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Ecological understanding ofroot-infecting fungi using trait-basedapproachesCarlos A. Aguilar-Trigueros1,2, Jeff R. Powell3, Ian C. Anderson3, Janis Antonovics4,and Matthias C. Rillig1,2

1 Institut fur Biologie, Plant Ecology, Freie Universitat Berlin, D-14195 Berlin, Germany2 Berlin-Brandenburg Institute of Advanced Biodiversity Research, D-14195 Berlin, Germany3 Hawkesbury Institute for the Environment, University of Western Sydney, Penrith NSW 2751, Australia4 Department of Biology, University of Virginia, Charlottesville, VA 22904, USA

Classification schemes have been popular to tame thediversity of root-infecting fungi. However, the useful-ness of these schemes is limited to descriptive purposes.We propose that a shift to a multidimensional trait-based approach to disentangle the saprotrophic–sym-biotic continuum will provide a better framework tounderstand fungal evolutionary ecology. Trait informa-tion reflecting the separation of root-infecting fungi fromfree-living soil relatives will help to understand the evo-lutionary process of symbiosis, the role that speciesinteractions play in maintaining their large diversity insoil and in planta, and their contributions at the ecosys-tem level. Methodological advances in several areassuch as microscopy, plant immunology, and metatran-scriptomics represent emerging opportunities to popu-late trait databases.

Limitations of categorical approaches to study plant–soil fungal interactionsUnderstanding the effects of plant–soil fungal interactionsin natural communities has become a major research areain plant science [1]. Interest in these interactions stemfrom increasing awareness that soil biota play an impor-tant role in plant performance, plant community assembly,and ecosystem functioning [2].

However, the complexity of soil fungal communitieschallenges our ability to understand the effects of suchinteractions on plant performance and on ecosystems pro-cesses. Recent surveys show that roots interact with phy-logenetically diverse groups of fungi [3]. Moreover, theeffects of particular plant–fungal combinations dependon environmental conditions and on the host andfungal genotypes [4]. In diverse communities and variable

environments, net responses may be due to complex indir-ect interactions among co-occurring fungi and plants [5].

Given these complex associations, researchers regularlyclassify fungal taxa into broad categories according toparticular criteria. These criteria may be based on nutri-tional mode (e.g., ‘biotroph’, ‘necrotroph’, or ‘saprotroph’[6]; see Glossary), presence of hyphal melanization andformation of septa (e.g., ‘dark septate endophytes’ [7]), oron a mix of taxonomic, morphological, and physiologicalcharacteristics (e.g., ‘arbuscular mycorrhizal’ or ‘ectomy-corrhizal’ [8]). These classificatory approaches have beenimportant for distilling broad generalities from the richbrew of fungal–plant interactions such as the recognition ofcontrasting plant defense mechanisms against infectingfungi with different nutritional modes [9].

However, assignment of root-infecting fungi into fixedcategories is problematic for species labeled as ‘endo-phytes’. For example, some of the criteria used in delineat-ing endophyte classes [10] are quantitative (number ofpotential hosts, number of co-infections within a host, ordegree of tissue colonization), but their delineation isimprecise (narrow vs broad host range; low vs high inplanta diversity; extensive vs limited in planta coloniza-tion). Similarly, a suggestion that ‘endophytic functionalgroups’ should be based on their effects on host fitnessresulted in the rather unsatisfying conclusion that ‘some

Opinion

Glossary

Biotroph: nutritional mode in which a fungal symbiont exclusively relies on

living host cells as a source of nutrients.

Functional trait: species traits directly linked with a particular ecosystem

process. Different species sharing similar functional traits are pooled into

functional groups.

Life history trait: traits reflecting allocation of resources of an individual into

different fitness components.

Necrotroph: nutritional mode in which a fungal symbiont causes host cell

death in order to acquire nutrients.

Saprotroph: nutritional mode in which a free-living fungus obtains nutrients

from decaying organic matter, without inducing the death of the tissue.

Symbiosis: a physiological or structurally intimate interaction between

phylogenetically unrelated organisms, without implying a specific effect of

fitness on either organisms.

