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Duke Herbarium Lichens: Publications since January 2018

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%% Lutzoni, Francois M.   
@article{fds346566,
   Author = {U'Ren, JM and Lutzoni, F and Miadlikowska, J and Zimmerman, NB and Carbone, I and May, G and Arnold, AE},
   Title = {Host availability drives distributions of fungal endophytes
             in the imperilled boreal realm.},
   Journal = {Nature Ecology and Evolution},
   Volume = {3},
   Number = {10},
   Pages = {1430-1437},
   Year = {2019},
   Month = {October},
   url = {http://dx.doi.org/10.1038/s41559-019-0975-2},
   Abstract = {Boreal forests represent the world's largest terrestrial
             biome and provide ecosystem services of global importance.
             Highly imperilled by climate change, these forests host
             Earth's greatest phylogenetic diversity of endophytes, a
             hyperdiverse group of symbionts that are defined by their
             occurrence within living, symptomless plant and lichen
             tissues. Endophytes shape the ecological and evolutionary
             trajectories of plants and are therefore key to the function
             and resilience of terrestrial ecosystems. A critical step in
             linking the ecological functions of endophytes with those of
             their hosts is to understand the distributions of these
             symbionts at the global scale; however, turnover in host
             taxa with geography and climate can confound insights into
             endophyte biogeography. As a result, global drivers of
             endophyte diversity and distributions are not known. Here,
             we leverage sampling from phylogenetically diverse boreal
             plants and lichens across North America and Eurasia to show
             that host filtering in distinctive environments, rather than
             turnover with geographical or environmental distance, is the
             main determinant of the community composition and diversity
             of endophytes. We reveal the distinctiveness of boreal
             endophytes relative to soil fungi worldwide and endophytes
             from diverse temperate biomes, highlighting a high degree of
             global endemism. Overall, the distributions of endophytes
             are directly linked to the availability of compatible hosts,
             highlighting the role of biotic interactions in shaping
             fungal communities across large spatial scales, and the
             threat that climate change poses to biological diversity and
             function in the imperilled boreal realm.},
   Doi = {10.1038/s41559-019-0975-2},
   Key = {fds346566}
}

@article{fds345375,
   Author = {Armaleo, D and Müller, O and Lutzoni, F and Andrésson, ÓS and Blanc,
             G and Bode, HB and Collart, FR and Dal Grande and F and Dietrich, F and Grigoriev, IV and Joneson, S and Kuo, A and Larsen, PE and Logsdon, JM and Lopez, D and Martin, F and May, SP and McDonald, TR and Merchant, SS and Miao, V and Morin, E and Oono, R and Pellegrini, M and Rubinstein, N and Sanchez-Puerta, MV and Savelkoul, E and Schmitt, I and Slot, JC and Soanes, D and Szövényi, P and Talbot, NJ and Veneault-Fourrey, C and Xavier, BB},
   Title = {The lichen symbiosis re-viewed through the genomes of
             Cladonia grayi and its algal partner Asterochloris
             glomerata.},
   Journal = {Bmc Genomics},
   Volume = {20},
   Number = {1},
   Pages = {605},
   Year = {2019},
   Month = {July},
   url = {http://dx.doi.org/10.1186/s12864-019-5629-x},
   Abstract = {BACKGROUND: Lichens, encompassing 20,000 known species, are
             symbioses between specialized fungi (mycobionts), mostly
             ascomycetes, and unicellular green algae or cyanobacteria
             (photobionts). Here we describe the first parallel genomic
             analysis of the mycobiont Cladonia grayi and of its green
             algal photobiont Asterochloris glomerata. We focus on
             genes/predicted proteins of potential symbiotic
             significance, sought by surveying proteins differentially
             activated during early stages of mycobiont and photobiont
             interaction in coculture, expanded or contracted protein
             families, and proteins with differential rates of evolution.
             RESULTS: A) In coculture, the fungus upregulated small
             secreted proteins, membrane transport proteins, signal
             transduction components, extracellular hydrolases and,
             notably, a ribitol transporter and an ammonium transporter,
             and the alga activated DNA metabolism, signal transduction,
             and expression of flagellar components. B) Expanded fungal
             protein families include heterokaryon incompatibility
             proteins, polyketide synthases, and a unique set of
             G-protein α subunit paralogs. Expanded algal protein
             families include carbohydrate active enzymes and a specific
             subclass of cytoplasmic carbonic anhydrases. The alga also
             appears to have acquired by horizontal gene transfer from
             prokaryotes novel archaeal ATPases and Desiccation-Related
             Proteins. Expanded in both symbionts are signal transduction
             components, ankyrin domain proteins and transcription
             factors involved in chromatin remodeling and stress
             responses. The fungal transportome is contracted, as are
             algal nitrate assimilation genes. C) In the mycobiont,
             slow-evolving proteins were enriched for components involved
             in protein translation, translocation and sorting.
             CONCLUSIONS: The surveyed genes affect stress resistance,
             signaling, genome reprogramming, nutritional and structural
             interactions. The alga carries many genes likely transferred
             horizontally through viruses, yet we found no evidence of
             inter-symbiont gene transfer. The presence in the photobiont
             of meiosis-specific genes supports the notion that sexual
             reproduction occurs in Asterochloris while they are
             free-living, a phenomenon with implications for the
             adaptability of lichens and the persistent autonomy of the
             symbionts. The diversity of the genes affecting the
             symbiosis suggests that lichens evolved by accretion of many
             scattered regulatory and structural changes rather than
             through introduction of a few key innovations. This predicts
             that paths to lichenization were variable in different
             phyla, which is consistent with the emerging consensus that
             ascolichens could have had a few independent
             origins.},
   Doi = {10.1186/s12864-019-5629-x},
   Key = {fds345375}
}

