Interactions of arboreal yeast endophytes: an unexplored discipline

Fungal Ecology xxx (2016) 1e10

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Interactions of arboreal yeast endophytes: an unexplored discipline Leandra Moller, Barbra Lerm, Alfred Botha* Department of Microbiology, Stellenbosch University, Stellenbosch, Western Cape, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 June 2015 Received in revised form 16 January 2016 Accepted 10 March 2016 Available online xxx

The value of healthy forest ecosystems is well known and trees in these systems form symbioses with a variety of living organisms. This review focuses on literature pertaining to the potential interactions of arboreal yeast endophytes with trees and their associated insects. Although very little is known about the symbioses of arboreal yeast endophytes, indications are that some of these unicellular fungi produce plant-growth promoting phytohormones, while others are antagonistic towards phytopathogens or are capable of producing pheromones that affect the behavior of insect herbivores. However, more research needs to be conducted to fully understand the role of arboreal yeast endophytes in ecosystem processes. © 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.

Corresponding editor: Peter E. Mortimer Keywords: Ants Endophytic yeasts Fungi Phytohormones Symbiosis Trees

1. Introduction It is known that healthy forest ecosystems are invaluable to the planet and all of its inhabitants, including humans (Krieger, 2001; Farber et al., 2002). Such forests are described as complex (Bengtsson et al., 2000; Franklin et al., 2002) and may include a wide diversity of trees that may form symbioses with many different living organisms (Carroll, 1988). These associations may be classified as either ecto- or endophytic, depending on whether the symbionts occur on the plant surface (phylloplane and rhizoplane) or whether they are associated with the internal tissues of plants (Rodriguez et al., 2004, 2009). Endophytic microorganisms are viewed as those that refrain from causing disease in their host (Wilson, 1995; Porras-Alfaro and Bayman, 2011), while often playing a pivotal role in plant survival. Studies aimed at revealing the role of these microorganisms have mainly focused on bacteria and filamentous fungi, thus often neglecting a ubiquitous group of unicellular fungi e yeasts (Schulz et al., 1993; Wearn et al., 2012). Yeasts are a polyphyletic group of fungi that primarily proliferate via asexual budding or cell fission (Kurtzman and Fell, 1998). However, some yeasts are also able to reproduce sexually by forming meiospores that are carried either on a basidium or within

an ascus. These meiosporangia, in contrast to those of macrofungi, are never enclosed within fruiting bodies. The unicellular nature of yeasts is viewed as an adaptation to growth in aqueous environments, where yeasts may either reproduce in suspension or as part of a biofilm attached to various submersed surfaces, including the walls of xylem vessels, as depicted in Fig. 1 (Decho, 1990; Lachance
nyik et al., 2004; Joubert et al., 2006; Gai and Starmer, 1998; Bra et al., 2009). It is well known that yeasts may associate with both the phylloplane and rhizoplane, where they interact with a variety of organisms and their physiochemical environment (Lindow and
cio, 2006; Botha, 2011; Starmer and Brandl, 2003; Fonseca and Ina Lachance, 2011). However, little is known about the interactions and roles of endophytic yeasts, especially those associated with trees. Since knowledge of plant-microbe symbioses is an important prerequisite for sustainable management of terrestrial ecosystems (Requena et al., 2001; Finlay, 2008), the overall objective of this study was to review the current state of knowledge on the ecology of arboreal yeast endophytes. The role of these yeasts within their natural habitat will be explored, including some of their potential interactions with trees and arboreal insects. Furthermore, future directions in the field of arboreal endophytic yeast ecology will be discussed.

* Corresponding author. E-mail address: [email protected] (A. Botha). http://dx.doi.org/10.1016/j.funeco.2016.03.003 1754-5048/© 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.

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L. Moller et al. / Fungal Ecology xxx (2016) 1e10

Fig. 1. An illustration of yeasts colonizing xylem vessels. Some yeasts occurring in these vessels (Gai et al., 2009; Khan et al., 2012) can utilize a wide diversity of simple nutrients (Kurtzman and Fell, 1998), such as amino acids, nitrate, carbohydrates and organic acids, thereby potentially altering the chemical composition of xylem sap. Additionally, the yeasts might produce phytohormones, such as indole-3-acetic acid and polyamines (Reyes-Becerril et al., 2011; Waqas et al., 2012), which are subsequently secreted into the sap. Bar ¼ ca.10 mm.

