrocar-bons from oil-contaminated soils than unin-fected plants (147). A study of Lolium perenneinoculated with the endophyte Acremoniumlolii showed an increase in plant resistance tozinc toxicity (22). Similarly, mycorrhizal fun-gal communities are known to vary in theirresponse to heavy metals and also to facilitateplant survival in contaminated soils (56). Phy-toremediation enhancement could be a resultof improvement in nutrition, protection againstpathogens or direct degradation or accumula-tion of heavy metals in specific structures (56,159). Few phytoremediation studies have fo-cused on endophytic fungi or complete micro-biomes to date, but given the utility of fungi inbioremediation, the potential is clear.

ENDOPHYTES AND PLANTRESPONSES TO CLIMATECHANGE

Given that plant microbiomes influence plantestablishment, resistance to environmentalstress, and survival, it is expected that they influ-ence the response of plants and ecosystems toclimate change (134). The study of how plant-fungal systems respond to environmental cuesis complicated by the fact that plant micro-biomes are dynamic and show large seasonal


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variation and host variation even among sym-patric plant species (34, 37, 83, 97). For exam-ple, in sub-Arctic plants colonized with AMFand DSE, Ranunculus acris showed high ratesof colonization by both throughout summer,Trollius europaeus had lower colonization, andin Alchemilla glomerulans colonization by DSEfungi decreased during the summer (135).

Despite these limitations, several studieshave demonstrated that endophytic communi-ties affect plant responses to various aspectsof climate change, such as warming, increasein carbon dioxide, increase in nitrogen depo-sition, and prolonged periods of drought (87,49). Warming increased density of some en-dophytic species in arctic willow (Salix arctica)in Canada (49). The association of plants withendophytes can also ameliorate the negative ef-fects of drought. Cacao plants colonized by theendophyte Trichoderma hamatum showed de-layed gene expression in drought conditions.This could be a result of an improvement innutrient acquisition, plant growth or signalingpathways when the plant is colonized by theendophyte. Fungal endophytes can also con-trol plant responses to stress through the pro-duction of specific molecules: Paraphaeosphaeriaquadriseptata produces a heat shock protein 90(HSP90) inhibitor, monocillin I, that enhancesheat stress tolerance in Arabidopsis (103).

The increase of CO2 in the atmospherestimulates photosynthetic activity and plantgrowth. Mycorrhizal and endophytic microbialcommunities depend on plant carbon, soelevated levels of CO2 can also modify plant-microbial interactions. P. sylvestris seedingsinoculated with dark septate fungi showedan increased in biomass under elevated CO2

conditions and an improvement in the use ofnutrients (3). Elevated CO2 stimulated themycorrhizal root colonization of Plantago lance-olata and stimulated growth of endophytic fungiin Festuca arundinacea, which affected the distri-bution of nitrogen between the two plants (32).

Long-term experiments indicate thatecosystem stability is positively dependenton root diversity and biomass, which is inturn influenced by the colonization levels

of mycorrhizal and endophytic fungi. Largenumbers of species are necessary to supportecosystem functioning, especially where landuse is intensive over large areas (99), but ourknowledge about the role of endophytic fungion plant and ecosystem stability is very limited.The establishment of long-term monitoringexperiments, and the use of quantitativeand standardized methods, is essential tounderstand the roles of plant microbiomes inresponses to climate change.

CONCLUSIONS

So do fungal endophytes matter? In many casesthey clearly do: We have presented examples inwhich diverse endophytes affect diverse plantsin diverse ways, including in their interactionswith fungal and insect pests. However, as notedabove, experiments with negative results are lesslikely to get published than positive ones. Aplant at any given moment contains a great di-versity of endophytes, some of which may laterbecome important, for better or worse. Mostwill probably never significantly affect the hostas individuals, but they may have impacts as partof the microbiome and functional metagenome.The fact that different organs of a single hostcontain different communities increases its phe-notypic plasticity (72), perhaps an advantage inunpredictable environments. This is itself anemergent property that is possible as a result ofthe complex interactions between microbiomesand plants.

It is increasingly clear that endophytes over-lap with other functional groups of plant-associated microorganisms—for example, theDSEs that form associations that function likemycorrhizae—so part of the importance of en-dophytes is self-contradictory, as some do notremain endophytes. Our increasing ability to vi-sualize complex interactions in the microbiomewill help us understand the roles of fungal en-dophytes. We believe that there are unknownbut important endophytes and effects of endo-phytes yet to be discovered.