@article{fds345376,
   Author = {Carbone, I and White, JB and Miadlikowska, J and Arnold, AE and Miller,
             MA and Magain, N and U'Ren, JM and Lutzoni, F},
   Title = {T-BAS Version 2.1: Tree-Based Alignment Selector Toolkit for
             Evolutionary Placement of DNA Sequences and Viewing
             Alignments and Specimen Metadata on Curated and Custom
             Trees.},
   Journal = {Microbiology Resource Announcements},
   Volume = {8},
   Number = {29},
   Year = {2019},
   Month = {July},
   url = {http://dx.doi.org/10.1128/MRA.00328-19},
   Abstract = {The Tree-Based Alignment Selector (T-BAS) toolkit combines
             phylogenetic-based placement of DNA sequences with alignment
             and specimen metadata visualization tools in an integrative
             pipeline for analyzing microbial biodiversity. The release
             of T-BAS version 2.1 makes available reference phylogenies,
             supports multilocus sequence placements and permits
             uploading and downloading trees, alignments, and specimen
             metadata.},
   Doi = {10.1128/MRA.00328-19},
   Key = {fds345376}
}

@article{fds344727,
   Author = {Chagnon, PL and Magain, N and Miadlikowska, J and Lutzoni,
             F},
   Title = {Species diversification and phylogenetically constrained
             symbiont switching generated high modularity in the lichen
             genus Peltigera},
   Journal = {Journal of Ecology},
   Volume = {107},
   Number = {4},
   Pages = {1645-1661},
   Year = {2019},
   Month = {July},
   url = {http://dx.doi.org/10.1111/1365-2745.13207},
   Abstract = {© 2019 The Authors. Journal of Ecology © 2019 British
             Ecological Society Ecological interactions range from purely
             specialized to extremely generalized in nature. Recent
             research has showed very high levels of specialization in
             the cyanolichens involving Peltigera (mycobionts) and their
             Nostoc photosynthetic partners (cyanobionts). Yet, little is
             known about the mechanisms contributing to the establishment
             and maintenance of such high specialization levels. Here, we
             characterized interactions between Peltigera and Nostoc
             partners at a global scale, using more than one thousand
             thalli. We used tools from network theory, community
             phylogenetics and biogeographical history reconstruction to
             evaluate how these symbiotic interactions may have evolved.
             After splitting the interaction matrix into modules of
             preferentially interacting partners, we evaluated how module
             membership might have evolved along the mycobionts’
             phylogeny. We also teased apart the contributions of
             geographical overlap vs phylogeny in driving interaction
             establishment between Peltigera and Nostoc taxa. Module
             affiliation rarely evolves through the splitting of large
             ancestral modules. Instead, new modules appear to emerge
             independently, which is often associated with a fungal
             speciation event. We also found strong phylogenetic signal
             in these interactions, which suggests that partner switching
             is constrained by conserved traits. Therefore, it seems that
             a high rate of fungal diversification following a switch to
             a new cyanobiont can lead to the formation of large modules,
             with cyanobionts associating with multiple closely retated
             Peltigera species. Finally, when restricting our analyses to
             Peltigera sister species, the latter differed more through
             partner acquisition/loss than replacement (i.e., switching).
             This pattern vanishes as we look at sister species that have
             diverged longer ago. This suggests that fungal speciation
             may be accompanied by a stepwise process of (a) novel
             partner acquisition and (b) loss of the ancestral partner.
             This could explain the maintenance of high specialization
             levels in this symbiotic system where the transmission of
             the cyanobiont to the next generation is assumed to be
             predominantly horizontal. Synthesis. Overall, our study
             suggests that oscillation between generalization and
             ancestral partner loss may maintain high specialization
             within the lichen genus Peltigera, and that partner
             selection is not only driven by partners’ geographical
             overlap, but also by their phylogenetically conserved
             traits.},
   Doi = {10.1111/1365-2745.13207},
   Key = {fds344727}
}

