Faculty & Staff

  • Image of Anne Pringle

    Anne Pringle

    L&S Mary Herman Rubinstein Professor of Botany and Bacteriology

    3207 Microbial Sciences Building
    Office: (608) 890-4364
    Lab: (608) 265-9996

Start and Promotion Dates

  • Associate Professor: 2015


Duke University Department of Botany and University Program in Genetics PhD 2001
University of Chicago  A.B. Honors Biology, with General Honors 1993

Areas of Study

ecology, evolution, fungi, invasion biology, conservation biology, dispersal, senescence

Research Overview

The Pringle laboratory focuses on the biology of species whose life histories and body plans seem very different from our own. Fungi encompass a hetereogeneous array of both microbes and macrobes, and the Pringle laboratory uses fungi as tools to test and elucidate general principles of ecology and evolution.

Research Papers

  • Heil JA, Wolock CJ, Pierce NE, Pringle A, Bittleston LS (2022) Sarracenia pitcher plant-associated microbial communities differ primarily by host species across a longitudinal gradient. Environmental microbiology : · Pubmed · DOI

    No abstract available.

  • Gentry SL, Lorch JM, Lankton JS, Pringle A (2021) Koch's postulates: Confirming Nannizziopsis guarroi as the cause of yellow fungal disease in Pogona vitticeps . Mycologia 113((6)):1253-1263 · Pubmed · DOI

    No abstract available.

  • Romero-Olivares AL, Morrison EW, Pringle A, Frey SD (2021) Correction to: Linking Genes to Traits in Fungi. Microbial ecology 82((1)):156 PMC8329815 · Pubmed · DOI

    No abstract available.

  • Iapichino M, Wang YW, Gentry S, Pringle A, Seminara A (2021) A precise relationship among Buller's drop, ballistospore, and gill morphologies enables maximum packing of spores within gilled mushrooms. Mycologia 113((2)):300-311 · Pubmed · DOI

    No abstract available.

  • Romero-Olivares AL, Morrison EW, Pringle A, Frey SD (2021) Linking Genes to Traits in Fungi. Microbial ecology 82((1)):145-155 PMC8282587 · Pubmed · DOI

    No abstract available.

  • Wang YW, Hess J, Slot JC, Pringle A (2020) De Novo Gene Birth, Horizontal Gene Transfer, and Gene Duplication as Sources of New Gene Families Associated with the Origin of Symbiosis in Amanita. Genome biology and evolution 12((11)):2168-2182 PMC7674699 · Pubmed · DOI

    No abstract available.

  • Lagomarsino Oneto D, Golan J, Mazzino A, Pringle A, Seminara A (2020) Timing of fungal spore release dictates survival during atmospheric transport. Proceedings of the National Academy of Sciences of the United States of America 117((10)):5134-5143 PMC7071907 · Pubmed · DOI

    No abstract available.

  • Adams CA, Zimmerman K, Fenstermacher K, Thompson MG, Skyrud W, Behie S, Pringle A (2019) Fungal Seed Pathogens of Wild Chili Peppers Possess Multiple Mechanisms To Tolerate Capsaicinoids. Applied and environmental microbiology 86((3)): PMC6974639 · Pubmed · DOI

    No abstract available.

  • Vargas N, Gonçalves SC, Franco-Molano AE, Restrepo S, Pringle A (2019) In Colombia the Eurasian fungus Amanita muscaria is expanding its range into native, tropical Quercus humboldtii forests. Mycologia 111((5)):758-771 · Pubmed · DOI

    No abstract available.

  • Lopez-Nieves S, Pringle A, Maeda HA (2019) Biochemical characterization of TyrA dehydrogenases from Saccharomyces cerevisiae (Ascomycota) and Pleurotus ostreatus (Basidiomycota). Archives of biochemistry and biophysics 665:12-19 · Pubmed · DOI

    No abstract available.

  • Boynton PJ, Peterson CN, Pringle A (2019) Superior Dispersal Ability Can Lead to Persistent Ecological Dominance throughout Succession. Applied and environmental microbiology 85((6)): PMC6414377 · Pubmed · DOI

    No abstract available.

  • Hoeksema JD, Bever JD, Chakraborty S, Chaudhary VB, Gardes M, Gehring CA, Hart MM, Housworth EA, Kaonongbua W, Klironomos JN, Lajeunesse MJ, Meadow J, Milligan BG, Piculell BJ, Pringle A, Rúa MA, Umbanhowar J, Viechtbauer W, Wang YW, Wilson GWT, Zee PC (2018) Erratum: Author Correction: Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Communications biology 1:142 PMC6127152 · Pubmed · DOI

    No abstract available.

  • Hoeksema JD, Bever JD, Chakraborty S, Chaudhary VB, Gardes M, Gehring CA, Hart MM, Housworth EA, Kaonongbua W, Klironomos JN, Lajeunesse MJ, Meadow J, Milligan BG, Piculell BJ, Pringle A, Rúa MA, Umbanhowar J, Viechtbauer W, Wang YW, Wilson GWT, Zee PC (2018) Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Communications biology 1:116 PMC6123707 · Pubmed · DOI

    No abstract available.

  • Hess J, Skrede I, Chaib De Mares M, Hainaut M, Henrissat B, Pringle A (2018) Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita. Molecular biology and evolution 35((11)):2786-2804 PMC6231487 · Pubmed · DOI

    No abstract available.

  • Bittleston LS, Wolock CJ, Yahya BE, Chan XY, Chan KG, Pierce NE, Pringle A (2018) Convergence between the microcosms of Southeast Asian and North American pitcher plants. eLife 7: PMC6130972 · Pubmed · DOI

    No abstract available.

