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1. Fungal elemental profiling unleashed through rapid laser-induced breakdown spectroscopy (LIBS)

Author

Tomás A. Rush, Ann M. Wymore, Miguel Rodríguez, Jr, Sara Jawdy, Rytas J. Vilgalys, Madhavi Z. Martin, and Hunter B. Andrews

Subjects
fungal behavior, elemental profiling, ionomics, endophytes, poplar, LIBS, Microbiology, QR1-502
Abstract

ABSTRACT Elemental profiling of fungal species as a phenotyping tool is an understudied topic and is typically performed to examine plant tissue or non-biological materials. Traditional analytical techniques such as inductively coupled plasma–optical emission spectroscopy (ICP-OES) and inductively coupled plasma–mass spectrometry (ICP-MS) have been used to identify elemental profiles of fungi; however, these techniques can be cumbersome due to the difficulty of preparing samples. Additionally, the instruments used for these techniques can be expensive to procure and operate. Laser-induced breakdown spectroscopy (LIBS) is an alternative elemental analytical technique—one that is sensitive across the periodic table, easy to use on various sample types, and is cost-effective in both procurement and operation. LIBS has not been used on axenic filamentous fungal isolates grown in substrate media. In this work, as a proof of concept, we used LIBS on two genetically distinct fungal species grown on a nutrient-rich and nutrient-poor substrate media to determine whether robust elemental profiles can be detected and whether differences between the fungal isolates can be identified. Our results demonstrate a distinct correlation between fungal species and their elemental profile, regardless of the substrate media, as the same strains shared a similar uptake of carbon, zinc, phosphorus, manganese, and magnesium, which could play a vital role in their survival and propagation. Independently, each fungal species exhibited a unique elemental profile. This work demonstrates a unique and valuable approach to rapidly phenotype fungi through optical spectroscopy, and this approach can be critical in understanding these fungi's behavior and interactions with the environment.IMPORTANCEHistorically, ionomics, the elemental profiling of an organism or materials, has been used to understand the elemental composition in waste materials to identify and recycle heavy metals or rare earth elements, identify the soil composition in space exploration on the moon or Mars, or understand human disorders or disease. To our knowledge, ionomic profiling of microbes, particularly fungi, has not been investigated to answer applied and fundamental biological questions. The reason is that current ionomic analytical techniques can be laborious in sample preparation, fail to measure all potential elements accurately, are cost-prohibitive, or provide inconsistent results across replications. In our previous efforts, we explored whether laser-induced breakdown spectroscopy (LIBS) could be used in determining the elemental profiles of poplar tissue, which was successful. In this proof-of-concept endeavor, we undertook a transdisciplinary effort between applied and fundamental mycology and elemental analytical techniques to address the biological question of how LIBS can used for fungi grown axenically in a nutrient-rich and nutrient-poor environment.

Published
2024
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2. Interactions with microbial consortia have variable effects in organic carbon and production of exometabolites among genotypes of Populus trichocarpa

Author

Alyssa A. Carrell, Miranda Clark, Sara Jawdy, Wellington Muchero, Gladys Alexandre, Jesse L. Labbé, and Tomás A. Rush

Subjects
beneficial bacteria, metabolomics, mycorrhizal fungi, poplar exometabolites, total organic carbon, Botany, QK1-989
Abstract

Abstract Poplar is a short‐rotation woody crop frequently studied for its significance as a sustainable bioenergy source. The successful establishment of a poplar plantation partially depends on its rhizosphere—a dynamic zone governed by complex interactions between plant roots and a plethora of commensal, mutualistic, symbiotic, or pathogenic microbes that shape plant fitness. In an exploratory endeavor, we investigated the effects of a consortium consisting of ectomycorrhizal fungi and a beneficial Pseudomonas sp. strain GM41 on plant growth (including height, stem girth, leaf, and root growth) and as well as growth rate over time, across four Populus trichocarpa genotypes. Additionally, we compared the level of total organic carbon and plant exometabolite profiles across different poplar genotypes in the presence of the microbial consortium. These data revealed no significant difference in plant growth parameters between the treatments and the control across four different poplar genotypes at 7 weeks post‐inoculation. However, total organic carbon and exometabolite profiles were significantly different between the genotypes and the treatments. These findings suggest that this microbial consortium has the potential to trigger early signaling responses in poplar, influencing its metabolism in ways crucial for later developmental processes and stress tolerance.