2. Functional roles of arboreal yeast endophytes Yeasts are known for their ability to produce a variety of me
nez-Díaz, tabolites, for example vitamins (Ruiz-Barba and Jime 1995; Leathers and Gupta, 1997), enzymes (Table 1) and hormones (Table 2). These metabolites may play a pivotal role in the interactions of yeast endophytes (Fig. 2) with other organisms. Recently, the knowledge of the diversity of endophytic yeasts was extensively reviewed (Doty, 2013), and the vast untapped biotechnological potential of these unicellular fungi was emphasized. In addition, the author highlighted endophytic yeast diversity of tree aerial organs, which was found to represent a wide diversity of ascomycetous and basidiomycetous yeasts belonging to the genera Candida, Cryptococcus, Cystofilobasidium, Debaryomyces, Filobasidium, Guehomyces, Meyerozyma, Rhodotorula, Sporobolomyces and Sporidiobolus. In more recent literature (Scholtysik et al., 2013; Solis et al., 2015) the endophytic status of some yeast species was corroborated, while it was revealed that other yeast species can also exist as tree endophytes (Table 1). To date, arboreal yeast endophyte research has primarily focused on the assessment of diversity, with a dearth of information on the functional role of these unicellular fungi in their host's biology. In contrast, bacterial and filamentous fungal endophytes are more researched, with most knowledge on the functional roles of endophytes stemming from research conducted on filamentous fungal endophytes of grasses (Porras-Alfaro and Bayman, 2011) and €, 2011). Nevertheless, the funcbacterial root endophytes (Pirttila tional roles of bacterial and filamentous fungal endophytes in leaves and stems of trees have been elucidated in some studies €, 2011). Considering (Brooks et al., 1994; Taghavi et al., 2009; Pirttila the evidence for convergent evolution between bacteria and yeasts (Bork et al., 1993; Brazhnik and Tyson, 2006), as well as between filamentous fungi and yeasts (Berbee and Taylor, 1992), the potential roles of arboreal yeast endophytes (Table 2) can be inferred from literature on bacterial and filamentous fungal tree

endophytes. It is known that endophytes can positively benefit their hosts €, through production of plant-growth promoting hormones (Pirttila 2011) and through antagonism against phytopathogens (Mengoni et al., 2003). Bacterial endophytes can mediate tree growth through the production of phytohormones, such as giberellins, €, 2011). For example, Taghavi et al. cytokinins and auxins (Pirttila (2009) demonstrated that bacterial endophytes, originating from a poplar hybrid (Populus trichocarpa
Populus deltoides) could improve the growth of another poplar hybrid (P. deltoides
Populus nigra) and ascribed this to the production of the auxin, indoleacetic acid (IAA), by the bacteria. However, representatives of some yeast species are also able to produce IAA in vitro (Table 2), and it was demonstrated that plant growth was improved when some of these yeasts, i.e. Cryptococcus laurentii (Cloete et al., 2009, 2010) and Rhodotorula glutinis (El-Tarabily, 2004), were applied exogenously to the rhizosphere. Considering these aspects, it seems likely that some endophytic yeasts might be able to improve their host tree's growth. However, it must be noted that phytohormone production levels may differ among endophytic yeasts, since intraspecific variation exists among yeasts with regard to the production of IAA (Moller et al., unpublished). This phenomenon should, therefore, be taken into account when the effect of these yeasts on tree physiology is studied in future. As mentioned, endophytes may also positively benefit their host through biological control of phytopathogens (Mengoni et al., 2003). In the study conducted by Brooks et al. (1994), it was found that Ceratocystis fagacearum-related crown loss and deaths of Spanish oak (Quercus texana) were reduced when endophytic bacteria, originating from aboveground organs of live oak (Quercus fusiformis), were inoculated into the stems of the trees. Furthermore, these authors demonstrated that the bacterial endophytes could inhibit growth of C. fagacearum in vitro, either through the production of antimicrobial compounds under nutrient-rich conditions or through the production of siderophore-like molecules under iron-limiting conditions. However, bacteria are not the only siderophore-producing microorganisms. It is well known that some yeast species belonging to the genera Rhodotorula and Sporobolomyces can produce the siderophore rhodotorulic acid (Table 2), which has been linked to their antagonistic relationship with various phytopathogens of crop plants and fruits (Calvente et al., 2001a, 2001b; Sansone et al., 2005). In addition, the antagonism of some yeasts towards bacteria, filamentous fungi and other yeast species has been ascribed to the production of killer toxins by these unicellular fungi (Polonelli and Morace, 1986). Interestingly, it was demonstrated that the killer toxin producing yeast Debaryomyces hansenii (Table 2) can inhibit the growth of Ophiostoma piceae and Ophiostoma piliferum on Pinus sylvestris timber (Payne and Bruce, 2001). Yet, the mode of antagonism was not elucidated by the authors. Considering these aspects, it seems plausible that arboreal yeast endophytes might benefit their host by inhibiting phytopathogen growth; various yeast species need to be tested in planta to determine whether this is a common occurrence. From the above it appears that arboreal yeast endophytes may play a vital role in the biology of their host trees, yet these interactions are not always confined to dual symbioses between yeasts and trees. In some instances multipartite interactions may occur, especially where insects are involved. 3. Potential multipartite interactions involving insects, trees and yeasts It is known that yeasts are associated with insects and a vast body of information exists on this topic (Reviewed by Suh and Blackwell, 2005; Vega and Dowd, 2005; Ganter, 2006). It is thus