  • Seminara A, Fritz J, Brenner MP, Pringle A (2018) A universal growth limit for circular lichens. Journal of the Royal Society, Interface 15((143)): PMC6030627 · Pubmed · DOI

    No abstract available.

  • Levitis DA, Zimmerman K, Pringle A (2017) Is meiosis a fundamental cause of inviability among sexual and asexual plants and animals? Proceedings. Biological sciences 284((1860)): PMC5563809 · Pubmed · DOI

    No abstract available.

  • Liu F, Chavez RL, Patek SN, Pringle A, Feng JJ, Chen CH (2017) Asymmetric drop coalescence launches fungal ballistospores with directionality. Journal of the Royal Society, Interface 14((132)): PMC5550963 · Pubmed · DOI

    No abstract available.

  • Golan JJ, Pringle A (2017) Long-Distance Dispersal of Fungi. Microbiology spectrum 5((4)): · Pubmed · DOI

    No abstract available.

  • Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant-fungal invasions. The New phytologist 215((4)):1314-1332 · Pubmed · DOI

    No abstract available.

  • Alim K, Andrew N, Pringle A, Brenner MP (2017) Mechanism of signal propagation in Physarum polycephalum . Proceedings of the National Academy of Sciences of the United States of America 114((20)):5136-5141 PMC5441820 · Pubmed · DOI

    No abstract available.

  • Baker CC, Martins DJ, Pelaez JN, Billen JP, Pringle A, Frederickson ME, Pierce NE (2017) Distinctive fungal communities in an obligate African ant-plant mutualism. Proceedings. Biological sciences 284((1850)): PMC5360918 · Pubmed · DOI

    No abstract available.

  • van Diepen LT, Frey SD, Landis EA, Morrison EW, Pringle A (2017) Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter. Ecology 98((1)):5-11 · Pubmed · DOI

    No abstract available.

  • Marbach S, Alim K, Andrew N, Pringle A, Brenner MP (2016) Pruning to Increase Taylor Dispersion in Physarum polycephalum Networks. Phys. Rev. Lett. 117(17):178103 · Pubmed

    How do the topology and geometry of a tubular network affect the spread of particles within fluid flows? We investigate patterns of effective dispersion in the hierarchical, biological transport network formed by Physarum polycephalum. We demonstrate that a change in topology-pruning in the foraging state-causes a large increase in effective dispersion throughout the network. By comparison, changes in the hierarchy of tube radii result in smaller and more localized differences. Pruned networks capitalize on Taylor dispersion to increase the dispersion capability.

  • Zimmerman KC, Levitis DA, Pringle A (2016) Beyond animals and plants: dynamic maternal effects in the fungus Neurospora crassa. J. Evol. Biol. 29(7):1379-93 · Pubmed

    Maternal effects are widely documented in animals and plants, but not in fungi or other eukaryotes. A principal cause of maternal effects is asymmetrical parental investment in a zygote, creating greater maternal vs. paternal influence on offspring phenotypes. Asymmetrical investments are not limited to animals and plants, but are also prevalent in fungi and groups including apicomplexans, dinoflagellates and red algae. Evidence suggesting maternal effects among fungi is sparse and anecdotal. In an experiment designed to test for maternal effects across sexual reproduction in the model fungus Neurospora crassa, we measured offspring phenotypes from crosses of all possible pairs of 22 individuals. Crosses encompassed reciprocals of 11 mating-type 'A' and 11 mating-type 'a' wild strains. After controlling for the genetic and geographic distances between strains in any individual cross, we found strong evidence for maternal control of perithecia (sporocarp) production, as well as maternal effects on spore numbers and spore germination. However, both parents exert equal influence on the percentage of spores that are pigmented and size of pigmented spores. We propose a model linking the stage-specific presence or absence of maternal effects to cellular developmental processes: effects appear to be mediated primarily through the maternal cytoplasm, and, after spore cell walls form, maternal influence on spore development is limited. Maternal effects in fungi, thus far largely ignored, are likely to shape species' evolution and ecologies. Moreover, the association of anisogamy and maternal effects in a fungus suggests maternal effects may also influence the biology of other anisogamous eukaryotes.

  • Bittleston LS, Pierce NE, Ellison AM, Pringle A (2016) Convergence in Multispecies Interactions. Trends Ecol. Evol. (Amst.) 31(4):269-80 · Pubmed

    The concepts of convergent evolution and community convergence highlight how selective pressures can shape unrelated organisms or communities in similar ways. We propose a related concept, convergent interactions, to describe the independent evolution of multispecies interactions with similar physiological or ecological functions. A focus on convergent interactions clarifies how natural selection repeatedly favors particular kinds of associations among species. Characterizing convergent interactions in a comparative context is likely to facilitate prediction of the ecological roles of organisms (including microbes) in multispecies interactions and selective pressures acting in poorly understood or newly discovered multispecies systems. We illustrate the concept of convergent interactions with examples: vertebrates and their gut bacteria; ectomycorrhizae; insect-fungal-bacterial interactions; pitcher-plant food webs; and ants and ant-plants.