Published
2023
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3. LaeA-Regulated Fungal Traits Mediate Bacterial Community Assembly

Author

Joanna Tannous, Casey M. Cosetta, Milton T. Drott, Tomás A. Rush, Paul E. Abraham, Richard J. Giannone, Nancy P. Keller, and Benjamin E. Wolfe

Subjects
Penicillium, fungal metabolites, microbiome, Microbiology, QR1-502
Abstract

ABSTRACT Potent antimicrobial metabolites are produced by filamentous fungi in pure culture, but their ecological functions in nature are often unknown. Using an antibacterial Penicillium isolate and a cheese rind microbial community, we demonstrate that a fungal specialized metabolite can regulate the diversity of bacterial communities. Inactivation of the global regulator, LaeA, resulted in the loss of antibacterial activity in the Penicillium isolate. Cheese rind bacterial communities assembled with the laeA deletion strain had significantly higher bacterial abundances than the wild-type strain. RNA-sequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in the laeA deletion strain. Inactivation of a core gene in the pseurotin biosynthetic cluster restored bacterial community composition, confirming the role of pseurotins in mediating bacterial community assembly. Our discovery demonstrates how global regulators of fungal transcription can control the assembly of bacterial communities and highlights an ecological role for a widespread class of fungal specialized metabolites. IMPORTANCE Cheese rinds are economically important microbial communities where fungi can impact food quality and aesthetics. The specific mechanisms by which fungi can regulate bacterial community assembly in cheeses, other fermented foods, and microbiomes in general are largely unknown. Our study highlights how specialized metabolites secreted by a Penicillium species can mediate cheese rind development via differential inhibition of bacterial community members. Because LaeA regulates specialized metabolites and other ecologically relevant traits in a wide range of filamentous fungi, this global regulator may have similar impacts in other fungus-dominated microbiomes.

Published
2023
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4. Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

Author

Tomás A. Rush, Joanna Tannous, Matthew J. Lane, Muralikrishnan Gopalakrishnan Meena, Alyssa A. Carrell, Jacob J. Golan, Milton T. Drott, Sylvain Cottaz, Sébastien Fort, Jean-Michel Ané, Nancy P. Keller, Dale A. Pelletier, Daniel A. Jacobson, David Kainer, Paul E. Abraham, Richard J. Giannone, and Jesse L. Labbé

Subjects
lipo-chitooligosaccharides, secondary metabolites, synergism, biosynthetic gene clusters, bacteria, Aspergillus, Microbiology, QR1-502
Abstract

ABSTRACT Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition. IMPORTANCE The activation of silent biosynthetic gene clusters (BGC) for the identification and characterization of novel fungal secondary metabolites is a perpetual motion in natural product discoveries. Here, we demonstrated that one of the best-studied symbiosis signaling compounds, lipo-chitooligosaccharides (LCOs), play a role in activating some of these BGCs, resulting in the production of known, putative, and unknown metabolites with biological activities. This collection of metabolites induced by LCOs differentially modulate bacterial growth, while the LCO standards do not convey the same effect. These findings create a paradigm shift showing that LCOs have a more prominent role outside of host recognition of symbiotic microbes. Importantly, our work demonstrates that fungi use LCOs to produce a variety of metabolites with biological activity, which can be a potential source of bio-stimulants, pesticides, or pharmaceuticals.

Published
2022
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5. Expanding the Biological Role of Lipo-Chitooligosaccharides and Chitooligosaccharides in Laccaria bicolor Growth and Development

Author

Manuel I. Villalobos Solis, Nancy L. Engle, Margaret K. Spangler, Sylvain Cottaz, Sébastien Fort, Junko Maeda, Jean-Michel Ané, Timothy J. Tschaplinski, Jesse L. Labbé, Robert L. Hettich, Paul E. Abraham, and Tomás A. Rush

Subjects
Laccaria bicolor, lipo-chitooligosaccharides, polarized growth, proteomics, chitooligosaccharides, Plant culture, SB1-1110
Abstract

The role of lipo-chitooligosaccharides (LCOs) as signaling molecules that mediate the establishment of symbiotic relationships between fungi and plants is being redefined. New evidence suggests that the production of these molecular signals may be more of a common trait in fungi than what was previously thought. LCOs affect different aspects of growth and development in fungi. For the ectomycorrhizal forming fungi, Laccaria bicolor, the production and effects of LCOs have always been studied with a symbiotic plant partner; however, there is still no scientific evidence describing the effects that these molecules have on this organism. Here, we explored the physiological, molecular, and metabolomic changes in L. bicolor when grown in the presence of exogenous sulfated and non-sulfated LCOs, as well as the chitooligomers, chitotetraose (CO4), and chitooctaose (CO8). Physiological data from 21 days post-induction showed reduced fungal growth in response to CO and LCO treatments compared to solvent controls. The underlying molecular changes were interrogated by proteomics, which revealed substantial alterations to biological processes related to growth and development. Moreover, metabolite data showed that LCOs and COs caused a downregulation of organic acids, sugars, and fatty acids. At the same time, exposure to LCOs resulted in the overproduction of lactic acid in L. bicolor. Altogether, these results suggest that these signals might be fungistatic compounds and contribute to current research efforts investigating the emerging impacts of these molecules on fungal growth and development.