Trait: any morphological, physiological, or phenological character of an

organism.

1360-1385/$ – see front matter

� 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2014.02.006

Corresponding author: Rillig, M.C. ([email protected]).Keywords: classification schemes; root-infecting fungi; trait-based approach; sapro-trophy–symbiosis continuum.

432 Trends in Plant Science, July 2014, Vol. 19, No. 7


endophytes may be latent pathogens, some may be derivedfrom pathogens, and others may be latent saprotrophs, butmany are neither’ [11]. Such classification schemes canprovide a useful initial framework to understand poorlystudied plant–fungal interactions, but the resulting gen-eralizations often include the listing of so many exceptionsto the proposed scheme that the framework is not usefuloperationally.

We argue that a shift in focus from classificationschemes to a multidimensional trait-based approachreflecting the biology of the fungi is necessary for a betterunderstanding of the ecology and evolution of root-infect-ing fungi. These approaches consider species as a conglom-erate of unique combinations of multiple traits, whichcould be depicted as species being points defined by multi-ple traits represented as dimensions (Figure 1). This viewdirectly links particular ecological and evolutionary ques-tions with trait information. The proposed multidimen-sional trait-based program presented here is focused on thetraits that allocate ‘endophytic’ or ‘pathogenic’ root fungi toa symbiotic lifestyle and separate them from free-livingsaprotrophic relatives. We explain how trait informationcan be used to address three essential questions: What arethe mechanisms behind the evolution of root endophytic orpathogenic lifestyles from free-living fungi and vice versa?

What is the importance of trait similarity in explaining theco-occurrence patterns of fungal genotypes or species inplanta and in the soil? And, which traits might be used tounderstand the functional diversity of soil fungi? This isillustrated conceptually in Figure 1.

A fungal-trait approach: understanding thesaprotrophic–symbiotic continuumTrait-based approaches rely on measurements of phenoty-pic characters or traits to guide inferences about particularecological or evolutionary processes (Box 1). For example,plant scientists have successfully used such approaches tounderstand how fire has influenced the evolution within thePinaceae by combining trait information with phylogeneticreconstructions [12], to measure the relative importance ofabiotic factors and biotic interactions in shaping communityassembly of tropical trees by measuring trait overdispersionin local communities [13], or to understand how plantdiversity influences the variability of decomposition rateswithin climate regions by combining decomposition datawith leaf traits from databases [14].

We explain how application of such trait-basedapproaches may be valuable at a conceptual level in under-standing the saprotrophic–symbiotic continuum in root-infecting fungi. This continuum is pertinent to this set of

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TRENDS in Plant Science

Figure 1. From categorization to trait analysis for root-infecting fungi. Schematic representation of a trait-based approach to understanding the ecology and evolution of

root-infecting fungi. Instead of placing species into fixed categories (A) such as pathogen, endophyte, or saprotroph, trait-based multivariate approaches represent species

as particular combinations of traits in various dimensions (B). Such information can be coupled with: (C) phylogenetic data to understand evolutionary change; (D) their

relationships to species performance under different environmental conditions to understand mechanisms of community assembly and species coexistence and; (E) with

their effects on ecosystem properties to explore their role in these processes. Note: the graphic in (D) represents the lower resource boundaries above which species 1 and 2

can still grow (zero net growth isoclines as in [54]). In this figure, the position of lines depends on the traits the species possess to exploit two resources: carbon from the

host or from decaying matter.

Opinion Trends in Plant Science July 2014, Vol. 19, No. 7

433


fungi because most root endophytes constitute a gray areaalong the saprotrophic–symbiotic spectrum [10] and facul-tative saprotrophy is a characteristic of most studied rootpathogens [15]. Indeed, this issue has been debated amongplant pathologists ever since the seminal work of Garrett[16]. More recently, it has been a major focus of studyamong researchers on ectomycorrhizal fungi [17,18].