  • Zimmerman K, Levitis D, Addicott E, Pringle A (2015) Selection of pairings reaching evenly across the data (SPREAD): A simple algorithm to design maximally informative fully crossed mating experiments. Heredity (Edinb) 116(2):182-9 (PMC4806887) · Pubmed

    We present a novel algorithm for the design of crossing experiments. The algorithm identifies a set of individuals (a 'crossing-set') from a larger pool of potential crossing-sets by maximizing the diversity of traits of interest, for example, maximizing the range of genetic and geographic distances between individuals included in the crossing-set. To calculate diversity, we use the mean nearest neighbor distance of crosses plotted in trait space. We implement our algorithm on a real dataset of Neurospora crassa strains, using the genetic and geographic distances between potential crosses as a two-dimensional trait space. In simulated mating experiments, crossing-sets selected by our algorithm provide better estimates of underlying parameter values than randomly chosen crossing-sets.

  • Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Doré J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Högberg N, Johansson T, Khouja HR, LaButti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R, Martino E, Murat C, Ngan CY, Nehls U, Plett JM, Pringle A, Ohm RA, Perotto S, Peter M, Riley R, Rineau F, Ruytinx J, Salamov A, Shah F, Sun H, Tarkka M, Tritt A, Veneault-Fourrey C, Zuccaro A, Tunlid A, Grigoriev IV, Hibbett DS, Martin F, Buée M, Din Y, Gardes M, Grelet G, Gryta H, Jargeat P, Sitrit Y, Zimmermann S (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47(4):410-5 · Pubmed

    To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall-degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.

  • Chaib De Mares M, Hess J, Floudas D, Lipzen A, Choi C, Kennedy M, Grigoriev IV, Pringle A (2015) Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita. New Phytol. 205(4):1552-64 · Pubmed

    The genus Amanita encompasses both symbiotic, ectomycorrhizal fungi and asymbiotic litter decomposers; all species are derived from asymbiotic ancestors. Symbiotic species are no longer able to degrade plant cell walls. The carbohydrate esterases family 1 (CE1s) is a diverse group of enzymes involved in carbon metabolism, including decomposition and carbon storage. CE1 genes of the ectomycorrhizal A. muscaria appear diverged from all other fungal homologues, and more similar to CE1s of bacteria, suggesting a horizontal gene transfer (HGT) event. In order to test whether AmanitaCE1s were acquired horizontally, we built a phylogeny of CE1s collected from across the tree of life, and describe the evolution of CE1 genes among Amanita and relevant lineages of bacteria. CE1s of symbiotic Amanita were very different from CE1s of asymbiotic Amanita, and are more similar to bacterial CE1s. The protein structure of one CE1 gene of A. muscaria matched a depolymerase that degrades the carbon storage molecule poly((R)-3-hydroxybutyrate) (PHB). Asymbiotic Amanita do not carry sequence or structural homologues of these genes. The CE1s acquired through HGT may enable novel metabolisms, or play roles in signaling or defense. This is the first evidence for the horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal fungi.

  • Hess J, Skrede I, Wolfe BE, LaButti K, Ohm RA, Grigoriev IV, Pringle A (2014) Transposable element dynamics among asymbiotic and ectomycorrhizal Amanita fungi. Genome Biol Evol 6(7):1564-78 (PMC4122921) · Pubmed

    Transposable elements (TEs) are ubiquitous inhabitants of eukaryotic genomes and their proliferation and dispersal shape genome architectures and diversity. Nevertheless, TE dynamics are often explored for one species at a time and are rarely considered in ecological contexts. Recent work with plant pathogens suggests a link between symbiosis and TE abundance. The genomes of pathogenic fungi appear to house an increased abundance of TEs, and TEs are frequently associated with the genes involved in symbiosis. To investigate whether this pattern is general, and relevant to mutualistic plant-fungal symbioses, we sequenced the genomes of related asymbiotic (AS) and ectomycorrhizal (ECM) Amanita fungi. Using methods developed to interrogate both assembled and unassembled sequences, we characterized and quantified TEs across three AS and three ECM species, including the AS outgroup Volvariella volvacea. The ECM genomes are characterized by abundant numbers of TEs, an especially prominent feature of unassembled sequencing libraries. Increased TE activity in ECM species is also supported by phylogenetic analysis of the three most abundant TE superfamilies; phylogenies revealed many radiations within contemporary ECM species. However, the AS species Amanita thiersii also houses extensive amplifications of elements, highlighting the influence of additional evolutionary parameters on TE abundance. Our analyses provide further evidence for a link between symbiotic associations among plants and fungi, and increased TE activity, while highlighting the importance individual species' natural histories may have in shaping genome architecture.

  • Alim K, Andrew N, Pringle A (2013) Physarum. Curr. Biol. 23(24):R1082-3 · Pubmed

    No abstract available.

  • Alim K, Amselem G, Peaudecerf F, Brenner MP, Pringle A (2013) Random network peristalsis in Physarum polycephalum organizes fluid flows across an individual. Proc. Natl. Acad. Sci. U.S.A. 110(33):13306-11 (PMC3746869) · Pubmed

    Individuals can function as integrated organisms only when information and resources are shared across a body. Signals and substrates are commonly moved using fluids, often channeled through a network of tubes. Peristalsis is one mechanism for fluid transport and is caused by a wave of cross-sectional contractions along a tube. We extend the concept of peristalsis from the canonical case of one tube to a random network. Transport is maximized within the network when the wavelength of the peristaltic wave is of the order of the size of the network. The slime mold Physarum polycephalum grows as a random network of tubes, and our experiments confirm peristalsis is used by the slime mold to drive internal cytoplasmic flows. Comparisons of theoretically generated contraction patterns with the patterns exhibited by individuals of P. polycephalum demonstrate that individuals maximize internal flows by adapting patterns of contraction to size, thus optimizing transport throughout an organism. This control of fluid flow may be the key to coordinating growth and behavior, including the dynamic changes in network architecture seen over time in an individual.