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Table 1 A list of arboreal yeast endophytes and their origin, as well as extracellular enzymes associated with each species.a Endophytic yeast species

Arboreal origin

Candida carpophila Candida conglobata Candida diddensiae Candida parapsilosis Candida railenensis Cryptococcus aerius Cryptococcus albidosimilis Cryptococcus albidus Cryptococcus diffluens Cryptococcus dimennae Cryptococcus flavescens Cryptococcus laurentii

Solanum cernuum S. cernuum S. cernuum Citrus sinensis Quercus rober Populus deltoides Ficus benjamina; Ficus elastica; Ficus religiosa F. benjamina; F. elastica; F. religiosa; Q. rober F. religiosa Fraxinus excelsior C. sinensis; S. cernuum C. sinensis; Malus domestica; S. cernuum

Cryptococcus magnus Cryptococcus rajasthanensis Cryptococcus stepposus Cystofilobasidium capitatum Debaryomyces hansenii

F. benjamina; F. elastica; F. religiosa S. cernuum F. elastica Q. rober M. domestica; Sequoia sempervirens

Filobasidium capsuligenum Filobasidium uniguttulatum Guehomyces pullulans Kwoniella mangroviensis Malassezia restricta Meyerozyma caribbica Meyerozyma guilliermondii Rhodotorula benthica Rhodotorula dairenensis Rhodotorula glutinis Rhodotorula graminis Rhodotorula lysiniphila Rhodotorula minuta Rhodotorula mucilaginosa

Eugenia bimarginata Unspecified S. sempervirens S. cernuum P. deltoides S. cernuum C. sinensis; S. cernuum F. benjamina; F. elastica C. sinensis Q. rober Populus trichocarpa F. benjamina; F. elastica F. benjamina; F. elastica; P. sylvestris C. sinensis; F. benjamina; F. elastica; F. religiosa; F. sylvatica; M. domestica; P. trichocarpa x deltoides Pinus tabulaeformis F. benjamina M. domestica M. domestica

Rhodotorula pinicola Rhodotorula slooffiae Sporobolomyces roseus Sporidiobolus pararoseus

Reference

Vieira et al., 2012 Vieira et al., 2012 Vieira et al., 2012 Gai et al., 2009 Isaeva et al., 2009 Gottel et al., 2011 Solis et al., 2015 Isaeva et al., 2009; Solis et al., 2015 Solis et al., 2015 Scholtysik et al., 2013 Gai et al., 2009; Vieira et al., 2012 Camatti-Sartori et al., 2005; Gai et al., 2009; Vieira et al., 2012 Solis et al., 2015 Vieira et al., 2012 Solis et al., 2015 Isaeva et al., 2009 Camatti-Sartori et al., 2005; Middelhoven, 2003 Vaz et al., 2012 Unterseher et al., 2007 Middelhoven, 2003 Vieira et al., 2012 Gottel et al., 2011 Vieira et al., 2012 Gai et al., 2009; Vieira et al., 2012 Solis et al., 2015 Gai et al., 2009 Isaeva et al., 2009 Xin et al., 2009 Solis et al., 2015 Pirttil€ a et al., 2003; Solis et al., 2015 Camatti-Sartori et al., 2005; Gai et al., 2009; Solis et al., 2015; Unterseher et al., 2013; Xin et al., 2009 Zhao et al., 2002 Solis et al., 2015 Camatti-Sartori et al., 2005 Camatti-Sartori et al., 2005

