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Mycologia, 101(6), 2009, pp. 823–832. DOI: 10.

# 2009 by The Mycological Society of America, Lawrence, KS 66044-8897

Phenotypic plasticity in fungi: a review with observations on
Aureobasidium pullulans
Ralph A. Slepecky
William T. Starmer1

sources include glass (Schabereiter-Gurtner et al
2001), painted material (Shirakawa et al 2002), as
well as rocks and marble (Urzı` et al 1999, 2001). It is
found in soil, freshwater and saltwater, ice (Zalar et al
2008) and is commonly recovered from the atmosphere (e.g. Shelton et al 2002, Lugauskas et al 2003,
Griffin et al 2003, Samson et al 2004) and above (i.e.
the Mir space station, Alekhova et al 2005). Unusual
sources of A. pullulans, often as a contaminant,
include for example samples containing ancient DNA
(Hauf et al 1995), aviation fuel (Rauch et al 2006),
spacecraft (La Duc et al 2003) and damaged nuclear
reactors (Zhdanova et al 2000). Aureobasidium pullulans is involved as the principal colonizer initiating
biodeterioration (e.g. plasticized polyvinyl chloride,
Webb et al 2000) has been used as an indicator of
environmental pollution (Deshpande et al 1992) and
is implicated in human disease (Taylor et al 2005).
The pleomorphic characteristic of fungi (Savile
1969) is also know as ‘‘phenotypic plasticity’’, that is
the ability of any organism to respond to environmental signals by altering morphology, physiological
state or behavior (West-Eberhard 1989). This ability is
widespread among taxa and has been studied
extensively primarily because of its importance to an
organism’s ability to survive and propagate. The
function that describes the range of phenotypes
produced by a single genotype in a suite of
environments is called a ‘‘reaction norm’’ and is a
concept generally adopted by geneticists studying
evolution and ecology (Pigliucci 1996). Because over
their lifetimes organisms occur in changing environmental conditions they are expected to have reaction
norms that scale to the variable environment they
inhabit and thus the individual is expected to be
phenotypically plastic. What determines the shape of
the reaction norm and how the change from one
phenotype to another occurs are central questions in
molecular, evolutionary and ecological genetics.
Pigliucci (1996) discusses two broad approaches to
studying phenotypic plasticity. One is statistical, which
uses the tools developed by students of quantitative
genetics. The major limitation of this method is that
the assumptions underlying the theory are often too
simple and as a consequence inferences about genetic
mechanisms can be unrealistic. The second approach
is a mechanistic study of the genes involved in
phenotypic plasticity. The initial phase of this
approach is to use a genetic screen designed to

Department of Biology, Syracuse University, Syracuse,
New York 13244

Abstract: Phenotypic plasticity in fungi is reviewed in
the context of observations on phenotypic changes in
the colony morphology of the fungus Aureobasidium
pullulans. The variation in colony form is shown to
depend on (i) the types of single carbon substrates
(sugars and sugar alcohols) used in the growth
medium, (ii) colony age, (iii) incubation temperature, (iv) light cycle and (v) substrate type. Expanding
colonies grow in a developmental sequence that show
synchronize growth phase shifts as well as unusual
transitions from homogeneous to sectored, yeast to
mycelial and giant to microcolonial growth forms.
Epigenetic influences on phenotypic switches are
suggested to be potential causes of form changes. The
desirable properties of a model organism for studying
phenotypic plasticity are discussed and past work on
the yeast-mycelial transition of fungi is reviewed.
Key words: epigenetics, model organism, yeastmycelial transition

Fungi are notable for their ability to switch growth
forms in response to environmental stimuli (Rayner
and Coates 1987). Most likely fungi rely on the
capacity to make these shifts to achieve survival,
dispersal and reproductive advantages, and no doubt
their success at these fundamental processes helps
explain their recognition as a kingdom. The ability of
fungi to alter forms and shift to different modes of
living has been of interest to mycologists because of
their importance to understanding fungal molecular
biology, ecology and evolution as well as their utility
in industry and their role in both infection and
biological control. One fungus that assumes many
different shapes (i.e. it is pleomorphic) and lives in a
wide variety of habitats is Aureobasidium pullulans.
This fungus has been recovered from diverse surfaces
types, especially the phylloplane (Andrews et al 2002,
McGrath and Andrews 2007, Andrews and Harris
1997, Woody et al 2007). Examples of other surface
Accepted for publication 7 May 2009.