Published
2022
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6. Bioprospecting Trichoderma: A Systematic Roadmap to Screen Genomes and Natural Products for Biocontrol Applications

Author

Tomás A. Rush, Him K. Shrestha, Muralikrishnan Gopalakrishnan Meena, Margaret K. Spangler, J. Christopher Ellis, Jesse L. Labbé, and Paul E. Abraham

Subjects
predictive biology, functional genomics, secondary metabolites, antimicrobials, integrated pest management, plant-microbe interactions, Plant culture, SB1-1110
Abstract

Natural products derived from microbes are crucial innovations that would help in reaching sustainability development goals worldwide while achieving bioeconomic growth. Trichoderma species are well-studied model fungal organisms used for their biocontrol properties with great potential to alleviate the use of agrochemicals in agriculture. However, identifying and characterizing effective natural products in novel species or strains as biological control products remains a meticulous process with many known challenges to be navigated. Integration of recent advancements in various “omics” technologies, next generation biodesign, machine learning, and artificial intelligence approaches could greatly advance bioprospecting goals. Herein, we propose a roadmap for assessing the potential impact of already known or newly discovered Trichoderma species for biocontrol applications. By screening publicly available Trichoderma genome sequences, we first highlight the prevalence of putative biosynthetic gene clusters and antimicrobial peptides among genomes as an initial step toward predicting which organisms could increase the diversity of natural products. Next, we discuss high-throughput methods for screening organisms to discover and characterize natural products and how these findings impact both fundamental and applied research fields.

Published
2021
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7. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Author

Tomás Allen Rush, Virginie Puech-Pagès, Adeline Bascaules, Patricia Jargeat, Fabienne Maillet, Alexandra Haouy, Arthur QuyManh Maës, Cristobal Carrera Carriel, Devanshi Khokhani, Michelle Keller-Pearson, Joanna Tannous, Kevin R. Cope, Kevin Garcia, Junko Maeda, Chad Johnson, Bailey Kleven, Quanita J. Choudhury, Jessy Labbé, Candice Swift, Michelle A. O’Malley, Jin Woo Bok, Sylvain Cottaz, Sébastien Fort, Verena Poinsot, Michael R. Sussman, Corinne Lefort, Jeniel Nett, Nancy P. Keller, Guillaume Bécard, and Jean-Michel Ané

Subjects
Science
Abstract

Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by certain bacteria and fungi that establish symbiotic relationships with plants. Here, the authors show that LCOs are produced also by many other, non-symbiotic fungi, and regulate fungal growth and development.

Published
2020
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8. Differences in Spore Size and Atmospheric Survival Shape Stark Contrasts in the Dispersal Dynamics of Two Closely Related Fungal Pathogens

Author

Jacob Golan, Daniele Lagomarsino Oneto, Shunping Ding, Reinhard Kessenich, Melvin Sandler, Tomás A. Rush, Daniel Levitis, Amanda Gevens, Agnese Seminara, and Anne Pringle

Abstract

A frequently ignored but critical aspect of microbial dispersal is survival in the atmosphere. We exposed spores of two closely related, morphologically dissimilar, and economically important fungal pathogens to typical atmospheric environments and modeled their movement in the troposphere. We first measured the mortality ofAlternaria solaniandA. alternataconidia exposed to ranges of solar radiation, relative humidity, and temperature. We then measured survival in an advantageous environment over 12 days.A. solaniconidia are nearly 10 times larger thanA. alternataconidia and most die after 24 hours. By contrast, over half ofA. alternataconidia remained viable at 12 days. The greater viability of the smaller spores is counterintuitive as larger spores are assumed to be more durable. To elucidate the consequences of survival rates for dispersal, we deployed models of atmospheric spore movement across North American. We predict 99% of the largerA. solaniconidia settle within 24 hours, with a maximum dispersal distance of 100 km. By contrast, mostA. alternataconidia remain airborne for more than 12 days and long-distance dispersal is possible, e.g., from Wisconsin to the Atlantic Ocean. We observe that the larger conidia ofA. solanisurvive poorly but also land sooner and move over shorter distances as compared to the smaller conidia ofA. alternata. Our data relating larger spore size to poorer survival in the atmosphere and shorter distances travelled likely translate to other fungal species and highlight the potential for starkly different dispersal dynamics among even closely related fungi.