Understanding the saprotrophic–symbiotic continuumis of particular relevance to plant–fungal associations thathave been labeled ‘endophytic’ or ‘root pathogenic’. Despitebeing considered major components of natural commu-nities [10,19], ‘endophytes’ are not well defined in termsof their nutritional mode and there is little empiricalunderstanding of their life history strategies, which in turnmakes predicting their community and ecosystem impactsdifficult.

Specifically, we propose that characterizing this conti-nuum using a trait-based approach can make inroads inthree ways: first, explaining the evolutionary trajectoriesof symbiotic fungi from soil-inhabiting relatives (and viceversa); second, understanding and predicting the func-tional role of fungi along this continuum in nutrient andcarbon dynamics within ecosystems; and third, providing amechanistic understanding of fungal community assembly

and maintenance of diversity both in soil and in planta. Inthe following section, we lay out the basis for such anapproach, defining classes of traits relevant to this con-tinuum, and suggest examples of relevant and measure-able traits.

Symbiotic and saprotrophic traits: a starting pointIn Table 1 we provide some examples of traits that weconsider to be critical in assessing the ecology and evolu-tion of ‘endophytic/pathogenic’ root-infecting fungi. As willbe evident from the brief discussion of the rationale foreach of them, these broad traits will themselves consist ofmany component traits that are operationally measurable.We expand on some of these points below.

Symbiotic traits are often related to the ability of fungito avoid or overcome resistance responses driven by theplant immune system as host resistance is the main filterpreventing the use of the root niche [20]. Other traits maybe related to the metabolic interactions that occur in suchsymbioses; for example, systems for translocation andbidirectional transport of nutrient and carbon resources[21]. Identification of relevant component traits for ‘rootendophytic’ associations depends on understanding themolecular and physiological activities in fungal coloniza-tion structures [22]. Saprotrophic traits are related to theenzymatic machinery required to degrade the diversity ofrecalcitrant carbon sources [23], production of antimicro-bial compounds during competition with other fungi [24]and with bacteria [25], and preventing or responding tofungivory by soil animals [26].

The traits in this continuum may help us to understandthe evolutionary process behind the transitions fromsaprotrophism to symbiosis and vice versa [27]. This couldbe achieved using comparative phylogenetic approachesquantifying the variation in saprotrophic and symbiotictraits and identifying potential life history trade-offs,instead of using categories such as endophyte, saprotroph,or pathogen as if they were characters [28]. It should alsobe possible to compare the evolutionary processes under-lying the colonization and exploitation of roots versusleaves by fungal endophytes or pathogens. The contrastbetween these two organs regarding their structure andtheir local environments [29] may help explain differencesin colonization patterns between root and leaf ‘pathogens’or ‘endophytes’ [4].

Trait-based approaches could also be used to unravelcompositional differences in fungal communities inhabitingroots, the rhizosphere, and bulk soils. As roots are livingorgans, fungal species with ‘symbiotic’ traits should dom-inate in the root compartment, whereas species with ‘sapro-trophic’ ones should be more abundant in the rhizosphereand bulk soil. Trait information, if mapped onto fungalcommunities found in various soil compartments, could beused to understand the ecological basis and predictability ofthese assemblages. For instance, canonical examples inagricultural research have led to the common view that rootnecrotrophic pathogens, despite having saprotrophic abil-ities, are outcompeted by ‘strict’ soil saprotrophs [30]. Traitinformation could be used to test whether such putativetrade-offs apply to root ‘endophytes’ or ‘pathogens’ in naturalsystems.

Box 1. Rationales for trait-based approaches

The rationale for collecting data for particular traits may differ. Traits

may be chosen because they are likely to contribute to answer

particular questions: a ‘top-down’ approach. Alternatively, traits may

be chosen because they can be integrated with the ever-increasing

body of genomic and gene expression data allowing linkage of

particular genes with tangible phenotypes, or traits, of ecological

importance. This would be a ‘bottom-up’ approach. Additionally,

there is tremendous value in including traits simply because they are

‘easy to measure’: databases are as valuable in generating hypoth-

eses as they are in testing them, and unusual and unpredicted trait

associations are a stimulus for deeper investigation.