Corresponding author. E-mail:


pullulans we discuss and review (i) the desirable properties of a model organism. The inoculated plates were sealed around the rims with parafilm.g. We recorded the effect of growth on 2% glucose supplemented with 20 mM nicotinamide (FIG. FIG. Even though microorganisms have been used for studies in plasticity (e. Bago et al 2004). pullulans (04313. Along with our observations on A. In this case colony morphology show characteristics of ‘‘phase transitions’’ where there are abrupt changes from one morphologic type to another along nutrient and agar density gradients. nutrient gradients and stress (Shapiro 1995. self-engineering. all of which can be beneficial and thus evolve. Although relatively minor there was a distinct change in response to light (FIG. 1E). The geometry of bacterial colonies can be a consequence of swarming. Stomp et al 2008). Growth at 9 C was recorded (FIG. in 2004. RESULTS We provided examples of the diversity of morphological (colony) responses. However medium supplemented with nicotinic acid is not expected to produce epigenetic changes. 1A) and might indicate an epigenetic effect. Promislow 2005. chemotactic auto-aggregation. (ii) with inocula from colonies growing on different sugar sources. (iii) responses to light and (iv) epigenetic influences on phenotypic plasticity. 1A). Massai Kopjes.5% dulcitol at 25 C (FIG. 2F. 2F. This photo response is immediately interrupted if the colony is shielded from light and allowed to grow in complete dark in the same incubator. Bacterial colonies growing on the surfaces in Petri dishes show differentiated structures that result from a complex series of morphological events. D) produces considerable sectoring (i. exemplify the degree of phenotypic plasticity that can occur in microorganisms grown in relatively simple culture conditions. Andrews 1992. such as Arabidopsis thaliana or Drosophila melanogaster. Nicotinamide (the amide of nicotinic acid) is known to inhibit histone deacetylases that are essential for epigenetic regulation of gene expression (Prusty et al 2008). 1C. We recorded the effect of increasing the concentration of glucose 0. G). In this case there are manifest changes in the growth pattern with discrete dynamic phases of growth as the colony expands. which indicated that little to no melanin accumulates at low temperature after 4 wk and somewhat more melanin is present after .5% glucose at 25 C (FIG. 1F). This property coupled with other natural attributes suggests that this microorganism could serve as a model for investigating a diversity of problems on the causes of phenotypic plasticity. Photographs were taken under standard conditions at various intervals over the period. Influences of temperature and time were recorded (FIG. The initial inoculum (. 0. especially in fungi ( Jennings 1993. movement and reproduction. often are employed as experimental organisms. Growth at 9 C (FIG. intercellular communication. Pattern formation in bacteria. The major strain in this study was subjected to PCR amplification and rDNA sequencing as described by Lachance et al (2005).5%) agar and was placed on the center of the agar medium in the Petri dish.104 yeast-phase cells suspended in 1 mL H2O) was taken from a culture growing on YNB glucose (0. 0.5–2% (FIG.e. Serengeti National Park. (ii) dimorphism in fungi. In essence growth tests for carbon assimilation were conducted on medium in 95 mm glass Petri dishes composed of 2% Bacto agar. Experiments in this latter category were conducted by supplementing with 20 mM nicotinamide or 20 mM nicotinic acid in buffered (100 mM phosphate) medium. G). These emergent phenotypes of single cells growing together and communicating affect survival. that is its environment.0% (w/v) carbon source.5% glucose. Colony morphology is relatively uniform after 4 wk on 0.e. 20 or 25 C. such as Bacillus subtilis (Mimura et al 2000). MATERIALS AND METHODS The source of inocula was a single strain of A. Colony morphology was a spreading black (melanin) branching structure after 4 wk on 0.5% or 2. A detailed description of these media is given by Yarrow (1998). (iii) using different nitrogen sources added to YCB (Bacto yeastcarbon base) and (iv) conditions that potentially demonstrate epigenetic influences on changing colony morphology.67% YNB (Bacto yeast-nitrogen base) and 0. Most of the growth media were single-carbon sources in agar.1) isolated from beetles in morning glory flowers. sectors with melanin) and distinct stages of growth if allowed to grow 12 wk.824 MYCOLOGIA detect plasticity genes or genetic networks involved in the transition from one phenotype to another. Additional growth tests were conducted under (i) constant light or dark and a light : dark (12 h : 12 h) photoperiod. and thus morphological shifts that occur on medium with nicotinamide but not on medium containing nicotinic acid can be a useful indicator of epigenetic control. To facilitate this type of work model plants and animals. We report here that the fungus Aureobasidium pullulans reversibly forms different types of colonies depending on the substrate and temperature on which it is grown. 1B) with daily growth rings apparent as the colony expanded for 3 wk. their great potential for understanding the mechanism of phenotypic plasticity have not been generally recognized. Shapiro (1998) emphasized the need to consider a bacterial population as a multicellular organism with complex signaling systems that result in coordinated behaviors. 2A). Ben-Jacob and Levine 2006). Colonies were grown 2–3 d up to 3–4 mo at 9. The colony under these conditions is more similar to the growth on the lower concentration (i.