@article{fds342447,
   Author = {Chen, K-H and Liao, H-L and Bellenger, J-P and Lutzoni,
             F},
   Title = {Differential gene expression associated with fungal trophic
             shifts along the senescence gradient of the moss Dicranum
             scoparium.},
   Journal = {Environmental Microbiology},
   Volume = {21},
   Number = {7},
   Pages = {2273-2289},
   Year = {2019},
   Month = {March},
   url = {http://dx.doi.org/10.1111/1462-2920.14605},
   Abstract = {Bryophytes harbour microbiomes, including diverse
             communities of fungi. The molecular mechanisms by which
             perennial mosses interact with these fungal partners along
             their senescence gradients are unknown, yet this is an ideal
             system to study variation in gene expression associated with
             trophic state transitions. We investigated differentially
             expressed genes of fungal communities and their host
             Dicranum scoparium across its naturally occurring senescence
             gradient using a metatranscriptomic approach. Higher
             activity of fungal nutrient-related (carbon, nitrogen,
             phosphorus and sulfur) transporters and Carbohydrate-Active
             enZyme (CAZy) genes was detected toward the bottom,
             partially decomposed, layer of the moss. The most prominent
             variation in the expression levels of fungal nutrient
             transporters was from inorganic nitrogen-related
             transporters, whereas the breakdown of organonitrogens was
             detected as the most enriched gene ontology term for the
             host D. scoparium, for those transcripts having higher
             expression in the partially decomposed layer. The abundance
             of bacterial rRNA transcripts suggested that more living
             members of Cyanobacteria are associated with the
             photosynthetic layer of D. scoparium, while members of
             Rhizobiales are detected throughout the gametophytes. Plant
             genes for specific fungal-plant communication, including
             defense responses, were differentially expressed, suggesting
             that different genetic pathways are involved in
             plant-microbe crosstalk in photosynthetic tissues compared
             to partially decomposed tissues.},
   Doi = {10.1111/1462-2920.14605},
   Key = {fds342447}
}

@article{fds340627,
   Author = {Lutzoni, F and Nowak, MD and Alfaro, ME and Reeb, V and Miadlikowska, J and Krug, M and Arnold, AE and Lewis, LA and Swofford, DL and Hibbett, D and Hilu, K and James, TY and Quandt, D and Magallón,
             S},
   Title = {Contemporaneous radiations of fungi and plants linked to
             symbiosis.},
   Journal = {Nature Communications},
   Volume = {9},
   Number = {1},
   Pages = {5451},
   Year = {2018},
   Month = {December},
   url = {http://dx.doi.org/10.1038/s41467-018-07849-9},
   Abstract = {Interactions between fungi and plants, including parasitism,
             mutualism, and saprotrophy, have been invoked as key to
             their respective macroevolutionary success. Here we evaluate
             the origins of plant-fungal symbioses and saprotrophy using
             a time-calibrated phylogenetic framework that reveals linked
             and drastic shifts in diversification rates of each kingdom.
             Fungal colonization of land was associated with at least two
             origins of terrestrial green algae and preceded embryophytes
             (as evidenced by losses of fungal flagellum, ca. 720 Ma),
             likely facilitating terrestriality through endomycorrhizal
             and possibly endophytic symbioses. The largest radiation of
             fungi (Leotiomyceta), the origin of arbuscular mycorrhizae,
             and the diversification of extant embryophytes occurred ca.
             480 Ma. This was followed by the origin of extant lichens.
             Saprotrophic mushrooms diversified in the Late Paleozoic as
             forests of seed plants started to dominate the landscape.
             The subsequent diversification and explosive radiation of
             Agaricomycetes, and eventually of ectomycorrhizal mushrooms,
             were associated with the evolution of Pinaceae in the
             Mesozoic, and establishment of angiosperm-dominated biomes
             in the Cretaceous.},
   Doi = {10.1038/s41467-018-07849-9},
   Key = {fds340627}
}