Extracellular enzyme productionb AMY

CEL

EST

LIP

PECc

PRT

XYL

 NA   V V V V  þ V V

 V NA V V NA  NA  þ V V

NA NA V  V  NA V NA þ V V

  V V V þ þ V þ þ V V

V V   V þ NA V V NA V V

 V V V V V NA V  þ V V

þ NA NA  NA þ þ þ þ NA V V

V   V 

þ  þ V V

þ NA V V V

þ þ V V V

V V  V V

V þ  V V

þ  NA NA NA

þ NA V  NA V  NA  V NA NA  

NA  þ  NA V V NA  V NA NA  V

NA NA NA NA NA NA V NA NA V V NA V V

NA NA V  þ V V NA  V V NA V V

þ NA V V NA V V NA V  V NA  V

þ NA þ NA NA þ V NA  V V NA V V

NA þ NA V NA V V NA   NA NA  V

 V V NA

V V V NA

V V V NA

V V V V

  NA NA

  V 

 NA  NA

a Extracellular enzyme data was taken from: Abranches et al., 1997; Amoresano et al., 2000; Arcuri et al., 2014; Bautista-Gallego et al., 2011; Birgisson et al., 2003; Braga ~o et al., 2011; Brizzio et al., 2007; Buzzini and Martini, 2002; Carvalho et al., 2013; Crognale et al., 2012; Da Silva et al., 2005; De Mot and Verachtert, 1985; et al., 1998; Branda
ho-Kellermann et al., 2011; Herna
ndez-Montiel et al., Fuentefria, 2004; García-Martos et al., 2001; Gildemacher et al., 2004; Goto et al., 1974; Gouliamova et al., 2012; Gue
nez et al., 1991; Kathiresan et al., 2011; Keszthelyi et al., 2008; Laconi and Pompei, 2007; Landell, 2006; Lara et al., 2010; Hirimuthugoda et al., 2006; Hou, 1993; Jime
rova
et al., 2014; Nahvi et al., 2005; Nakamura et al., 2000; Notario et al., 1979; 2014; Loperena et al., 2012; Melo, 2014; Merin et al., 2014; Middelhoven, 1997; Molna
mez et al., 2012; Saha and Bothast, 1996; Scorzetti et al., 2000; Singh et al., 2013; Smaniotto et al., Pavlova et al., 2002; Resende, 2014; Rodarte et al., 2011; Rodríguez-Go 2014; Song et al., 2010; Stevens and Payne, 1977; Strauss et al., 2001; Tan Gana et al., 2014; Trindade et al., 2002; Vaca et al., 2013; Wisniewski et al., 1991; Zullo and Ciafardini, 2008; Zullo et al., 2010, 2013. b PRT (protease); EST (esterase); CEL (cellulase); LIP (lipase); AMY (amylase); PEC (pectinase); XYL (xylanase); NA (data unavailable); V (variable); þ (positive);  (negative). c Includes pectate lyases and polygalacturonases.

not surprising that most arboreal yeast endophytes listed in Table 2 were also isolated from exoskeletons, frass, guts, haemolymph, as well as fungal gardens, of different insects. Various roles were ascribed to yeast symbionts of insects, such as providers of digestive enzymes, suppliers of essential amino acids and vitamins, as well as detoxifiers of toxic plant metabolites (Vega and Dowd, 2005). These interactions are, however, not limited to the bipartite symbioses between insects and yeasts, but may also be extended to multipartite associations when additional microorganisms are involved. A potential multipartite symbiosis involving arboreal yeast endophytes is the interaction between trees, bark beetles (Coleoptera: Scolytidae: Scolytinae) and their associated blue stain fungi. The association between bark beetles and blue stain fungi, as well as the subsequent effect on trees, has been extensively researched (Reid et al., 1967; Ballard et al., 1984; Yousuf et al., 2014). This association is, however, multipartite as it also involves some yeasts not known to

be endophytic, such as Kuraishia capsulata and Ogataea pini, which produce semiochemicals that affect the aggregation of bark beetles (Reviewed by Davis, 2015). These yeasts may also interact positively or negatively with the filamentous fungi associated with bark beetles (See Davis, 2015). Yet, it seems probable that arboreal yeast endophytes may also partake in this multipartite interaction, based on the isolation of some yeast species, i.e. Candida diddensiae, Cryptococcus diffluens, C. laurentii, Cryptococcus magnus and Meyerozyma guilliermondii, from trees as well as bark beetles (Table 2). Since, the isolation of these yeasts (except M. guilliermondii) from bark beetles (Shifrine and Phaff, 1956;
n et al., 1984; Giordano et al., 2013; Bridges et al., 1984; Leufve Lou et al., 2014) seems to be rare, it is tempting to speculate that the yeasts are not bark beetle symbionts, but that they originate from the host tree instead. Nevertheless, until yeast endophytes are isolated from coniferous trees, this theory remains uncorroborated. If yeasts, such as C. diddensiae, C. diffluens and C. magnus, are found