pullulans produced similar results. pullulans . C) and 2% (Fig. A 5 4 wk at 25 C. Lower temperature resulted in more melanin and in some cases (glycerol and i-erythritol) dynamic developmental phases of growth.0% glucose at 25 C. Colonies of A. 2. These examples illustrate the diverse and complex changes that occur over time and as a consequence of alterations in simple carbon sources. 1. Experiments conducted with inocula from colonies grown on four different carbon sources (0. 12 h light : 12 h dark photoperiod (back and front illuminated). Colonies grown under continuous light or dark on the same medium appear similar to the colony in A. The colonies (FIGS. pullulans cultured on YNB + dulcitol. 2B.5% glucose. 2. bar: A 5 1 cm. Colonies grown at 25 C without supplements appear similar to the colony in A. GenBank: FJ744598) in these studies had strong similarity (greater than 98% similarity) to many sequences from different strains of A. E) dulcitol respectively. Colonies of A. 0. 2D. 0. 2A) on medium that was not supplemented. In this case an epigenetic effect is implicated because the amide is expected to induce changes in the chromatin while the acid is not and should appear like the colony (FIG. Colony morphology was noted (FIG.0% glucose. supplemented with 20 mM nicotinamide and 20 mM nicotinic acid respectively. Tests with other strains of A.SLEPECKY AND STARMER: PHENOTYPIC PLASTICITY IN FUNGI 825 FIG. dulcitol. 2. F and G 5 0. 3) were grown from a suspension of cells from a single strain of A.5% glucose.5% dulcitol. Partial rDNA sequence of the strain (04-313. pullulans cultured on YNB + glucose. E 5 2. as were those grown in media supplemented with 20 mM nicotinic acid (FIGS. supplemented with 20 mM nicotinamide and 20 mM nicotinic acid respectively. We also recorded growth on 0. but other carbon and nitrogen sources showed diverse phenotypes and changes over time. D and E 5 4 wk at 25 C. 0. bar: A 5 1 cm.5% (FIG. 2B. F 5 2. A 5 salicin. pullulans grown on YNB + 0. B and C 5 4 wk at 25 C. B 5 glycerol and C 5 i-erythritol) when incubated 4 wks at 25 C (column 1) and 4 wk at 9 C (column 2) or 12 wk at 9 C (column 3). C and D 5 0.5%. 3) on other carbon sources (0. A 5 4 wk at 25 C.5% glucose agar. 12 wk. 1. This was expected and indicated that intraspecific variation in phenotypic plasticity also exists.5% glucose at 9 C for 4 and 12 wk respectively. 2C. D). Each photo is 5 cm square. Colonies grown at 25 C without supplements appear similar to the colony in A. B 5 3 wk at 20 C. Each photo is 5 cm square.0% glucose at 25 C supplemented with 20 mM nicotinamide.5% glucose.1. mannitol and salicin) each transferred to all four original sources showed that morphological changes experienced on the original plates were reversible. Not all tests are shown. E). FIG.5% glucose at 9 C for 4 and 12 wk respectively. Colonies grown on media supplemented with 20 mM nicotinamide were recorded (FIGS. Note that this is true for either concentration of dulcitol. 0. glucose.5% w/v.