@article{fds340995,
   Author = {Miadlikowska, J and Magain, N and Pardo-De La Hoz and CJ and Niu, D and Goward, T and Sérusiaux, E and Lutzoni, F},
   Title = {Species in section Peltidea (aphthosa group) of the genus
             Peltigera remain cryptic after molecular phylogenetic
             revision},
   Journal = {Plant and Fungal Systematics},
   Volume = {63},
   Number = {2},
   Pages = {45-64},
   Year = {2018},
   Month = {December},
   url = {http://dx.doi.org/10.2478/pfs-2018-0007},
   Abstract = {© 2018 Jolanta Miadlikowska et al., published by Sciendo
             2018. Closely related lichen-forming fungal species
             circumscribed using phenotypic traits (morphospecies) do not
             always align well with phylogenetic inferences based on
             molecular data. Using multilocus data obtained from a
             worldwide sampling, we inferred phylogenetic relationships
             among five currently accepted morphospecies of Peltigera
             section Peltidea (P. aphthosa group). Monophyletic
             circumscription of all currently recognized morphospecies
             (P. britannica, P. chionophila, P. frippii and P. malacea)
             except P. aphthosa, which contained P. britannica, was
             confirmed with high bootstrap support. Following their
             re-delimitation using bGMYC and Structurama, BPP validated
             14 putative species including nine previously unrecognized
             potential species (five within P. malacea, five within P.
             aphthosa, and two within P. britannica). Because none of the
             undescribed potential species are corroborated
             morphologically, chemically, geographically or ecologically,
             we concluded that these monophyletic entities represent
             intraspecific phylogenetic structure, and, therefore, should
             not be recognized as new species. Cyanobionts associated
             with Peltidea mycobionts (51 individuals) represented 22
             unique rbcLX haplotypes from five phylogroups in Clade II
             subclades 2 and 3. With rare exceptions, Nostoc taxa
             involved in trimembered and bimembered associations are
             phylogenetically closely related (subclade 2) or identical,
             suggesting a mostly shared cyanobiont pool with infrequent
             switches. Based on a broad geographical sampling, we confirm
             a high specificity of Nostoc subclade 2 with their
             mycobionts, including a mutualistically exclusive
             association between phylogroup III and specific lineages of
             P. malacea.},
   Doi = {10.2478/pfs-2018-0007},
   Key = {fds340995}
}

@article{fds339810,
   Author = {Hoz, CJPDL and Magain, N and Lutzoni, F and Goward, T and Restrepo, S and Miadlikowska, J},
   Title = {Contrasting Symbiotic Patterns in Two Closely Related
             Lineages of Trimembered Lichens of the Genus
             Peltigera},
   Journal = {Frontiers in Microbiology},
   Volume = {9},
   Number = {NOV},
   Publisher = {FRONTIERS MEDIA SA},
   Year = {2018},
   Month = {November},
   url = {http://dx.doi.org/10.3389/fmicb.2018.02770},
   Abstract = {© 2018 Pardo-De la Hoz, Magain, Lutzoni, Goward, Restrepo
             and Miadlikowska. Species circumscription is key to the
             characterization of patterns of specificity in symbiotic
             systems at a macroevolutionary scale. Here, a worldwide
             phylogenetic framework was used to assess the biodiversity
             and symbiotic patterns of association among partners in
             trimembered lichens from the genus Peltigera, section
             Chloropeltigera. We sequenced six loci of the main fungal
             partner and performed species discovery and validation
             analyses to establish putative species boundaries. Single
             locus phylogenies were used to establish the identity of
             both photobionts, Nostoc (cyanobacterium) and Coccomyxa
             (green alga). Distribution and specificity patterns were
             compared to the closely related clade, section Peltidea,
             which includes mainly Peltigera species with trimembered
             thalli. For section Chloropeltigera, eight fungal species
             (including five newly delimited putative species) were found
             in association with nine Nostoc phylogroups and two
             Coccomyxa species. In contrast, eight fungal species
             (including three newly delimited putative species) in
             section Peltidea were found in association with only four
             Nostoc phylogroups and the same two Coccomyxa species as for
             section Chloropeltigera. This difference in cyanobiont
             biodiversity between these two sections can potentially be
             explained by a significantly higher frequency of sexual
             reproductive structures in species from section
             Chloropeltigera compared to section Peltidea. Therefore,
             horizontal transmission of the cyanobiont might be more
             prevalent in Chloropeltigera species, while vertical
             transmission might be more common in Peltidea species. All
             Peltigera species in section Chloropeltigera are generalists
             in their association with Nostoc compared to more
             specialized Peltigera species in section Peltidea.
             Constrained distributions of Peltigera species that
             associate strictly with one species of green algae
             (Coccomyxa subellipsoidea) indicate that the availability of
             the green alga and the specificity of the interaction might
             be important factors limiting geographic ranges of
             trimembered Peltigera, in addition to constraints imposed by
             their interaction with Nostoc partners and by climatic
             factors.},
   Doi = {10.3389/fmicb.2018.02770},
   Key = {fds339810}
}