Published
2023
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9. Fungal antibiotics control bacterial community diversity in the cheese rind microbiome

Author

Joanna Tannous, Casey M. Cosetta, Milton T. Drott, Tomás A. Rush, Paul E. Abraham, Richard J. Giannone, Nancy P. Keller, and Benjamin E. Wolfe

Abstract

Potent antimicrobial metabolites are produced by filamentous fungi in pure lab cultures, but their ecological functions in nature are often unknown. Using an antibiotic-producingPenicilliumisolate and the cheese rind microbial community, we demonstrate that a fungal specialized metabolite can regulate the diversity of bacterial communities. Inactivation of the global regulator, LaeA, resulted in the loss of antibacterial activity in thePenicilliumisolate. Cheese rind bacterial communities assembled with thelaeAdeletion strain had significantly higher bacterial abundances than the wild-type strain. RNA-sequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in thelaeAdeletion strain. Inactivation of a core gene in the pseurotin biosynthetic cluster restored bacterial community composition, demonstrating the role of pseurotins in mediating bacterial community assembly. Our discovery demonstrates how antibiotic production can drive the assembly of microbiomes and provides an ecological context for widespread fungal specialized metabolites.

Published
2022
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10. A guidance into the fungal metabolomic abyss: Network analysis for revealing relationships between exogenous compounds and their outputs

Author

Muralikrishnan Gopalakrishnan Meena, Matthew J. Lane, Joanna Tannous, Alyssa A. Carrell, Paul E. Abraham, Richard J. Giannone, Jean-Michel Ané, Nancy P. Keller, Jesse L. Labbé, David Kainer, Daniel A. Jacobson, and Tomás A. Rush

Abstract

Fungal specialized metabolites include many bioactive compounds with potential applications as pharmaceuticals, agrochemical agents, and industrial chemicals. Exploring and discovering novel fungal metabolites is critical to combat antimicrobial resistance in various fields, including medicine and agriculture. Yet, identifying the conditions or treatments that will trigger the production of specialized metabolites in fungi can be cumbersome since most of these metabolites are not produced under standard culture conditions. Here, we introduce a data-driven algorithm comprising various network analysis routes to characterize the production of known and putative specialized metabolites and unknown analytes triggered by different exogenous compounds. We use bipartite networks to quantify the relationship between the metabolites and the treatments stimulating their production through two routes. The first, called the direct route, determines the production of known and putative specialized metabolites induced by a treatment. The second, called the auxiliary route, is specific for unknown analytes. We demonstrated the two routes by applying chitooligosaccharides and lipids at two different temperatures to the opportunistic human fungal pathogen Aspergillus fumigatus. We used various network centrality measures to rank the treatments based on their ability to trigger a broad range of specialized metabolites. The specialized metabolites were ranked based on their receptivity to various treatments. Altogether, our data-driven techniques can track the influence of any exogenous treatment or abiotic factor on the metabolomic output for targeted metabolite research. This approach can be applied to complement existing LC/MS analyses to overcome bottlenecks in drug discovery and development from fungi.NoticeThis manuscript has been authored by UT-Battelle, LLC, under contract DE-AC05-00OR22725 with the US Department of Energy (DOE). The US government retains and the publisher, by accepting the article for publication, acknowledges that the US government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for US government purposes. DOE will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).Author summaryTriggering silent biosynthetic gene clusters in fungi to produce specialized metabolites is a tedious process that requires assessing various environmental conditions, applications of epigenetic modulating agents, or co-cultures with other microbes. We provide a data-driven solution using network analysis, called “direct route”, to characterize the production of known and putative specialized metabolites triggered by various exogenous compounds. We also provide a “auxiliary route” to distinguish unique unknown analytes amongst the abundantly produced analytes in response to these treatments. The developed techniques can assist researchers to identify treatments or applications that could positively influence the production of a targeted metabolite or recognize unique unknown analytes that can be further fractionated, characterized, and screened for their biological activities and hence, discover new metabolites.

Published
2022
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11. Farysia magdalena sp. nov. and description of the anamorph of Anthracocystis heteropogonicola from the Americas

Author

Tomás Allen Rush, M. Catherine Aime, Sebastian Albu, and Teeratas Kijpornyongpan

Subjects
0106 biological sciences, Western hemisphere, 0303 health sciences, Phylogenetic tree, biology, Ustilaginaceae, fungi, Anthracocystis, Fungus, biology.organism_classification, 010603 evolutionary biology, 01 natural sciences, Agricultural and Biological Sciences (miscellaneous), Yeast, 030308 mycology & parasitology, 03 medical and health sciences, Botany, Phyllosphere, Ecology, Evolution, Behavior and Systematics
Abstract

Several interesting Ustilaginaceae yeast morphs were isolated during ongoing surveys of phylloplane-associated fungi in Louisiana (USA) and Guyana. Here we describe Farysia magdalena sp. nov., a phylloplane yeast isolated in southern Louisiana, based on phylogenetic analyses, assimilation profiles and morphological characters, and discuss the yeast morphs in this genus. Additionally, we describe the anamorphic stage of Anthracocystis heteropogonicola, isolated from plant phylloplanes from the Americas. This is the first report of this fungus in the Western Hemisphere and the first description of the yeast morph for a species of Anthracocystis.