the capacity to retain genotypes for multiple testing in different environments). It is widely thought that fungi develop differentially to explore and exploit the environment and to respond quickly by changing mycelia when environmental conditions change. bar: C2 5 1 cm. grow and reproduce. such as Desirable properties of a model organism. For example the fact that DNA or its modification is the genetic determinant was revealed by colony changes in pneumococcus (Avery et al 1944). Studies with A.826 MYCOLOGIA adhesive nets and conidial traps. In addition complex signals. Their response to environmental signals can result in structures for catching nematodes. For example the nematode-trapping fungus Arthrobotrys oligosopora develops different structures from mycelia for infecting and parasitizing nematodes or other fungi. pullulans cultured on 0. FIG. and unitary organism with determinant structures (e. DISCUSSION Colony changes due to mutagenesis were important in early studies in microbial genetics. The strongest similarity (99%) was with group 3 and 4 strains defined respectively as A.—Four properties that make fungi attractive for studies of plasticity are (i) the ability to use clones for comprehensive genetic investigations (i. However phenotypic change (not due to treatment with mutagens) in colonies is not often observed. Hallsworth and Magan 1996. deposited in GenBank. namibiae by Zalar et al (2008). pH. Morrow and Fraser 2009). 4 wk at 9 C (column 2) and 12 wk at 9 C (column 3). virulence. Colony of A. regulation (Rayner and Coates 1987) and pathogenicity in plants and animals (Rippon 1980. pathogenesis and antigen-antibody interaction (i. while others refer to it as a yeast-like fungus. Peabody et al 2003. host immune mechanisms. (iii) the ability to use fungal species in evolutionary studies. such as bacteria and fungi. possibly because pure cultures have only a single characteristic colony morphology or variation in colony type is seen only among strains. However fungi are well known for their extreme phenotypic plasticity (Slutsky et al 1985.e. either by selection experiments (Scheiner 2002) or in comparative tests of adaptive roles and (iv) the fact that many fungi have indeterminate growth and thus provide the opportunity to study the function of genetic mosaics and the utility of dynamic boundaries (Peabody et al 2003). (ii) the phenotypic reversibility of the same culture over time and after sequential culturing. such as those that are involved in symbiotic associations. subglaciale and var.g. Madhani and Fink 1998. Each photo is 5 cm square. pullulans var. Andrews 1992. nutrients. pullulans. Romano 1966.5% (w/v) salicin (A). osmotic pressure. glycerol (B) or i-erythritol (C) 4 wk at 25 C (column 1). resistance) can be used as the target for reaction norm investigations (Lachke et al 2000.—Some mycologists consider A. signaling (Lengeler et al 2000. pullulans has been . 2005. A. Saikkonen et al 2004. Lee et al 2003). also are possible (Wickerham and Kurtzman 1975. disperse. Several reviews of dimorphism in fungi discuss general features (Scherr and Weaver 1953. Even though the phenotypic plasticity in fungi is common and well known among mycologists (Slutsky et al 1985. By far the most extensively studied phenotypic change in fungi is the yeastmycelial (YM) transition.e. Bago et al 2004) and have properties that make them suitable for laboratory studies of how and why phenotypes change when environmental conditions change. water potential. such as temperature. His review emphasized the potential insights that are possible from thinking about architectural modules employed by microorganisms to survive. Experimental investigations of basic environmental signals. Macoris et al 2006). Bo¨ lker 2001. pullulans to be a black yeast. Bemmann 1981). mobile animals). 3. Lee et al 2003. Nadal et al 2008. and for mycoparasitism by developing hyhal coils and appressoria (Nordbring-Hertz 2004). phase transitions and cell differentiation (Maresca and Kobayashi 1989). Andrews (1998) discusses the fundamental difference between modular organisms. light and their interactions. Andrews 1992) it is generally under appreciated. quorum sensing (Nickerson et al 2006). Bago et al 2004).