  • Fritz JA, Seminara A, Roper M, Pringle A, Brenner MP (2013) A natural O-ring optimizes the dispersal of fungal spores. J R Soc Interface 10(85):20130187 (PMC3971719) · Pubmed

    The forcibly ejected spores of ascomycete fungi must penetrate several millimetres of nearly still air surrounding sporocarps to reach dispersive airflows, and escape is facilitated when a spore is launched with large velocity. To launch, the spores of thousands of species are ejected through an apical ring, a small elastic pore. The startling diversity of apical ring and spore shapes and dimensions make them favoured characters for both species descriptions and the subsequent inference of relationships among species. However, the physical constraints shaping this diversity and the adaptive benefits of specific morphologies are not understood. Here, we develop an elastohydrodynamic theory of the spore's ejection through the apical ring and demonstrate that to avoid enormous energy losses during spore ejection, the four principal morphological dimensions of spore and apical ring must cluster within a nonlinear one-dimensional subspace. We test this prediction using morphological data for 45 fungal species from two different classes and 18 families. Our sampling encompasses multiple loss and gain events and potentially independent origins of this spore ejection mechanism. Although the individual dimensions of the spore and apical ring are only weakly correlated with each other, they collapse into the predicted subspace with high accuracy. The launch velocity appears to be within 2 per cent of the optimum for over 90 per cent of all forcibly ejected species. Although the morphological diversity of apical rings and spores appears startlingly diverse, a simple principle can be used to organize it.

  • Pringle A (2013) Asthma and the diversity of fungal spores in air. PLoS Pathog. 9(6):e1003371 (PMC3675135) · Pubmed

    No abstract available.

  • Marmeisse R, Nehls U, Opik M, Selosse MA, Pringle A (2013) Bridging mycorrhizal genomics, metagenomics and forest ecology. New Phytol. 198(2):343-6 · Pubmed

    No abstract available.

  • Wolfe BE, Tulloss RE, Pringle A (2012) The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS ONE 7(7):e39597 (PMC3399872) · Pubmed

    Microbial symbioses have evolved repeatedly across the tree of life, but the genetic changes underlying transitions to symbiosis are largely unknown, especially for eukaryotic microbial symbionts. We used the genus Amanita, an iconic group of mushroom-forming fungi engaged in ectomycorrhizal symbioses with plants, to identify both the origins and potential genetic changes maintaining the stability of this mutualism. A multi-gene phylogeny reveals one origin of the symbiosis within Amanita, with a single transition from saprotrophic decomposition of dead organic matter to biotrophic dependence on host plants for carbon. Associated with this transition are the losses of two cellulase genes, each of which plays a critical role in extracellular decomposition of organic matter. However a third gene, which acts at later stages in cellulose decomposition, is retained by many, but not all, ectomycorrhizal species. Experiments confirm that symbiotic Amanita species have lost the ability to grow on complex organic matter and have therefore lost the capacity to live in forest soils without carbon supplied by a host plant. Irreversible losses of decomposition pathways are likely to play key roles in the evolutionary stability of these ubiquitous mutualisms.

  • Richard F, Glass NL, Pringle A (2012) Cooperation among germinating spores facilitates the growth of the fungus, Neurospora crassa. Biol. Lett. 8(3):419-22 (PMC3367758) · Pubmed

    Fusions between individuals are a common feature of organisms with modular, indeterminate life forms, including plants, marine invertebrates and fungi. The consequences of fusion for an individual fungus are poorly understood. We used wild-type and fusion mutant strains of the genetic model Neurospora crassa to chronicle the fitness in two different laboratory habitats, and in each experiment started colonies from multiple different densities of asexual spores. On round Petri dishes, fusion enabled wild-type colonies to grow larger than mutant (soft) colonies; but in linear 'race tubes', the soft mutant always grew more quickly than the wild-type. Starting a colony with more spores always provided an advantage to a wild-type colony, but was more often neutral or a cost to the soft mutant. The ability to fuse does not provide a consistent advantage to wild-type colonies; net benefits are shaped by both habitat and initial spore densities.

  • Wolfe BE, Pringle A (2012) Geographically structured host specificity is caused by the range expansions and host shifts of a symbiotic fungus. ISME J 6(4):745-55 (PMC3309363) · Pubmed

    The inability to associate with local species may constrain the spread of mutualists arriving to new habitats, but the fates of introduced, microbial mutualists are largely unknown. The deadly poisonous ectomycorrhizal fungus Amanita phalloides (the death cap) is native to Europe and introduced to the East and West Coasts of North America. By cataloging host associations across the two continents, we record dramatic changes in specificity among the three ranges. On the East Coast, where the fungus is restricted in its distribution, it associates almost exclusively with pines, which are rarely hosts of A. phalloides in its native range. In California, where the fungus is widespread and locally abundant, it associates almost exclusively with oaks, mirroring the host associations observed in Europe. The most common host of the death cap in California is the endemic coast live oak (Quercus agrifolia), and the current distribution of A. phalloides appears constrained within the distribution of Q. agrifolia. In California, host shifts to native plants are also associated with a near doubling in the resources allocated to sexual reproduction and a prolonged fruiting period; mushrooms are twice as large as they are elsewhere and mushrooms are found throughout the year. Host and niche shifts are likely to shape the continuing range expansion of A. phalloides and other ectomycorrhizal fungi introduced across the world.