Published
2020
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12. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Author

Candice L. Swift, Arthur QuyManh Maes, Nancy P. Keller, Cristobal Carrera Carriel, Kevin Garcia, Guillaume Bécard, Joanna Tannous, Quanita J. Choudhury, Jean-Michel Ané, Michelle A. O’Malley, Junko Maeda, Jin Woo Bok, Michelle Keller-Pearson, Tomás Allen Rush, Patricia Jargeat, Virginie Puech-Pagès, Sylvain Cottaz, Michael R. Sussman, Fabienne Maillet, Jeniel E. Nett, Adeline Bascaules, Jessy Labbé, Kevin R. Cope, Alexandra Haouy, Bailey Kleven, Véréna Poinsot, Chad J. Johnson, Sébastien Fort, Corinne Lefort, Devanshi Khokhani, Fort, Sébastien, University of Wisconsin-Madison, Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, Evolution des Interactions Plantes-Microorganismes, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Interactions moléculaires et réactivité chimique et photochimique (IMRCP), Institut de Chimie de Toulouse (ICT-FR 2599), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), South Dakota State University (SDSTATE), North Carolina State University [Raleigh] (NC State), University of North Carolina System (UNC), The University of Tennessee [Knoxville], University of Georgia [USA], University of California [Santa Barbara] (UC Santa Barbara), University of California (UC), Centre de Recherches sur les Macromolécules Végétales (CERMAV), Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA), Université Fédérale Toulouse Midi-Pyrénées, Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, University of California [Santa Barbara] (UCSB), University of California, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Fluides, Energie, Réacteurs, Matériaux et Transferts (FERMAT), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), BIBAC - Chimie analytique et interactions biomolécules - matière molle biomimétique (BIBAC), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT), and ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017)

Subjects
0301 basic medicine, Hypha, Science, General Physics and Astronomy, Oligosaccharides, Chitin, 02 engineering and technology, Biology, General Biochemistry, Genetics and Molecular Biology, Article, Microbiology, Microbial ecology, 03 medical and health sciences, Fungal biology, Pseudohyphal growth, Symbiosis, Ascomycota, Mycorrhizae, Spore germination, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Cellular microbiology, Fungal ecology, lcsh:Science, [SDV.BBM.BC] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Chitosan, Multidisciplinary, Ecology, Phylum, Basidiomycota, Fatty Acids, fungi, Fungi, General Chemistry, Spores, Fungal, 021001 nanoscience & nanotechnology, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Spore, 030104 developmental biology, lcsh:Q, 0210 nano-technology, Bacteria, Rhizobium, Signal Transduction
Abstract

Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development., Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by certain bacteria and fungi that establish symbiotic relationships with plants. Here, the authors show that LCOs are produced also by many other, non-symbiotic fungi, and regulate fungal growth and development.

Published
2020
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13. Variation in the Internal Transcribed Spacer Region of Phakopsora pachyrhizi and Implications for Molecular Diagnostic Assays

Author

Cade N. Kane, Jacob Golan, Tomás Allen Rush, Alistair R. McTaggart, R. W. Schneider, and M. Catherine Aime

Subjects
Genetics, Phakopsora pachyrhizi, biology.protein, Plant Science, Biology, Internal transcribed spacer, Soybean rust, biology.organism_classification, Agronomy and Crop Science, DNA barcoding, Polymerase
Abstract

Phakopsora pachyrhizi, the causal agent of soybean rust (SBR), is a global threat to soybean production. Since the discovery of SBR in the continental United States, quantitative polymerase chain reaction assays based on the internal transcribed spacer (ITS) ribosomal DNA locus were established for its rapid detection. However, insufficient data were initially available to test assays against factors that could give rise to misidentification. This study aimed to reevaluate current assays for (i) the potential for false-positive detection caused by nontarget Phakopsora species and (ii) the potential for false-negative detection caused by intraspecific variation within the ITS locus of P. pachyrhizi. A large amount of intraspecific and intragenomic variation in ITS was detected, including the presence of polymorphic ITS copies within single leaf samples and within single rust sori. The diagnostic assays were not affected by polymorphisms in the ITS region; however, current assays are at risk of false positives when screened against other species of Phakopsora. This study raises caveats to the use of multicopy genes (e.g., ITS) in single-gene detection assays and discusses the pitfalls of inferences concerning the aerobiological pathways of disease spread made in the absence of an evaluation of intragenomic ITS heterogeneity.