Recent studies on the human microbiomehave yielded amazing results. For example, the


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bacterial community of the skin and digestivesystem is unique for each individual (36, 46).Differences among progeny of interspecific hy-brids of Populus in relationships with endo-phytes (15) and in endophytes among leaveson a single tree (98) suggest that plants mayalso have unique microbiomes, probably at thelevel of cultivars, if not at the level of individ-uals. As pressures on the global food supply

increase because of population growth, increas-ing affluence, and climate change, agriculturewill be forced to do more with less. Plant ge-netics and breeding are receiving widespreadattention as ways to address this need (157).We believe that understanding and manipulat-ing the complex interactions of plant micro-biomes, although less obvious, will be equallyimportant.

SUMMARY POINTS

1. In interactions with plants and the environment, fungal endophytes show functionaloverlap and complex interactions with other groups: mycorrhizal fungi, pathogens, sapro-trophs, epiphytes, and bacteria.

2. Until recently culturability of endophytes was a limiting factor. Direct PCR from planttissue allows unculturable species to be detected. Metagenome approaches and otherPCR approaches allow simultaneous detection and the study of active components of thewhole microbiome.

3. Some interactions among endophytes, other microbiome components, host plants,pathogens, and pests show emergent properties. The study of plant microbiomes asa system allows analysis and integration of these complex interactions.

4. DSEs are found in roots of many plant groups, especially in nutrient-poor boreal soilsand arid systems. As a heterogeneous and sometimes dominant group, their importanceis increasingly evident and includes mycorrhizal functions in some plants.

5. Some endophytes may be latent pathogens, some may be derived from pathogens, andothers may be latent saprotrophs, but many are neither.

6. Endophytes have been shown to protect various plants from a wide range of pathogensand insect pests. Some function by antagonism, inducing host defenses, and/or improvingplant health and nutrition.

7. Some endophytes enable plant hosts to survive in hostile environments where neitherhost nor endophyte can survive alone. This emergent property shows that endophytescould affect plant responses to climate change.

8. Endophytes are a mine for bioprospecting. By extrapolation from numbers of new en-dophytes and metabolites reported in the past twenty years, many interesting cases areyet to be discovered.

FUTURE ISSUES

1. Toward a synthesis era: Can the research community agree on guidelines for isolation,extraction, amplification, annotation, and sequence database curation?

2. How do we identify functional cores of plant microbiomes and predict which endophytesare likely to affect plant health or produce useful secondary metabolites?


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3. Which endophytes are metabolically active in the plant, and which are merelyhitchhikers?

4. How can we best apply a systems biology approach to complex, simultaneous interactionsof the different groups of organisms that affect plant health?

5. How can useful endophytes be applied for pest control or to confer other desired traitson their hosts?

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

Endophytic research in the Porras-Alfaro Lab is supported by the Long Term Ecological Re-search Network (Sevilleta and Niwot LTER sites) and the National Science Foundation (Awardnumber: 0919510). We thank the UPR CREST-CATEC project (National Science Foundation)for support and Marıa Davila for editorial assistance.

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PY49-FrontMatter ARI 8 July 2011 9:55

Annual Review ofPhytopathology

Volume 49, 2011Contents

Not As They SeemGeorge Bruening � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Norman Borlaug: The Man I Worked With and KnewSanjaya Rajaram � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �17

Chris Lamb: A Visionary Leader in Plant ScienceRichard A. Dixon � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �31

A Coevolutionary Framework for Managing Disease-Suppressive SoilsLinda L. Kinkel, Matthew G. Bakker, and Daniel C. Schlatter � � � � � � � � � � � � � � � � � � � � � � � � � � �47

A Successful Bacterial Coup d’Etat: How Rhodococcus fascians RedirectsPlant DevelopmentElisabeth Stes, Olivier M. Vandeputte, Mondher El Jaziri, Marcelle Holsters,

and Danny Vereecke � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �69

Application of High-Throughput DNA Sequencing in PhytopathologyDavid J. Studholme, Rachel H. Glover, and Neil Boonham � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �87