concentric growth stages and developmental patterns. 1994) and induce filamentous growth (in S. and its expression is influenced by temperature and pH (Wickerham and Kurtzman 1975). Kockova´-Kratochvı´lova´ et al (1980) illustrate the multiple growth forms of giant colonies that develop for A. In some cases the compounds (e. Metabolic processes involved in the YM transition are not well know but glutathione metabolism that leads to reduced thiol might play a role in the YM transition ( Ju¨rgensen et al 2001) and t-RNA methylation also might affect the differentiation process (Steiman et al 1990). extent of radial filamentous growth and degree of pigment accumulation. pullulans. pullulans from leaf surfaces and observed variation in colony morphology. pullulans are responsible (Taylor et al 2005). In Rippon’s (1980) comprehensive review of dimorphism in pathogenic fungi he concluded. order Dothideales. family Dothideaceae. Samson et al 2004) and has been implicated as a major cause of allergic disease in humans. It is also airborne (Shelton et al 2002. the YM growth transition) have reported the following interesting features. Kockova´-Kratochvı´lova´ et al 1980) involves the formation of blastoconidia that can give rise to promycelium that either can form (i) aerial hyphae that produce chlamydospores divided by septa (also called arthroconidia) that bud to form blastoconidia or (ii) hyphae with lateral outgrowths of blastococonidia that form chlamydospores with melanin in their cell walls (chlamydospores are freed from the hyphae and bud to form hyaline blastoconidia).’’ A review of 260 publications (Bemmann 1981) on the dimorphism of fungi summarizes these factors as influences of dimorphism: atmosphere.SLEPECKY AND STARMER: PHENOTYPIC PLASTICITY IN FUNGI redefined by Zalar et al (2008). subglaciale and var. In addition they observed concentric rings of pigmentation when colonies grew in light-dark cycles. Finlay 1987). A. carbon and energy sources as well as nitrogen and other supplements. Moreover increases in Zn2+ additions to continuous cultures caused a gradual shift through three growth regions (Reeslev et al 1993). Moragues et al 1988. inoculum. They define four varieties of the species (var. namibiae) and describe them. alcohols) might function by induction of changes in the plasma membrane (Sevilla et al 1983. melanogenum. Pasquier-Clouet and Zucca 1987). varied margins. Its life cycle (Pechak and Crang 1977. Janisiewicz and Korsten 2002) and has become the model organism for ecological studies of the phylloplane (Andrews et al 2002. pullulans. Pollock et al (1992) obtained several strains of A. including a great range in colony color. Dimorphism in other fungi. the change from yeast-like cells to chlamydospores is influenced by both glucose concentration and a limiting nitrogen source (Bermejo et al 1981) as well as interstrain variability (Gadd and Cooper 1984). who recognized the two morphological states of Blastomyces dermatitidis. Campbell et al 2004) and that mycelial versus yeast development is a function of population density (Park 1984. pullulans is multiphasic and can undergo a budding to hyphal-form change. the fact that hyphal and unicellular blastospores do not produce pullulan-like compounds (Simon et al 1993. General observations on the change to mycelial growth include a decrease in both protein and RNA content (Sevilla et al 1988). pullulans might explain its widespread occurrence in nature.e. especially polysaccharides such as pullulan (Catley 1979) and enzymes (Buzzini and Martini 2002). Aureobasidium pullulans has been used for the production of extracellular compounds. temperature. A diversity of other 827 investigations on the role of carbon and nitrogen compounds in artificial medium demonstrates pronounced affects on the YM transition (Kockova´Kratochvı´lova´ and Hronska´ 1981. pH. This change in the ploidy level is largely due to changes in actin structure (Kopecka´ et al 2003). They diagram and describe diverse colors. cerevisae Lorenz et al 2000). Studies on mechanisms for changes in growth form from yeast to mycelial (i. It has been found in most habitats and is prominent in the phyllosphere. McGrath and Andrews 2007. Related to the YM-transition. var. These varieties are members of class Ascomycota. var. all similar to what we find in our study. It should be noted that hyphae become multinucleate as a result of the uncoupling of nuclear division from cytokinesis.g. Nickerson et al (2006) reviewed the phenomenon of quorum sensing in . These studies led to experimental demonstration that incubation temperature was important in the transition between a ‘‘yeast-like’’ phase and a ‘‘mouldphase’’ (Hamburger 1907). were described by Gilchrist and Stokes (1898) and Ricketts (1901). The versatile appetite and tolerance to stress of A. sectored growth. ‘‘The single most important external factor affecting the growth phase of dimorphic pathogenic fungi is temperature. pullulans varies considerably among strains. Its importance to the biological control of plant diseases has received considerable attention (Buck et al 1998. Colony color in A. recent studies on conidia emitted from flowers suggest high-molecular weight allergens in A. especially different growth forms of pathogenic taxa. Woody et al 2007). and all are thought to be restricted to clonal reproduction.—Early studies on the influences of external factors on dimorphism in fungi.