Published
2019
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14. Microevolution in the pansecondary metabolome of

Author

Milton T, Drott, Tomás A, Rush, Tatum R, Satterlee, Richard J, Giannone, Paul E, Abraham, Claudio, Greco, Nandhitha, Venkatesh, Jeffrey M, Skerker, N Louise, Glass, Jesse L, Labbé, Michael G, Milgroom, and Nancy P, Keller

Subjects
Fungal Proteins, Aspergillus, Genetic Speciation, Multigene Family, Metabolome, Secondary Metabolism, Genomics, Metagenomics, Genome, Fungal, Biological Sciences, Phylogeny, United States, Aspergillus flavus
Abstract

Fungi produce a wealth of pharmacologically bioactive secondary metabolites (SMs) from biosynthetic gene clusters (BGCs). It is common practice for drug discovery efforts to treat species’ secondary metabolomes as being well represented by a single or a small number of representative genomes. However, this approach misses the possibility that intraspecific population dynamics, such as adaptation to environmental conditions or local microbiomes, may harbor novel BGCs that contribute to the overall niche breadth of species. Using 94 isolates of Aspergillus flavus, a cosmopolitan model fungus, sampled from seven states in the United States, we dereplicate 7,821 BGCs into 92 unique BGCs. We find that more than 25% of pangenomic BGCs show population-specific patterns of presence/absence or protein divergence. Population-specific BGCs make up most of the accessory-genome BGCs, suggesting that different ecological forces that maintain accessory genomes may be partially mediated by population-specific differences in secondary metabolism. We use ultra-high-performance high-resolution mass spectrometry to confirm that these genetic differences in BGCs also result in chemotypic differences in SM production in different populations, which could mediate ecological interactions and be acted on by selection. Thus, our results suggest a paradigm shift that previously unrealized population-level reservoirs of SM diversity may be of significant evolutionary, ecological, and pharmacological importance. Last, we find that several population-specific BGCs from A. flavus are present in Aspergillus parasiticus and Aspergillus minisclerotigenes and discuss how the microevolutionary patterns we uncover inform macroevolutionary inferences and help to align fungal secondary metabolism with existing evolutionary theory.

Published
2021

15. Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi

Author

Tatum R. Satterlee, Milton T. Drott, Paul E. Abraham, Richard J. Giannone, Jeffrey M. Skerker, N. Louise Glass, Tomás Allen Rush, Nancy P. Keller, Claudio Greco, Michael G. Milgroom, Jesse L. Labbé, and Nandhitha Venkatesh

Subjects
Comparative genomics, education.field_of_study, Multidisciplinary, Population, Niche, Microevolution, Biology, biology.organism_classification, Aspergillus parasiticus, Population genomics, Evolutionary biology, Adaptation, Secondary metabolism, education
Abstract

Fungi produce a wealth of pharmacologically bioactive secondary metabolites (SMs) from biosynthetic gene clusters (BGCs). It is common practice for drug discovery efforts to treat species' secondary metabolomes as being well represented by a single or a small number of representative genomes. However, this approach misses the possibility that intraspecific population dynamics, such as adaptation to environmental conditions or local microbiomes, may harbor novel BGCs that contribute to the overall niche breadth of species. Using 94 isolates of Aspergillus flavus, a cosmopolitan model fungus, sampled from seven states in the United States, we dereplicate 7,821 BGCs into 92 unique BGCs. We find that more than 25% of pangenomic BGCs show population-specific patterns of presence/absence or protein divergence. Population-specific BGCs make up most of the accessory-genome BGCs, suggesting that different ecological forces that maintain accessory genomes may be partially mediated by population-specific differences in secondary metabolism. We use ultra-high-performance high-resolution mass spectrometry to confirm that these genetic differences in BGCs also result in chemotypic differences in SM production in different populations, which could mediate ecological interactions and be acted on by selection. Thus, our results suggest a paradigm shift that previously unrealized population-level reservoirs of SM diversity may be of significant evolutionary, ecological, and pharmacological importance. Last, we find that several population-specific BGCs from A. flavus are present in Aspergillus parasiticus and Aspergillus minisclerotigenes and discuss how the microevolutionary patterns we uncover inform macroevolutionary inferences and help to align fungal secondary metabolism with existing evolutionary theory.