  • Wolfe BE, Kuo M, Pringle A (2012) Amanita thiersii is a saprotrophic fungus expanding its range in the United States. Mycologia 104(1):22-33 · Pubmed

    Although most species in the genus Amanita form ectomycorrhizal associations, a few are reported to be saprotrophs living in grassland habitats. Little is known about the ecology and distribution of these free-living Amanita species. We describe the ecology of Amanita thiersii, a species commonly collected in lawns throughout the Mississippi River Basin. Stable isotopes of carbon, transcriptomic sequences and patterns of growth on complex carbon sources provide evidence for A. thiersii as a saprotrophic species. Sporocarps of A. thiersii are less depleted in (13)C compared to published data for ectomycorrhizal fungi, supporting a saprotrophic mode of carbon acquisition in the field. Orthologs of cellulase genes known to play key roles in the decomposition of cellulose in other basidiomycetes were identified in a transcriptome of A. thiersii, establishing that this species has the genetic potential to degrade cellulose. Amanita thiersii also can use artificial cellulose or sterile grass litter as a sole carbon source. DNA sequences of three nuclear gene regions and banding patterns from four inter-simple sequence repeat markers were identical across 31 populations from throughout the known range of the species, which suggests the genetic diversity of A. thiersii populations is low. Maps of A. thiersii collections made from the 1950s until present suggest this species is experiencing a range expansion. It was reported first in 1952 in Texas and now occurs in nine states north to Illinois. These data provide an ecological context for interpreting the genome of A. thiersii, currently being sequenced at the United States Department of Energy's Joint Genome Institute.

  • Mushegian AA, Peterson CN, Baker CC, Pringle A (2011) Bacterial diversity across individual lichens. Appl. Environ. Microbiol. 77(12):4249-52 (PMC3131627) · Pubmed

    Symbioses are unique habitats for bacteria. We surveyed the spatial diversity of bacterial communities across multiple individuals of closely related lichens using terminal restriction fragment length polymorphism (T-RFLP) and pyrosequencing. Centers of lichens house richer, more consistent assemblages than species-poor and compositionally disparate lichen edges, suggesting that ecological succession plays a role in structuring these communities.

  • Roper M, Seminara A, Bandi MM, Cobb A, Dillard HR, Pringle A (2010) Dispersal of fungal spores on a cooperatively generated wind. Proc. Natl. Acad. Sci. U.S.A. 107(41):17474-9 (PMC2955148) · Pubmed

    Because of their microscopic size, the forcibly ejected spores of ascomycete fungi are quickly brought to rest by drag. Nonetheless some apothecial species, including the pathogen Sclerotinia sclerotiorum, disperse with astonishing rapidity between ephemeral habitats. Here we show that by synchronizing the ejection of thousands of spores, these fungi create a flow of air that carries spores through the nearly still air surrounding the apothecium, around intervening obstacles, and to atmospheric currents and new infection sites. High-speed imaging shows that synchronization is self-organized and likely triggered by mechanical stresses. Although many spores are sacrificed to produce the favorable airflow, creating the potential for conflict among spores, the geometry of the spore jet physically targets benefits of the airflow to spores that cooperate maximally in its production. The ability to manipulate a local fluid environment to enhance spore dispersal is a previously overlooked feature of the biology of fungal pathogens, and almost certainly shapes the virulence of species including S. sclerotiorum. Synchronous spore ejection may also provide a model for the evolution of stable, self-organized behaviors.

  • Wolfe BE, Richard F, Cross HB, Pringle A (2010) Distribution and abundance of the introduced ectomycorrhizal fungus Amanita phalloides in North America. New Phytol. 185(3):803-16 · Pubmed

    Despite a growing awareness of the global reach of ectomycorrhizal (EM) fungal introductions, little is known about the fate of introduced EM fungi in novel ranges. Using herbarium specimens, species distribution models, and field collections of sporocarps, root tips and extramatrical mycelia, we assessed the distribution and abundance of the European species Amanita phalloides in North America. There are two distinct ranges of the fungus, one along the West Coast (California to British Columbia) and the second on the East Coast (Maryland to Maine). As predicted by a species distribution model, the West Coast range is larger. Amanita phalloides is more frequently found in native forests on the West Coast than on the East Coast. At Point Reyes Peninsula in California, A. phalloides dominates community sporocarp biomass, and is frequent as root tips. In individual soil cores at Point Reyes, root tips of A. phalloides make up 50% of total root tip biomass. Hyphae of A. phalloides are frequent, but make up only 2% of total hyphal biomass. The contrasting patterns of the distribution and abundance of A. phalloides on the East and West Coasts of North America may influence both its future spread and its impacts.

  • Pringle A (2009) Mycorrhizal networks. Curr. Biol. 19(18):R838-9 · Pubmed

    No abstract available.