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Table 2 The ability of yeast species, representing arboreal yeast endophytes, to produce the phytohormone indole-3-acetic acid (IAA) and siderophores, to exert killer activity and antagonism against phytopathogens, as well as their known association with insects. The data was obtained from literature.a Endophytic yeast IAA Antagonism against phytopathogens species productionb Candida carpophila Candida conglobata Candida diddensiae Candida parapsilosis Candida railenensis Cryptococcus aerius Cryptococcus albidosimilis Cryptococcus albidus Cryptococcus diffluens Cryptococcus dimennae Cryptococcus flavescens Cryptococcus laurentii

Cryptococcus magnus Cryptococcus rajasthanensis Cryptococcus stepposus Cystofilobasidium capitatum Debaryomyces hansenii

Filobasidium capsuligenum Filobasidium uniguttulatum Guehomyces pullulans Kwoniella mangroviensis Malassezia restricta Meyerozyma caribbica Meyerozyma guilliermondii

Rhodotorula benthica Rhodotorula dairenensis Rhodotorula glutinis Rhodotorula graminis

Siderophore Killer Insect association production activity

þ

NA

NA

V

þ

NA

NA

NA

NA

NA

NA

V

þ

Aspergillus flavus; Aspergillus parasiticus; Aspergillus sojae þ

V

NA

Ustilago maydis

NA

NA

Hypothenemus hampei guts, feces, cuticles and galleries; Ips typographus gut Apis mellifera gut; Atta laevigata exoskeleton; Apis mellifera nests; Drosophila melanogaster crop; Leptura rubra midgut; Solenopsis invicta haemolymph Aphaenogaster senilis and Pheidole pallidula exoskeletons

NA

NA



V

Atta sexdens fungal garden

NA

NA

NA

NA



V

NA

Fusarium oxysporum; Fusarium proliferatum; Phialocephala virens A. flavus; Botryodiplodia theobromae; Botrytis cinerea; Penicillium expansum NA



NA

A. sexdens fungal garden; A. mellifera, C. hemipterus and Cotinis nitida guts; Drosophila sp. crop Dendroctonus sp. and I. typographus guts

NA

NA



NA

Apis florea honey gut

þ

Colletotrichum graminicola; Escovopsis sp.; Fusarium  graminearum; Gibberella zeae; Septoria nodorum Alternaria alternata; Aspergillus niger; B. cinerea; Fusarium  sambucinum; Fusarium solani var. coeruleum; Monilinia fructicola; Penicillium digitatum; P. expansum; Penicillium italicum; Rhizopus stolonifer



NA

þ

B. cinerea; Colletotrichum gloeosporioides; Escovopsis sp.;  M. fructicola; NA NA

NA

A. sexdens and Atta texana fungal gardens; A. sexdens male integument; O. nubilalis gut Atta bisphaerica, A. sexdens, A. texana, Mycocepurus goeldii and Trachymyrmex sp. fungal gardens; Atta capiguara and A. laevigata exoskeletons; A. sexdens male integument; Camponotus vicinus infrabuccal pocket; Dendroctonus frontalis larval gallery; I. typographus homogenate A. texana fungal garden; Dendroctonus valens and P. pallidula exoskeleton I. typographus gut A. sexdens male integument

NA

NA

NA

NA

NA

NA

B. cinerea

NA

V

NA

NA

NA B. theobromae; B. cinerea; Geotrichum candidum; Ophiostoma piceae; Ophiostoma piliferum; P. digitatum; P. italicum; Rhizopus microsporus

V

NA

B. cinerea



V

Aethina concolor, A. senilis, Crematogaster auberti, Drosophila floricola and Formica rufa exoskeletons; A. mellifera and C. nitida guts; A. sexdens fungal garden; A. sexdens male integument; C. vicinus nest and frass; S. invicta haemolymph NA