Published
2021

16. amPEPpy 1.0: a portable and accurate antimicrobial peptide prediction tool

Author

Jessy Labbé, Margaret K. Spangler, Stephen J. Minter, Travis J Lawrence, Tomás Allen Rush, David J. Weston, Dana L. Carper, and Alyssa A. Carrell

Subjects
Pore Forming Cytotoxic Proteins, Statistics and Probability, chemistry.chemical_classification, 0303 health sciences, Genome, Computer science, 0206 medical engineering, Antimicrobial peptides, Peptide, 02 engineering and technology, Computational biology, Antimicrobial, Biochemistry, Computer Science Applications, 03 medical and health sciences, Computational Mathematics, Computational Theory and Mathematics, chemistry, Molecular Biology, Software, 020602 bioinformatics, 030304 developmental biology
Abstract

Summary Antimicrobial peptides (AMPs) are promising alternative antimicrobial agents. Currently, however, portable, user-friendly and efficient methods for predicting AMP sequences from genome-scale data are not readily available. Here we present amPEPpy, an open-source, multi-threaded command-line application for predicting AMP sequences using a random forest classifier. Availability and implementation amPEPpy is implemented in Python 3 and is freely available through GitHub (https://github.com/tlawrence3/amPEPpy). Supplementary information Supplementary data are available at Bioinformatics online.

Published
2020
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17. Variation in the Internal Transcribed Spacer Region of

Author

Tomás Allen, Rush, Jacob, Golan, Alistair, McTaggart, Cade, Kane, R W, Schneider, and M Catherine, Aime

Subjects
Phakopsora pachyrhizi, Molecular Diagnostic Techniques, DNA, Ribosomal Spacer, Genetic Variation, Soybeans, Pathology, Molecular, United States, Plant Diseases
Published
2019

18. First Report of Puccinia thaliae Rust on Canna Lily in Louisiana

Author

R. Kaur, Tomás Allen Rush, M. C. Aime, and D. M. Ferrin

Subjects
Puccinia, education.school_district, biology, Host (biology), Canna, Plant Science, biology.organism_classification, Rust, East Baton Rouge Parish, Herbaceous perennial, Ornamental plant, Botany, education, Agronomy and Crop Science, Urediniospore
Abstract

Canna lily is a monocot, herbaceous perennial ornamental plant in the Cannaceae that is native to tropical South America and cultivated throughout the southern United States. Canna lily is a popular garden and landscaping plant and a large horticultural industry depends on this plant. In September 2008 and again in November 2009, two species of Canna lily (Canna × generalis L.H. Bailey and C. indica L.) were found to be severely infected with rust disease in three garden locations in southern Louisiana (East Baton Rouge Parish, Lafayette Parish, and Orleans Parish). Diseased samples from both host species and all locations exhibited similar symptoms of numerous, yellowish brown, subepidermal, erumpent, and irregular-shaped uredinia on both leaf surfaces. Initially, sori were scattered, later covering the entire leaf with coalescing pustules. Urediniospores were subglobose to ovoid or pyriform, echinulate, and measured 25.74 to 37.18 (–38.61) × 17.16 to 27.17 (–28.6) μm, with thickened apical walls, 1.3 to 1.6 μm, and one to two equatorial germ pores. Telia and teliospores were not observed on any of the collected samples. Pathogen identity was confirmed as Puccinia thaliae Dietel by nuclear ribosomal large subunit (28S) DNA sequencing with rust-specific primers (1). The sequence (deposited in GenBank as No. HQ434482), when blasted, was found to match sequence No. EU851154 of P. thaliae from C. indica with 98% identity (719 of 730 bp), the differences being attributed to a single insertion at bp 423 to 436 of sequence No. EU851154. The sequences of P. thaliae obtained from two different samples from Louisiana were identical and did not match any other sequence in GenBank. In North America P. thaliae is reported to cause rust on C. indica L. in Florida and C. × generalis in Texas, as well as on two members of the Marantaceae (Maranta arundinacea L. and Thalia geniculata L.) in Florida and M. arundinaceae in Mexico (2). To our knowledge, this is the first report of P. thaliae in Louisiana on Canna lily. Voucher materials (C. × generalis = LSU00123378 and C. indica = LSU00123384) have been deposited in the Bernard Lowy Mycological Herbarium (LSUM). References: (1) M. C. Aime. Mycoscience 47:112, 2006. (2) D. F. Farr and A.Y. Rossman. Fungal Databases. Systematic Mycology and Microbiology Laboratory, ARS, USDA. Retrieved 12 February from http://nt.ars-grin.gov/fungaldatabases/ , 2010.