Traits can be used to test hypotheses of evolutionary processes in

conjunction with independently derived, usually sequence-based,

phylogenetic information. Thus, they provide objective ways to

identify and test potential evolutionary trade-offs in life history traits

and relate them to environmental conditions using phylogenetic

comparative methods. For example, this approach has been used to

evaluate allocation of carbon by arbuscular mycorrhiza fungal species

to hyphal structures in roots and soil where percentage of root

colonization and length of extraradical mycelia were used as traits [55].

Trait-based approaches can also be used to understand commu-

nity assembly. First, they allow the identification of potentially

important physiological and ecological mechanisms by correlating

traits with species performance along environmental gradients [56].

Second, trait similarity among species can be used to infer niche

similarity and determine its effects on species sorting [57]. For

example, the existence of trait trade-offs in important ecological

factors or niche axes is fundamental for a mechanistic under-

standing of species coexistence [54].

At the ecosystem level, species sharing traits that influence

particular ecosystem properties or responses of species to environ-

mental conditions can be pooled into particular functional groups

[58]. For example, Tilman [34] showed that functional trait diversity

is a better predictor of community productivity than taxonomic

diversity. This functional ecology perspective identifies those traits

that affect the ability of species to persist during environmental

change (response traits) and influence the environment (effect

traits), and establishes the link between these set of traits to build

models of community assembly and ecosystem functioning [59].

Recently, there has been a call to use this conceptual framework for

ectomycorrhizal fungi [37].


434


Trait information also allows the formulation of novelhypotheses. For example, does high trait diversity at thecommunity level increase resistance to invasion by otherfungi? Successful invasion depends on the number of openniches [31], and established fungal communities exhibitinghigh trait diversity may reduce resources (space, nutrients,organic matter) or limit access to resources (by priminghost defenses or producing antibiotics). For fungi at thesymbiotic end of the spectrum, is growth in the soil envir-onment limited by the diversity of resident saprotrophictraits in the rhizosphere? Relationships between traitdiversity and invasion resistance may help predict thelikelihood of disease outbreaks by highly virulent root-infecting fungi in agricultural systems.

Assessing trait similarity provides a better means toassess the effect of competition among co-infecting fungi inthe evolution, maintenance, and frequency of mutualisticor pathogenic interactions [32]. Another application mightbe in coupling trait information with the comparisons ofroot-infecting fungal communities among invasive plantsin their native and introduced ranges: such informationmay help explain the alleged reduction of pathogen attackof invasive plants in the introduced ranges if infectingfungi do not possess the traits to effectively exploit thenew host [33].

A trait-based approach for the saprotrophic–symbioticcontinuum may better capture the importance of root-infecting fungi in carbon and nutrient cycling at the

Table 1. Examples of traits that are potentially important for characterizing fungi that fall along the symbiotic and saprotrophiccontinuum

Fungal traits Description and rationale Refs

Production of cell wall degrading enzymes They broaden the spectrum of carbon sources for saprotrophic growth, but at the

same time they trigger host defenses as a result of disruption of cell walls in living

cells.

[60]

Lignolytic ability The ability to decompose lignin (e.g., by white rot saprotrophs) expands availability

of carbon substrates in woody systems. This trait seems rare in ectomycorrhizal

fungi.

[61]

Antibiotic production Key traits to cope with interference competition by fungi and bacteria are the

production of antibiotics as well as the enzymes that degrade them.

[62]

Palatability Soil fungi may produce toxic metabolites, melanin, or crystalline cell inclusions to

avoid fungivory by soil animals.

[26]

Resting structures Resting structures permit survival under adverse conditions: a lack of appropriate

hosts or inadequate carbon sources. Whether this is more or less likely in endophytic

fungi is not known, and may depend on root or plant longevity.

[63]

Dispersal/transmission mode Root symbiotic fungi have both vertical and horizontal transmission, but how these

transmission modes differ from corresponding dispersal modes of more

saprotrophic fungi is not understood.