NA

B. cinerea

NA

V

NA

NA

A. alternata; B. cinerea; P. expansum

þ

V

NA

NA

NA

NA

NA

NA

NA

NA

NA

NA

þ

B. cinerea; R. stolonifer

NA

NA

þ

B. theobromae; B. cinerea; P. digitatum; P. italicum; Penicillium roqueforti

NA

þ

NA

NA

NA

NA

Neomida sp. and Triplax sp. guts; Xyleborus crassiusculus, Xyleborus ferrugineus and Xyleborus affinis mycangia Aedes aegypti crop; A. sexdens and M. goeldii fungal gardens; Brachypeplus glaber and Megalodacne sp. guts Acromyrmex sp. nest; A. aegypti, Dendroctonus brevicomis, Dendroctonus mexicanus, Dendroctonus pseudotsugae, Dendroctonus rufipennis and D. valens midguts; A. sexdens fungal garden; C. vicinus exoskeleton, frass, infrabuccal pocket and nest; Chauliodes cornutus exoskeleton and gut; Chauliodes rastricornis, Ips pini homogenate, O. nubulalis and Ululodes macleayanus guts; M. goeldii and Trachymyrmex sp. fungal gardens NA

þ

NA

þ

V

NA

þ

A. niger; A. alternaria; B. cinerea; P. digitatum; P. expansum; P. italicum; Pezicula malicorticis; R. stolonifer

þ

þ

þ

Monilinia vaccinii-corymbosi

þ

V

A. mellifera honey stomach and feces; A. laevigata fungal pellet, A. sexdens fungal garden, C. vicinus frass and nest; C. nitida gut; Helicoverpa armigera gut Apis dorsata and Xylocopa sp. honey stomachs

NA

þ

NA

V

Carpophilus hemipterus, Diabrotica virgifera virgifera and Ostrinia nubilalis guts; Xestobium plumbeum mycetome NA

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Table 2 (continued ) Endophytic yeast IAA Antagonism against phytopathogens species productionb

Siderophore Killer Insect association production activity

Rhodotorula lysiniphila Rhodotorula minuta Rhodotorula mucilaginosa Rhodotorula pinicola Rhodotorula slooffiae Sporobolomyces roseus Sporidiobolus pararoseus

NA

NA

NA

NA

NA



C. gloeosporioides; P. digitatium; P. italicum

V



A. mellifera gut

þ

þ

V

A. mellifera and C. nitida guts; A. sexdens fungal garden; A. texana nest; C. hemipterus exoskeleton

NA

Arthrobacter globiformis; B. cinerea; Fusarium vasinfectum; P. digitatum; P. italicum; Verticillium alboatrum; Verticillium dahliae; NA