This phenomenon is possibly due to quorum sensing (Hornby et al 2001) but is known only in a few fungi (Candida albicans and Ceratocystis ulmi). (i.e. The capacity to anticipate regular environmental change by using circadian rhythms is largely based on a conserved transcription-translation-based negative feedback loop that can be reset by light and temperature (Dunlap and Loros 2006). such as hyphal development. cerevisae as the phenotype to study the effects of environmental stressors on phenotypic plasticity. albicans and S. cerevisae) or grow by budding (U. CO2.—Responses to light (Marsh et al 1959. while those involved in DNA processing and transcription had low phenotypic plasticity). At least one antibiotic (Valinomycin) is known to suppress hyphal growth in C. a yeast that undergoes both budding-hyphal transitions and high-frequency-phenotypic switching (both of which are thought to contribute to successful pathogensis). The plasticity of each gene was compared as to their connectivity to transcription factors and to downstream genes. chelating agents and transition metals (Romano 1966). which we report here for A. This adaptive explanation for high-frequency phenotypic switching has been proposed as the mechanism used by other opportunistic pathogens (C. They found that a ccg-8 in Neurospora is a homolog of opi1p (a gene involved in transcriptional regulation of inositol in S. There is no doubt that signaling pathways and genetic networks play a fundamental role in sensing environmental cues that induce the morphogenesis that characterizes phenotypic plasticity in fungi (Madhani and Fink 1998. Inoculation size also influences the growth phase and is thought to be a general determinant of colony morphology (Hornby et al 2004. Saccharomyces cerevisae and Ustilago maydis) respond to nutrient limitation by using the same signaling transduction pathways but produce either pseudo-hyphal growth (C. pullulans. infectious structure and sclerotia formation. He also studied the association of the gene with biological processes to see whether the degree of plasticity was related to their function. In a study by Sa´nchez-Martı´nez and Pe´rez-Martı´n (2001) three fungi (Candida albicans. cerevisae). Nadal et al 2008. as well as to antibiotic treatment (Lachke et al 2000). albicans) that respond quickly to changes in their host (Soll 2002). Lengeler et al 2000). These include nutrient limits. HLP. In this case the kinase triggers a two-component signaling pathway. but the observation that growth ring formation cease after returning cultures to the dark suggests that . In general morphogenesis and virulence is regulated by the conserved cAMP (cyclic adenosine monophosphate) and mitogen-activated protein (MAP) kinase signaling pathway in a variety of fungi and is know to be involve in sensing nutrient levels in S. Xu 2000). sporulation and spore germination) and other morphological transitions. Their survey included 17 fungal genomes and discovered that 11 well described clock controlled genes (ccg) of Neurospora to be conserved in the other fungi. Bourret et al 1969) and circadian rhythms appear to be widespread in fungal groups. pullulans found by Pollock et al (1992).828 MYCOLOGIA dimorphic fungi and listed similar environmental signals that induce the YM transition. is reversibly switched by regulation of MT-II metallothionein genes and a hemolysin-like protein. Lee et al (2003) review the extensive literature and associated reviews that focus on phytopathogens. Breitkreutz et al 2003. albicans (Watanabe et al 2005). Circadian clock genes known in Neurospora crassa have homologs in several other fungi (Lombardi and Brody 2005). Wenger and Lilly 1966. Morrow and Fraser 2009). In fact fungi can use similar signaling pathways in response to environmental signals that ultimately result in same or even different outcomes. The light response in A. Nickerson et al 2006). Responses to light. Candida glabrata. They implicate cAMP signaling in reproductive functions (mating. It is clear that the cAMP and MAP signaling is important to phenotypic plasticity in fungi and that two-component signaling is a common means for fungi to sense and react to environmental signals (Klein and Tebbets 2007). Virulence in human pathogenic fungi is induced by temperature and accompanied by the phase transition from the mycelial to the yeast growth form. Nemecek et al (2006) demonstrate that a hybrid histidine kinase senses the host signal and induces the phase transition that results in virulent gene expression. cerevisae (Lee et al 2003. It is hypothesized that switching is a means to achieve phenotypic plasticity that lets populations respond rapidly to the changing physiology and immune responses of the host. is not known to be under the influence of clock-controlled genes. pH. The linkage of the YM transition with sexual reproduction and virulence apparently has an ancient origin and is widespread in fungi (Madhani and Fink 1998. (ii) phenotypic plasticity is associated with a gene’s biological function. maydis). and (iii) phenotypic plasticity is correlated with the number of transcription factors associated with a gene. protein production and defense had high phenotypic plasticity. He found the following: (i) The number of transcription factors that regulate phenotypic plasticity was influenced by the substructure of the network in which it was associated. those genes involved in energy utilization. Promislow (2005) used the expression level of mRNA genes in S. nitrogen source.