[10]

Degradation of antimicrobial

root exudates

Root exudates (either inducible or constitutive) constrain growth patterns of fungal

species and are a component of host resistance. Whether and how they are

degraded is likely to be important in colonization.

[64]

Penetration structures Many symbiotic fungi have specialized structures for initial penetration of host

tissue. These structures also produce physical, enzymatic, and chemical signals that

enable the early infection process.

[65]

Ratio of intercellular to

intracellular colonization

Extensive intercellular growth (apolastic growth) may reflect the ability of fungi to

avoid the disruption of host cell walls, and thus avoid the activation of resistance

responses such as by reactive oxygen species, phenols, pathogenesis-related

proteins, and phytoalexins.

[9]

Perifungal membrane Some symbionts have structures that include the invagination of plant membranes

(e.g., haustoria and arbuscules), but such invaginations may also occur in fungi with

saprotrophic abilities (e.g., Piriformospora indica).

[66,67]

Induction of host cell wall reinforcements Cell wall thickening is one of the first general responses against pathogen invasion.

The ability to avoid or prevent such responses during hyphal penetration may be

essential for a symbiotic lifestyle.

[68]

Phytotoxin production and

detoxification enzymes

Some fungi depend on the production of phytotoxins and the ability to degrade

plant-derived antimicrobial compounds for successful entry.

[60,69]

Fungal invertases Symbiotic fungi can obtain sugars from the host by either secreting fungal

invertases or by being reliant on plant invertases. Fungal invertases are seemingly

absent in ectomycorrhizal symbionts.

[70]

Transporter traits and their expression In some fungi, establishment of symbiosis requires effective exchange of resources

with the host plant. Gene expression is regulated in fungi based on their location in

the host cells, the compounds being transported, and the direction of transport.

Although such processes are well established in mycorrhizal associations, there is

little evidence whether other root symbionts exhibit similar mechanisms of resource

exchange.

[21,50]

Extraradical mycelia and ‘foraging’ pattern Root fungal symbionts often maintain dual growth in the root and the soil. Allocation

of biomass to the extraradical mycelium and the spatial distribution of hyphae in soil

affect the transfer of nutrients. Several morphological ‘foraging types’ have been

identified in ectomycorrhizae and are likely in other root symbionts.

[55,71,72]


435


ecosystem level, in a manner completely analogous to theuse of ‘functional trait analysis’ in plants [34,35]. Little iscurrently known about the effects of fungal trait diversityon ecosystem processes, although the recent frameworksproposed for mycorrhizal associations [36,37] suggest thatother root-inhabiting fungi may be important contributorsto ecosystem function. Trait-based approaches would allowthe recognition of factors that correlate with the mainecosystem processes to identify the taxa driving such effectsand lead to a better understanding of ecosystem drivers.

Trait measurement and storage of trait information inhigh quality databasesThe full application of any trait-based approach dependson the accessibility of databases that are well-curated,well-funded, and linked to genomic and phylogenetic infor-mation. Phylogenetic databases have already been createdfor taxonomic purposes (e.g., UNITE [38]; http://www.dee-my.de for ectomycorrhizal fungi). Thus, there is an excel-lent window of opportunity to integrate trait informationgenerated from morphological and physiological character-ization of newly isolated fungi with such platforms. Traitsare measured on particular individuals, and meaningfulextrapolations to species (or higher ranks) also depend onhaving estimates of trait variability among individuals andpopulations, as well as on the adequacy of the speciesconcept for fungi [36].

Additionally, to be meaningful, trait information shouldbe presented together with data on the conditions andcircumstances under which the traits were measured(‘metadata’). Trait information collected from culturablefungi under controlled conditions is useful to quantify aparticular trait (e.g., phytotoxin production). Analogously,plant ecologists have populated trait databases with mea-surements from controlled experimental conditions withstandardized methods [39]. This level of control enablesthe use of meta-analytical tools to filter out the effect ofvariable conditions and to better address broad-scale func-tional diversity–ecosystem functioning questions [14].