Published
2019

19. The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots

Author

Nathaniel Schleif, Steven H. Strauss, Emmeline Fung, Sara S. Jawdy, Heike Bücking, Jessy Labbé, Edward Steigerwald, Fabienne Maillet, Tomás Allen Rush, Virginie Puech-Pagès, Kimberly G. Schnell, Kevin R. Cope, Muthusubramanian Venkateshwaran, Junko Maeda, Jean-Michel Ané, Cathleen Ma, Kevin Garcia, Guillaume Bécard, Jonathan Setzke, Patricia Jargeat, Yunqian Wang, Adeline Bascaules, Thomas B. Irving, University of Wisconsin-Madison, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Oregon State University (OSU), Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, South Dakota State University (SDSTATE), Laboratoire des interactions plantes micro-organismes (LIPM), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Evolution des Interactions Plantes-Microorganismes, Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), United States Department of Agriculture (USDA) : 2017-67014-26530 WIS01695, National Science Foundation (NSF) : DGE-1256259, United States Department of Energy (DOE) : DE-SC0018247, National Science Foundation (NSF) : 1546742, 1331098, Tree Genomics and Biosafety Cooperative at Oregon State University, NSF Center for Advanced Forestry Systems : 1238305, Plant-Microbe Interfaces Scientific Focus Area in the Genomic Science Program, Office of Biological and Environmental Research in the DOE, Office of Science, United States Department of Energy (DOE) : DE-AC05-00OR22725, ANR-14-CE18-0008,NICE CROPS,Bio-stimulateurs chitiniques naturels pour une agriculture durable(2014), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), ANR-11-INBS-0010,METABOHUB,Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation(2011), Erist, Montpellier, Appel à projets générique - Bio-stimulateurs chitiniques naturels pour une agriculture durable - - NICE CROPS2014 - ANR-14-CE18-0008 - Appel à projets générique - VALID, Towards a Unified theory of biotic Interactions: the roLe of environmental - - TULIP2010 - ANR-10-LABX-0041 - LABX - VALID, Développement d'une infrastructure française distribuée pour la métabolomique dédiée à l'innovation - - METABOHUB2011 - ANR-11-INBS-0010 - INBS - VALID, Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), and Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
0106 biological sciences, 0301 basic medicine, Lipopolysaccharides, MESH: Signal Transduction, [SDV]Life Sciences [q-bio], Plant Science, Fungus, Biology, Root hair, Photosynthesis, MESH: Plant Roots / microbiology, 01 natural sciences, MESH: Lipopolysaccharides / chemistry, [SDV.BV.BOT] Life Sciences [q-bio]/Vegetal Biology/Botanics, Laccaria, 03 medical and health sciences, Symbiosis, Laccaria bicolor, MESH: Calcium / metabolism, Mycorrhizae, Botany, MESH: Populus / metabolism, Colonization, MESH: Gene Expression Regulation, Plant, MESH: Mycorrhizae / physiology, Research Articles, [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Lateral root, fungi, Cell Biology, [SDV.EE.IEO] Life Sciences [q-bio]/Ecology, environment/Symbiosis, 15. Life on land, [SDV.BV.BOT]Life Sciences [q-bio]/Vegetal Biology/Botanics, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, MESH: Laccaria / metabolism, 030104 developmental biology, Populus, MESH: Symbiosis / physiology, Actinorhizal plant, 010606 plant biology & botany, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wildtype Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.

Published
2019
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20. The genus Meira: phylogenetic placement and description of a new species

Author

Tomás Allen Rush and M. Catherine Aime

Subjects
Molecular Sequence Data, DNA, Ribosomal, Microbiology, Exobasidiales, Phylogenetics, Genus, DNA, Ribosomal Spacer, Botany, RNA, Ribosomal, 18S, Cluster Analysis, DNA, Fungal, Mycological Typing Techniques, Molecular Biology, Phylogeny, Ustilaginomycotina, biology, Phylogenetic tree, Basidiomycota, Fungal genetics, Genes, rRNA, RNA, Fungal, Exobasidiomycetes, Sequence Analysis, DNA, General Medicine, biology.organism_classification, Incertae sedis, United States, Plant Leaves, Magnolia, RNA, Ribosomal, Evolutionary biology
Abstract

The genus Meira currently contains three recently described species of mite-associated basidiomycete yeasts from Israel and Japan and is placed in the Exobasidiomycetes (Ustilaginomycotina) Incertae sedis. A previously undescribed species of Meira was isolated from the phylloplane of a magnolia leaf in Louisiana, USA. Herein, we describe Meira miltonrushii sp. nov. and include phylogenetic analyses from three rDNA loci to resolve the placement of Meira. This study provides evidence that Meira belongs to the family Brachybasidiaceae in the Exobasidiales and supports the placement of another mite-associated yeast genus, Acaromyces, within Cryptobasidiaceae (Exobasidiales). We also examine sequences produced by numerous environmental studies that suggest Meira species can be found as endophytes of many plant species. To our knowledge, this is the first record of a member of the genus Meira in North America.

Published
2013
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