We want to emphasize that the overall colony morphology and the dynamics involved are also of importance and are diverse. Dormancy. 2. germination. 2nd ed. 2005. 1944. Nicotinamide is a potent inhibitor of sirtuins (Sir2) and changes in nicotinamide concentration in the cell nucleus causes concomitant changes in Sir2-mediated gene silencing. 3) that occur in concentric zones demonstrate synchronism in phenotypic changes as the environment changes. In this case we do not know the molecular causes. Lysak LV. ———. However Park (1982) showed the Y/M forms are influenced by the types of nitrogen in the medium and that M forms can develop within a Y colony. 1.g. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transforma- . eds. Population biology of Aureobasidium pullulans on apple leaf surfaces. Epigenetic effects. Guerrero et al 2006). New York: Dekker. pullulans reported here it is possible that nicotinamide is suppressing histone deacetylases that modify chromatin structures. Time-dependent changes (FIG. We thank Andre´ Lachance for providing the partial rDNA sequence. Zagustina NA. Ultimately the adaptive features of the colony form (e. Spear RN. (ii) alteration of anabolic and catabolic processes. These changes are probably a result of nutrient depletion as well as exudates of the colony as it spreads across the agar surface. Silencing is a consequence of deacetylation of histones that lead to transcriptional down regulation (Sauve et al 2006). In: Wicklow DT. Yarrowia liplolytica and Ustilago maydis. we are enthusiastic about the potential use of this organism to investigate a diversity of problems on the proximate and ultimate cause of phenotypic plasticity. sporulation and dispersal. Aleksandrova AA. however the sectoring observed (e. So¨derstro¨m BE. A. pullulans (FIGS. serves as a model organism in the study of the phyllosphere and is important to both industry and medicine. In addition Reyna-Lo´pez and Ruiz-Herrera (2004) showed that changes in DNA methylation patterns occur during the dimorphic transitions of Mucor rouxii.—Many of the above studies were concerned with changes in cell morphology. eds. 1998. In the experiments with A. cerevisae Halme et al (2004) demonstrated that epigenetic silencing of the gene FLO11 regulates a key developmental switch that controls growth of either peudohyhae (FLO11 on) or yeast cell forms (FLO11 silent). LITERATURE CITED Alekhova TA. Appl Biochem Microbiol 41:382–389. Bacteria as modular organisms. pullulans is ubiquitous. this switch can be suppressed by addition of nicotinamide but not nicotinic acid. The fungal community.—The results reported here on the potential epigenetic influences and the capacity to dissect and understand the genetic pathways involved in the YM transition suggest a promising direction for future research into the genetics and mechanisms involved in switching cell types and achieving morphological diversity from a single genotype. FIG. and the connection to colony morphology is not always established. pullulans grows in the mycelial phase when dulcitol (galactitol) is the sole carbon source (FIG. In: Carroll GC. Avery DT. 1 glucose) could be similar. 2002. Conclusions. 1997. Annu Rev Microbiol 52:105–126. 3) illustrate the spectrum of the reaction norm. but the cascade of events induced by different environmental signals could lead to (i) different epigenetic influences.SLEPECKY AND STARMER: PHENOTYPIC PLASTICITY IN FUNGI the response might not be controlled by a clock-like mechanism. In general the phenotypes observed involve the entire population of cells and thus differ from phenotypic switching that spontaneously occurs in a small proportion of the population 829 in Candida albicans and Cryptococcus neoformans (Slutsky et al 1985. Can J Microbiol 48:500–513. McCarty MJ. In fact in S. ———. and thus the YM transition is likely to be an epigenetic phenomenon. This phenomenon provides a unique opportunity to study time-dependent changes in gene expression that lead to changes in the phenotype. Given that A. ———. Nordheim EV. Fungal life history strategies. growth. Harris RF. Monitoring of microbial degraders in manned space stations. ACKNOWLEDGMENTS We appreciate the technical assistance of Virginia Aberdeen. dispersal. Bezborodov AM.g. 1992. This could imply a change in the regulation of gene expression (Prusty et al 2008). This time-dependent characteristic could be of interest. The research was partially supported by the National Science Foundation. 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