Aspergillus flavusSaori Amaike and Nancy P. Keller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 107

Cuticle Surface Coat of Plant-Parasitic NematodesKeith G. Davies and Rosane H.C. Curtis � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 135

Detection of Diseased Plants by Analysis of Volatile OrganicCompound EmissionR.M.C. Jansen, J. Wildt, I.F. Kappers, H.J. Bouwmeester, J.W. Hofstee,

and E.J. van Henten � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 157

Diverse Targets of Phytoplasma Effectors: From Plant Developmentto Defense Against InsectsAkiko Sugio, Allyson M. MacLean, Heather N. Kingdom, Victoria M. Grieve,

R. Manimekalai, and Saskia A. Hogenhout � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 175

Diversity of Puccinia striiformis on Cereals and GrassesMogens S. Hovmøller, Chris K. Sørensen, Stephanie Walter,

and Annemarie F. Justesen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 197

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Emerging Virus Diseases Transmitted by WhitefliesJesus Navas-Castillo, Elvira Fiallo-Olive, and Sonia Sanchez-Campos � � � � � � � � � � � � � � � � � 219

Evolution and Population Genetics of Exotic and Re-EmergingPathogens: Novel Tools and ApproachesNiklaus J. Grunwald and Erica M. Goss � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 249

Evolution of Plant Pathogenesis in Pseudomonas syringae:A Genomics PerspectiveHeath E. O’Brien, Shalabh Thakur, and David S. Guttman � � � � � � � � � � � � � � � � � � � � � � � � � � � 269

Hidden Fungi, Emergent Properties: Endophytes and MicrobiomesAndrea Porras-Alfaro and Paul Bayman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

Hormone Crosstalk in Plant Disease and Defense: More Than JustJASMONATE-SALICYLATE AntagonismAlexandre Robert-Seilaniantz, Murray Grant, and Jonathan D.G. Jones � � � � � � � � � � � � � 317

Plant-Parasite Coevolution: Bridging the Gap between Geneticsand EcologyJames K.M. Brown and Aurelien Tellier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Reactive Oxygen Species in Phytopathogenic Fungi: Signaling,Development, and DiseaseJens Heller and Paul Tudzynski � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 369

Revision of the Nomenclature of the Differential Host-PathogenInteractions of Venturia inaequalis and MalusVincent G.M. Bus, Erik H.A. Rikkerink, Valerie Caffier, Charles-Eric Durel,

and Kim M. Plummer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 391

RNA-RNA Recombination in Plant Virus Replication and EvolutionJoanna Sztuba-Solinska, Anna Urbanowicz, Marek Figlerowicz,

and Jozef J. Bujarski � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 415

The Clavibacter michiganensis Subspecies: Molecular Investigationof Gram-Positive Bacterial Plant PathogensRudolf Eichenlaub and Karl-Heinz Gartemann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 445

The Emergence of Ug99 Races of the Stem Rust Fungus is a Threatto World Wheat ProductionRavi P. Singh, David P. Hodson, Julio Huerta-Espino, Yue Jin, Sridhar Bhavani,

Peter Njau, Sybil Herrera-Foessel, Pawan K. Singh, Sukhwinder Singh,and Velu Govindan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 465

The Pathogen-Actin Connection: A Platform for DefenseSignaling in PlantsBrad Day, Jessica L. Henty, Katie J. Porter, and Christopher J. Staiger � � � � � � � � � � � � � � � 483

vi Contents

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Understanding and Exploiting Late Blight Resistance in the Ageof EffectorsVivianne G.A.A. Vleeshouwers, Sylvain Raffaele, Jack H. Vossen, Nicolas Champouret,

Ricardo Oliva, Maria E. Segretin, Hendrik Rietman, Liliana M. Cano,Anoma Lokossou, Geert Kessel, Mathieu A. Pel, and Sophien Kamoun � � � � � � � � � � � � � � � 507

Water Relations in the Interaction of Foliar Bacterial Pathogenswith PlantsGwyn A. Beattie � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 533

What Can Plant Autophagy Do for an Innate Immune Response?Andrew P. Hayward and S.P. Dinesh-Kumar � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 557

Errata

An online log of corrections to Annual Review of Phytopathology articles may be found athttp://phyto.annualreviews.org/

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hidden fungi, emergent properties: endophytes and...

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