  • Pringle A, Adams RI, Cross HB, Bruns TD (2009) The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol. Ecol. 18(5):817-33 · Pubmed

    The deadly poisonous Amanita phalloides is common along the west coast of North America. Death cap mushrooms are especially abundant in habitats around the San Francisco Bay, California, but the species grows as far south as Los Angeles County and north to Vancouver Island, Canada. At different times, various authors have considered the species as either native or introduced, and the question of whether A. phalloides is an invasive species remains unanswered. We developed four novel loci and used these in combination with the EF1α and IGS loci to explore the phylogeography of the species. The data provide strong evidence for a European origin of North American populations. Genetic diversity is generally greater in European vs. North American populations, suggestive of a genetic bottleneck; polymorphic sites of at least two loci are only polymorphic within Europe although the number of individuals sampled from Europe was half the number sampled from North America. Endemic alleles are not a feature of North American populations, although alleles unique to different parts of Europe were common and were discovered in Scandinavian, mainland French, and Corsican individuals. Many of these endemic European haplotypes were found together at single sites in California. Early collections of A. phalloides dated prior to 1963 and annotated using sequences of the ITS locus proved to be different species of Amanita. The first Californian collections that we confirmed as A. phalloides were made from the Del Monte Hotel (now the Naval Postgraduate School) in Monterey, and on the campus of the University of California, Berkeley, in 1938 and in 1945. These historical data are used in combination with data on A. phalloides' current distribution to estimate a rate of spread for A. phalloides in California. Many species of ectomycorrhizal (EM) fungi have been introduced across and among continents, but with this evidence, the death cap becomes the only known invasive EM fungus in North America.

  • Vellinga EC, Wolfe BE, Pringle A (2009) Global patterns of ectomycorrhizal introductions. New Phytol. 181(4):960-73 · Pubmed

    Plants have often been moved across the globe with intact root systems. These roots are likely to have housed symbiotic ectomycorrhizal (EM) fungi and the movement of plants may have facilitated the introduction of EM fungi.Here, we report data compiled from a newly created database of EM fungal introductions.We estimate the magnitude of EM fungal introductions around the world and examine patterns associated with these introductions. We also use the data to develop a framework for understanding the invasion biology of EM fungi.At least 200 species of basidiomycete and ascomycete EM fungi have been moved from native ranges to novel habitats. The majority of recorded introductions are associated with Pinus or Eucalyptus plantations in the southern hemisphere. Most introduced species appear to be constrained from spreading in novel habitats and associate only with their introduced hosts. Aspects of life history, including host range, may influence the ability of EM species to establish or invade. Human-caused introductions of EM fungi are a common and global phenomenon.The mechanisms controlling EM fungi in novel habitats and potential impacts of EM fungal introductions are almost entirely unknown.

  • Roper M, Pepper RE, Brenner MP, Pringle A (2008) Explosively launched spores of ascomycete fungi have drag-minimizing shapes. Proc. Natl. Acad. Sci. U.S.A. 105(52):20583-8 (PMC2634873) · Pubmed

    The forcibly launched spores of ascomycete fungi must eject through several millimeters of nearly still air surrounding fruiting bodies to reach dispersive air flows. Because of their microscopic size, spores experience great fluid drag, and although this drag can aid transport by slowing sedimentation out of dispersive air flows, it also causes spores to decelerate rapidly after launch. We hypothesize that spores are shaped to maximize their range in the nearly still air surrounding fruiting bodies. To test this hypothesis we numerically calculate optimal spore shapes-shapes of minimum drag for prescribed volumes-and compare these shapes with real spore shapes taken from a phylogeny of >100 species. Our analysis shows that spores are constrained to remain within 1% of the minimum possible drag for their size. From the spore shapes we predict the speed of spore launch, and confirm this prediction through high-speed imaging of ejection in Neurospora tetrasperma. By reconstructing the evolutionary history of spore shapes within a single ascomycete family we measure the relative contributions of drag minimization and other shape determinants to spore shape evolution. Our study uses biomechanical optimization as an organizing principle for explaining shape in a mega-diverse group of species and provides a framework for future measurements of the forces of selection toward physical optima.

  • Pringle A, Bever JD (2008) Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol. 180(1):162-75 · Pubmed

    Although arbuscular mycorrhizal (AM) fungi are ubiquitous symbionts of plants, the mutualism has rarely been tested in nature. In experiments designed to explore the ecological relevance of associations between different fungal and plant species in a natural environment, plant species were infected with different species of fungi and grown in separate trials in the laboratory and a North Carolina (USA) field. The benefits to plants varied dramatically as plant species were grown with different species of AM fungi. Effects of mycorrhizal fungi in nature were generally correlated to effects in the growth chamber, suggesting that laboratory data do reflect dynamics between plants and AM fungi in the field. Initial size at transplant and experimental block were also significant predictors of plant growth in the field. Correlation statistics between laboratory and field data were weaker when analyses involved plant species less responsive to infection by any AM fungus, suggesting that the response of a species to inoculation is a good predictor of its sensitivity to specific AM fungi in the field. AM fungal identity appears to influence the growth and reproduction of plants in the field.

  • Peterson CN, Day S, Wolfe BE, Ellison AM, Kolter R, Pringle A (2008) A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environ. Microbiol. 10(9):2257-66 · Pubmed

    The community of organisms inhabiting the water-filled leaves of the carnivorous pitcher-plant Sarracenia purpurea includes arthropods, protozoa and bacteria, and serves as a model system for studies of food web dynamics. Despite the wealth of data collected by ecologists and zoologists on this food web, very little is known about the bacterial assemblage in this microecosystem. We used terminal restriction fragment length polymorphism (T-RFLP) analysis to quantify bacterial diversity within the pitchers as a function of pitcher size, pH of the pitcher fluid and the presence of the keystone predator in this food web, larvae of the pitcher-plant mosquito Wyeomyia smithii. Results were analysed at two spatial scales: within a single bog and across three isolated bogs. Pitchers were sterile before they opened and composition of the bacterial assemblage was more variable between different bogs than within bogs. Measures of bacterial richness and diversity were greater in the presence of W. smithii and increased with increasing pitcher size. Our results suggest that fundamental ecological concepts derived from macroscopic food webs can also be used to predict the bacterial assemblages in pitcher plants.