Coupling this approach with in situ trait measurementsunder natural conditions (in mesocosms or the field) andwith species abundance data will allow estimates of thecontribution of a species in the context of environmentalvariability. Furthermore, in situ measurement of intras-pecific trait variability could be used to refine models ofcommunity assembly [40]. However, caution must be takenwhen such trait information is intended to be used outsidethe particular system from which the traits were mea-sured. It has been shown that traits with high levels ofplasticity and measured from extreme habitats divergefrom mean values in databases [41].

In situ measurements are the only option to incorporatetrait information for non-culturable fungi and are analo-gous to measurements for long-lived plant species (e.g.,wood traits for tree species in the TRY database [42]).Hyphal length in soil or nutrient concentration in thehyphae can be measured following extraction of hyphaedirectly from the environment or from substrate-filledcompartments [43,44]. Enzyme activity assays performedon ectomycorrhizal root tips [45] or fungal carbon sub-strate usage by fungi [46] are usually measured on excised

material, but they may not accurately reflect process ratesdue to the effects of the manipulations. Meta-transcrip-tomic and other gene expression profiling approaches arepromising and have the potential to lead to major insightsat the community level [47,48] and would be especiallyvaluable if these could be targeted at fungal gene expres-sion in particular. More sophisticated approaches at theindividual level using ‘omics’ tools (e.g., single cell geno-mics [49] and laser microdissection [50]) that can simul-taneously examine fungal characters and identify thespecies being examined hold exciting promise for futurestudies of soil fungal communities.

Concluding remarksRigorous comparative studies linked with phylogeneticinformation that is focused on traits, rather than qualitativecategories, are necessary to determine what constitutes anadaptation to a particular lifestyle. In turn, traits can beused to make predictions about the impact and causes ofcommunity structure, and traits that strongly influenceecosystem function can be highlighted and measured forpredicting outcomes. In this opinion paper, as illustrated inFigure 1, we advocate a more objective trait-based approachto characterizing the processes involved in the interactionsof root- and soil-inhabiting fungi, and hence provide a way toassess their importance at the evolutionary, community,and ecosystem levels. Others have strongly supported theuse of trait-based approaches to move forward research onplant–fungal interactions [51,52] and on microbial ecology[53]. In particular, there has been a recent call to explicitlyuse conceptual frameworks from functional ecology inresearch on ectomycorrhizas, promoting the integration ofthis important fungal group into research on linking diver-sity with ecosystem functioning.

Although broad categories have their place in the initialdevelopment of a discipline, they provide a rather abstractview of multicomponent processes at such a level of sim-plicity that they may actually inhibit understanding. Instudies of root-inhabiting fungi, there has been a tendencyto use qualitative categories to describe the saprotrophic–symbiotic continuum, rather than search for generaliza-tions that come from more quantitative studies. Here, weadvocate a trait-based approach to understand the evolu-tionary ecology of root-inhabiting fungi and illustrate howthis approach promises a clear way forward in this complexand technically difficult field.

AcknowledgmentsWe thank the Alumni Network Program of Freie Universitat Berlin forfunding. C.A.A-T. was also supported by the German Academic ExchangeService (DAAD), I.C.A. by a fellowship from the German Federal Ministryof Education and Research, and J.A. by an Alexander von HumboldtResearch Award. We thank Sarah Hortal, Anna Simonin, Jen Walker,Erik Verbruggen, and anonymous reviewers for constructive comments.

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Plant Science Conferences in 2014

4th Pan-American Congress on Plants and BioEnergy4–7 June, 2014

Guelph, Canada

http://my.aspb.org/BlankCustom.asp?page=Bioenergy2014

The 8th Scandinavian Plant Physiology Society PhD Students Conference16–19 June, 2014

Uppsala, Sweden

http://phd2014.spps.fi/

ESF-EMBO SymposiumBiology of plastids – towards a blueprint for synthetic organelles

21–26 June, 2014

Pultusk, Polen

http://bioplastids.esf.org/programme.html

Plant Biology Europe FESPB/EPSO 2014 CongressLearning from the past, preparing for the future

22–26 June, 2014

Dublin, Ireland

http://europlantbiology.org/


438

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