NA

NA

I. typographus gut

NA

B. cinerea

NA

NA

NA

NA

B. cinerea; C. graminicola; P. expansum

þ

þ

A. sexdens fungal garden; O. nubilalis gut

NA

B. cinerea; M. fructicola; P. italicum

NA

þ

C. vicinus nest soil

a Data on IAA production, phytopathogen antagonism, siderophore production, killer activity and insect associations of yeasts were taken from: Abranches et al., 1997; Afsah-Hejri, 2013; Akhtyamova and Sattarova, 2013; Arcuri et al., 2014; Arras et al., 1998, 1999; Atkin et al., 1970; Ba and Phillips, 1996; Bridges et al., 1984; Buck and Jeffers, 2004; Calvente et al., 1999, 2001; Campos Guzman, 2010; Carreiro et al., 1997, 2002; Chalutz and Wilson, 1990; Chand-Goyal and Spotts, 1996; Cline et al., 2014; Cook, 1997, 2002a, 2002b; De Camargo and Phaff, 1957; De Capdeville et al., 2007; De Vega et al., 2014; Droby et al., 1989, 1993, 1997; El-Tarabily, 2004; Elad et al., 1994; Filonow, 1999, 2001; Filonow et al., 1996; Fokkema and van der Meulen, 1976; Gilliam et al., 1974; Giordano et al., 2013; Golubev, 2006; Golubev and Bab'eva, 1972; Golubev et al.,
zquez et al., 2009; Gusm~ 1988; Guetsky et al., 2002; Guevara-Va ao et al., 2007, 2010; Hashem et al., 2014; Helbig, 2002; Hern
andez-Montiel et al., 2010, 2012; Huang et al., 2012; Janisiewicz and Bors, 1995; Janisiewicz et al., 1994, 2010; Jiang et al., 2009; Jones et al., 1999; Jurzitza, 1959; Kalogiannis et al., 2006; Khan et al., 2004; Knoth et al., 2014;
n and Nehls, 1986; Leufve
n et al., 1984; Lim et al., 2005; Lima et al., 1998; Limtong and Kostovcik et al., 2015; Lachance et al., 2001; Langdon, 2009; Leibinger et al., 1997; Leufve
r Koowadjanakul, 2012; Llorente et al., 1997; Lou et al., 2014; Maharshi et al., 2009; Mankowski and Morrell, 2004; Mashope, 2007; Melo, 2014; Miller and Mrak, 1953; Molna et al., 2008; Morace et al., 1984; Mushtaq et al., 2013; Nguyen et al., 2007; Niknejad et al., 2012; Nutaratat et al., 2014; Ortega, 2012; Pagnocca et al., 2008; Patino-Vera et al.,
rez et al., 2003; Petersson and Schnurer, 1995; Pirttila € et al., 2004; Prillinger et al., 1996; Qin and Tian, 2005; Qin et al., 2003, 2006; Rao et al., 2005; Payne and Bruce, 2001; Pe 2007; Redmond et al., 1987; Resende, 2014; Rivera et al., 2008, 2009; Roberts, 1990; Rodrigues et al., 2009; Saksinchai et al., 2012; Sandhu and Waraich, 1985; Sansone et al., 2005; Santos et al., 2004; Sanz Ferramola et al., 2013; Schisler et al., 1995; Shifrine and Phaff, 1956; Starmer et al., 1976; Sugiprihatini et al., 2011; Suh and Blackwell, 2004; Surussawadee et al., 2014; Sweet and Douglas, 1991; Taqarort et al., 2008; Tian et al., 2004, 2007; Trindade et al., 2002; Vega and Dowd, 2005; Vishniac and Johnson, 1990; Williamson and Fokkema, 1985; Wisniewski et al., 1991; Wszelaki and Mitcham, 2003; Xin et al., 2009; Yao et al., 2004; Yu et al., 2008; Zhang et al., 2003, 2004a, 2004b, 2005; Zhang et al., 2007a, 2007b; Zhang et al., 2007; Zhao et al., 2012; Zheng et al., 2005. b NA (Data unavailable); V (variable); þ (positive);  (negative).

to be endophytes of conifers, they might play a role in the aggregation of beetles onto their host tree. This hypothesis is based on
n et al. (1984), who isolated these yeast species the work of Leufve from the hindgut of the Eurasian spruce bark beetle (Ips typographus) and demonstrated that the yeasts could partly convert the

Fig. 2. Dark field light microscopy of a root cross section from the sclerophyll Agathosma betulina, stained with Lugol's iodine solution, revealed dark stained endophytic yeast cells within the cortex of the root. The yeast was identified as Meyerozyma guilliermondii using molecular techniques (Cloete et al., 2010). Bar ¼ 20 mm. (Photo was generously provided by Dr. K. J. Cloete).

aggregation pheromone cis-verbenol (Sun et al., 2006) to the aggregation pheromone trans-verbenol and the anti-aggregation
n and pheromone verbenone, in vitro. In addition, Leufve Birgersson (1987) estimated that yeasts present in the galleries of I. typographus were responsible for the production of verbenone. Therefore, volatile production by C. diddensiae, C. diffluens and C. magnus can potentially affect the aggregation of I. typographus
n et al., 1984) on its host, Norway spruce (Picea abies; (Leufve Christiansen and Bakke, 1988). Ultimately, the yeast endophytes might gain from such a multipartite interaction by being dispersed to new habitats by emerging adult beetles. M. guilliermondii, however, might be a symbiont of bark beetles, since this yeast is associated with the guts of a wide range of beetles (Suh and Blackwell, 2005; Suh et al., 2005), including that of different Dendroctonus beetles (Lim et al., 2005; Rivera et al., 2008, 2009; Cardoza et al., 2009; Campos Guzman, 2010). Interestingly, M. guilliermondii was found to transform a-pinene to cis-verbenol (Campos Guzman, 2010) in vitro, thus if this yeast is found to be a conifer endophyte, it might assist in the attraction of bark beetles to their host trees. It is thus evident that the isolation of yeast endophytes from healthy tree hosts of bark beetles are imperative in the future, as these unicellular fungi may ultimately be found to play a role in bark beetle ecology, which inevitably impacts silviculture. Another potential multipartite association that may ultimately be found to impact trees, and consequently forestry, is that between leaf-cutter ants (Acromyrmex and Atta), their fungal symbionts and other microorganisms occurring within the ants' fungal gardens. Within the fungal gardens, leaf-cutter ants cultivate their sole food source, the basidiomycetous fungus Leucoagaricus gongylopharus (Pagnocca et al., 2008; Schultz and Brady, 2008; Rodrigues et al., 2009, 2014; Ward et al., 2015), by continually supplying it with fresh leaf material for growth. These fungal gardens are, however, not limited to the mutualistic fungus and were