  • Gilchrist MA, Sulsky DL, Pringle A (2006) Identifying fitness and optimal life-history strategies for an asexual filamentous fungus. Evolution 60(5):970-9 · Pubmed

    Filamentous fungi are ubiquitous and ecologically important organisms with rich and varied life histories, however, there is no consensus on how to identify or measure their fitness. In the first part of this study we adapt a general epidemiological model to identify the appropriate fitness metric for a saprophytic filamentous fungus. We find that fungal fitness is inversely proportional to the equilibrium density of uncolonized fungal resource patches which, in turn, is a function of the expected spore production of a fungus. In the second part of this study we use a simple life history model of the same fungus within a resource patch to show that a bang-bang resource allocation strategy maximizes the expected spore production, a critical fitness component. Unlike bang-bang strategies identified in other life-history studies, we find that the optimal allocation strategy for saprophytes does not entail the use of all of the resources within a patch.

  • Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol. Lett. 9(5):501-15 · Pubmed

    Advances in ecology during the past decade have led to a much more detailed understanding of the potential negative consequences of species' introductions. Moreover, recent studies of mycorrhizal symbionts have led to an increased knowledge of the potential utility of fungal inoculations in agricultural, horticultural and ecological management. The intentional movement of mycorrhizal fungal species is growing, but the concomitant potential for negative ecological consequences of invasions by mycorrhizal fungi is poorly understood. We assess the degree to which introductions of mycorrhizal fungi may lead to unintended negative, and potentially costly, consequences. Our purpose is to make recommendations regarding appropriate management guidelines and highlight top priority research needs. Given the difficulty in discerning invasive species problems associated with mycorrhizal inoculations, we recommend the following. First, careful assessment documenting the need for inoculation, and the likelihood of success, should be conducted prior to inoculation because inoculations are not universally beneficial. Second, invasive species problems are costly and often impossible to control by the time they are recognized. We recommend using local inoculum sources whenever possible. Third, non-sterile cultures of inoculum can result in the movement of saprobes and pathogens as well as mutualists. We recommend using material that has been produced through sterile culture when local inoculum is not available. Finally, life-history characteristics of inoculated fungi may provide general guidelines relative to the likelihood of establishment and spread. We recommend that, when using non-local fungi, managers choose fungal taxa that carry life-history traits that may minimize the likelihood of deleterious invasive species problems. Additional research is needed on the potential of mycorrhizal fungi to spread to non-target areas and cause ecological damage.

  • Pringle A, Patek SN, Fischer M, Stolze J, Money NP (2006) The captured launch of a ballistospore. Mycologia 97(4):866-71 · Pubmed

    Ballistospore discharge is a feature of 30000 species of mushrooms, basidiomycete yeasts and pathogenic rusts and smuts. The biomechanics of discharge may involve an abrupt change in the center of mass associated with the coalescence of Buller's drop and the spore. However this process occurs so rapidly that the launch of the ballistospore has never been visualized. Here we report ultra high-speed video recordings of the earliest events of spore dispersal using the yeast Itersonilia perplexans and the distantly related jelly fungus Auricularia auricula. Images taken at camera speeds of up to 100,000 frames/ s demonstrate that ballistospore discharge does involve the coalescence of Buller's drop and the spore. Recordings of I. perplexans demonstrate that although coalescence may result from the directed collapse of Buller's drop onto the spore, it also may involve the movement of the spore toward the drop. The release of surface tension at coalescence provides the energy and directional momentum to propel the drop and spore away from the fungus. Analyses show that ballistospores launch into the air at initial accelerations in excess of 10,000 g. There is no known analog of this micromechanical process in animals, plants or bacteria, but the recent development of a surface tension motor may mimic the fungal biology described here.

  • Pringle A, Baker DM, Platt JL, Wares JP, Latgé JP, Taylor JW (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59(9):1886-99 · Pubmed

    Microbes and other organisms smaller than one to a few millimeters in size are hypothesized to have global populations, in contrast to the geographically restricted ranges of larger organisms. However, fungi, which routinely have reproductive propagules no larger than 10 micrometers, challenge the generality of this hypothesis because recent studies have shown that globally distributed morphological species embrace two or more geographically restricted phylogenetic species. We used the concordance of gene genealogies to recognize phylogenetic species in the globally distributed opportunistic human pathogenic fungus, Aspergillus fumigatus. Based on DNA sequence data of five loci for each of 63 individuals collected from five continents, we have delineated two phylogenetic species in this single morphological species. Unlike all other fungi examined to date, both genetically isolated groups showed a global distribution with no evidence of a correlation between genotype and geographic location. Sexual reproduction has never been observed in A. fumigatus, but when the same data were used to explore the association of alleles at the five loci for one of the phylogenetic species, evidence was found to support recombination. The discovery of a cryptic species is medically relevant because different species are likely to differ in virulence or drug resistance. The discovery of a globally distributed A. fumigatus species clade highlights the need for ecological studies of the fungus to either document global dispersal or propose alternative mechanisms by which it persists as single, global phylogenetic population.

  • Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution 57(12):2721-41 · Pubmed

    We critically examined methods for recognizing species in the model filamentous fungal genus Neurospora by comparing traditional biological species recognition (BSR) with more comprehensive applications of both BSR and phylogenetic species recognition (PSR). Comprehensive BSR was applied to a set of 73 individuals by performing extensive crossing experiments and delineating biological species based on patterns of reproductive success. Within what were originally considered two species, N. crassa and N. intermedia, we recognized four reproductively isolated biological species. In a concurrent study (Dettman et al. 2003), we used genealogical concordance of four independent nuclear loci to recognize phylogenetic species in Neurospora. Overall, the groups of individuals identified as species were similar whether recognized by reproductive success or by phylogenetic criteria, and increased genetic distance between parents was associated with decreased reproductive success of crosses, suggesting that PSR using genealogical concordance can be used to reliably recognize species in organisms that are not candidates for BSR. In one case, two phylogenetic species were recognized as a single biological species, indicating that significant phylogenetic divergence preceded the development of reproductive isolation. However, multiple biological species were never recognized as a single phylogenetic species. Each of the putative N. crassa x N. intermedia hybrids included in this study was confidently assigned to a single species, using both PSR and BSR. As such, no evidence for a history of hybridization in nature among Neurospora species was observed. By performing reciprocal mating tests, we found that mating type, parental role, and species identity of parental individuals could all influence the reproductive success of matings. We also observed sympatry-associated sexual dysfunction in interspecific crosses, which was consistent with the existence of reinforcement mechanisms.

  • Pringle A, Moncalvo JM, Vilgalys R (2003) Revisiting the rDNA sequence diversity of a natural population of the arbuscular mycorrhizal fungus Acaulospora colossica. Mycorrhiza 13(4):227-31 · Pubmed

    In 1999, the diversity of a field population of the arbuscular mycorrhizal (AM) fungus Acaulospora colossica was characterized using DNA sequence data. Since 1999, AM fungal sequences have accumulated rapidly within public databases. Moreover, novel phylogenetic tools have been developed and can be used to interpret the data. A second analysis of those sequences collected in 1999 demonstrates that while the majority of the sequences are, in fact, sequences of A. colossica; a minority of the sequences still cannot be identified with confidence. Those sequences identified as A. colossica can be used to show that (1) the nuclear rDNA ITS regions are remarkably diverse, and (2) sequences isolated from different spores of the same site may be more closely related to each other than to sequences of other sites, so that the genetic diversity of an AM fungal field population may be spatially structured; however, identical sequences can also be recovered from different sites.

  • Pringle A, Taylor J (2002) The fitness of filamentous fungi. Trends Microbiol. 10(10):474-81 · Pubmed

    Fitness is a common currency in comparative biology. Without data on fitness, hypotheses about the adaptive significance of phenotypes or basic mechanisms of evolution, for example natural selection, remain speculative. Experiments with fungi can address questions specific to fungi or questions with a broader significance. Fungi can challenge the generality of fundamental evolutionary principles, yet there are no standard measures of fungal fitness. We argue that focusing on a single aspect of a complex life cycle, or a single measure of fitness (e.g. the number of asexual spores) is appropriate. Choosing which aspect of fitness to measure can be facilitated by an understanding of how fitness measures are correlated. Choices can also be based on the ecology of a species, for example whether a fungus is semelparous and reproduces once, or iteroparous and reproduces multiple times.

  • Pringle A, Bever JD (2002) Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am. J. Bot. 89(9):1439-46 · Pubmed

    Interest in the diversity of arbuscular mycorrhizal (AM) fungal communities has been stimulated by recent data that demonstrate that fungal communities influence the competitive hierarchies, productivity, diversity, and successional patterns of plant communities. Although natural communities of AM fungi are diverse, we have a poor understanding of the mechanisms that promote and maintain that diversity. Plants may coexist by inhabiting disparate temporal niches; plants of many grasslands are either warm or cool season specialists. We hypothesized that AM fungi might be similarly seasonal. To test our hypothesis, we tracked the sporulation of individual AM fungal species growing within a North Carolina grassland. Data were collected in 1996 and 1997; in 1997, sampling focused on two common species. We found that AM fungi, especially Acaulospora colossica and Gigaspora gigantea, maintained different and contrasting seasonalities. Acaulospora colossica sporulated more frequently in the warm season, but Gi. gigantea sporulated more frequently in the cool season. Moreover, AM fungal species were spatially aggregated at a fine scale. Contrasting seasonal and spatial niches may facilitate the maintenance of a diverse community of AM fungi. Furthermore, these data may illuminate our understanding of the AM fungal influence on plant communities: various fungal species may preferentially associate with different plant species and thereby promote diversity in the plant community.

  • Sniegowski PD, Pringle A, Hughes KA (1994) Effects of autosomal inversions on meiotic exchange in distal and proximal regions of the X chromosome in a natural population of Drosophila melanogaster. Genet. Res. 63(1):57-62 · Pubmed

    We have investigated the interchromosomal effect of the naturally-occurring paracentric inversions In(2L)t and In(3R)P on meiotic recombination in two regions of the X chromosome in Drosophila melanogaster. Previous authors have suggested that the rate of recombination at the tip of the X chromosome may be substantially higher in some natural populations than values measured in the laboratory, due to the interchromosomal effect of heterozygous autosomal inversions. This suggestion was motivated by observations that transposable elements are not as common at the tip of the X chromosome as predicted by recent research relating reduced meiotic exchange to increased element abundance in D. melanogaster. We examined the effects of heterozygous In(2L)t and In(3R)P on recombination at both the tip and base of the X chromosome on a background of isogenic major chromosomes from a natural population. Both inversions substantially increased the rate of recombination at the base; neither one affected recombination at the tip. The results suggest that the presence of inversions in the study population does not elevate rates of crossing over at the tip of the X chromosome. The relevance of these results to ideas relating transposable element abundance to recombination rates is discussed.

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