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found also to harbour bacteria, yeasts and other filamentous fungi (Craven et al., 1970; Bacci et al., 1995; Pagnocca et al., 1996; Carreiro et al., 1997, 2002; Rodrigues et al., 2008, 2014). Moreover, bacteria belonging to the genus Pseudonocardia, associated with leaf-cutter ants (Currie et al., 1999b; Cafaro and Currie, 2005), were also demonstrated to be antagonistic to the main fungal pathogen of leaf-cutter ant fungal gardens, i.e. Escovopsis (Currie et al., 1999a). In addition, various roles were proposed for yeasts involved in this multipartite interaction, i.e. assistance with the breakdown of plant polysaccharides (Carreiro et al., 2002; Arcuri et al., 2014), detoxification of built up metabolic compounds (Mendes et al., 2012), regulation of fungal populations in the gardens (Arcuri et al., 2014), and protection of the gardens against fungal pathogens (Rodrigues et al., 2009). Considering that the arboreal yeast endophytes listed in Table 2 were regularly isolated from leaf-cutter ants, it seems that yeast endophytes might gain more from their ant hosts than just nutrition. Ants are known to carry yeasts on their exoskeleton (De Vega and Herrera, 2012) and it is thus likely that leaf-cutter ants may facilitate the dispersal of yeasts present in their fungal gardens to new trees during foraging. In addition, leaf-cutter ants may potentially inoculate tree leaves with these yeasts, which in turn may become endophytic when entering the tree's vascular system. Since several yeasts associated with leaf-cutter ants may produce IAA, siderophores or even inhibit phytopathogens (Table 2) research on the interactions between these yeasts, leaf-cutter ants and trees would be expedient. 4. Conclusion During the past decade, most research on arboreal endophytic yeasts consisted of identifying these unicellular fungi without much emphasis being placed on their function in the ecosystem. In the relatively few cases where interactions of these yeasts were studied, in vitro experiments were conducted on non-endophytic strains in unrelated research fields. Nevertheless, a wide diversity of complex interactions might occur between arboreal yeasts and biotic factors. This review highlighted these interactions and summarized some known and potential functions of endophytic yeasts that were isolated from trees (Table 2). Clear indications exist that arboreal endophytic yeasts may exert a positive effect on tree health; however, no research to date has been directed at highlighting the functional role of these yeasts within trees. Future studies should, therefore, focus on determining the effect of individual yeast strains on tree performance with regard to growth, physiology, yield, and resistance towards phytopathogens. In future, the challenge will, however, be to determine the actual contribution of endophytic yeasts to ecosystem processes relative to that of endophytic filamentous fungi and bacteria. Additionally, complex interactions such as those between these yeasts, trees and arboreal insects should be studied to fully understand the role of endophytic yeasts in arboreal ecosystems. Ideally, such knowledge gained from experiments should be conducted under field conditions. Technological advances in DNA sequence analyses of total community DNA (Hunt et al., 2004; Zachow et al., 2008), especially next-generation sequencing technologies (Shokralla et al., 2012; Lindahl et al., 2013) may be used in conjunction with culturing techniques for this purpose. However, these studies should be conducted taking into account the limitations of both culturing and modern molecular analyses (Ellis et al., 2003; Spiegelman et al., 2005; Lindahl et al., 2013), including the selectivity of culture media and the bias of screening only for selected taxonomic informative gene sequences with molecular techniques. In addition, € et al., fluorescence in situ hybridization (Spear et al., 1999; Pirttila 2000) may be used to visualize yeasts while growing within plant tissues. A full understanding of the role of arboreal yeast endophytes

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Please cite this article in press as: Moller, L., et al., Interactions of arboreal yeast endophytes: an unexplored discipline, Fungal Ecology (2016), http://dx.doi.org/10.1016/j.funeco.2016.03.003