@article{fds339561,
   Author = {Korotkin, HB and Swenie, RA and Miettinen, O and Budke, JM and Chen,
             K-H and Lutzoni, F and Smith, ME and Matheny, PB},
   Title = {Stable isotope analyses reveal previously unknown trophic
             mode diversity in the Hymenochaetales.},
   Journal = {American Journal of Botany},
   Volume = {105},
   Number = {11},
   Pages = {1869-1887},
   Year = {2018},
   Month = {November},
   url = {http://dx.doi.org/10.1002/ajb2.1183},
   Abstract = {PREMISE OF THE STUDY:The Hymenochaetales are dominated by
             lignicolous saprotrophic fungi involved in wood decay.
             However, the group also includes bryophilous and terricolous
             taxa, but their modes of nutrition are not clear. Here, we
             investigate patterns of carbon and nitrogen utilization in
             numerous non-lignicolous Hymenochaetales and provide a
             phylogenetic context in which these non-canonical ecological
             guilds arose. METHODS:We combined stable isotope analyses of
             δ13 C and δ15 N and phylogenetic analyses to explore
             assignment and evolution of nutritional modes. Clustering
             procedures and statistical tests were performed to assign
             trophic modes to Hymenochaetales and test for differences
             between varying ecologies. Genomes of Hymenochaetales were
             mined for presence of enzymes involved in plant cell wall
             and lignin degradation and sucrolytic activity. KEY
             RESULTS:Three different trophic clusters were detected -
             biotrophic, saprotrophic, and a second biotrophic cluster
             including many bryophilous Hymenochaetales and mosses.
             Non-lignicolous Hymenochaetales are generally biotrophic.
             All lignicolous Hymenochaetales clustered as saprotrophic
             and most terricolous Hymenochaetales clustered as
             ectomycorrhizal. Overall, at least 15 species of
             Hymenochaetales are inferred as biotrophic. Bryophilous
             species of Rickenella can degrade plant cell walls and
             lignin, and cleave sucrose to glucose consistent with a
             parasitic or endophytic life style. CONCLUSIONS:Most
             non-lignicolous Hymenochaetales are biotrophic. Stable
             isotope values of many bryophilous Hymenochaetales cluster
             as ectomycorrhizal or in a biotrophic cluster indicative of
             parasitism or an endophytic life style. Overall, trophic
             mode diversity in the Hymenochaetales is greater than
             anticipated, and non-lignicolous ecological traits and
             biotrophic modes of nutrition are evolutionarily derived
             features.},
   Doi = {10.1002/ajb2.1183},
   Key = {fds339561}
}

@article{fds339618,
   Author = {Magain, N and Truong, C and Goward, T and Niu, D and Goffinet, B and Sérusiaux, E and Vitikainen, O and Lutzoni, F and Miadlikowska,
             J},
   Title = {Species delimitation at a global scale reveals high species
             richness with complex biogeography and patterns of symbiont
             association in peltigera section peltigera (Lichenized
             ascomycota: Lecanoromycetes)},
   Journal = {Taxon},
   Volume = {67},
   Number = {5},
   Pages = {836-870},
   Publisher = {WILEY},
   Year = {2018},
   Month = {October},
   url = {http://dx.doi.org/10.12705/675.3},
   Abstract = {© International Association for Plant Taxonomy (IAPT) 2018,
             all rights reserved. This comprehensive phylogenetic
             revision of sections Peltigera and Retifoveatae of the
             cyanolichen genus Peltigera is based on DNA sequences from
             more than 500 specimens from five continents. We amplified
             five loci (nrITS, β-tubulin and three intergenic spacers
             part of colinear orthologous regions [COR]) for the
             mycobiont, and the rbcLX locus for the cyanobacterial
             partner Nostoc. Phylogenetic inferences (RAxML, BEAST) and
             species delimitation methods (bGMYC, bPTP, bPP) suggest the
             presence of 88 species in section Peltigera, including 50
             species new to science, hence uncovering a surprisingly high
             proportion of previously unnoticed biodiversity. The
             hypervariable region in ITS1 (ITS1-HR) is a powerful marker
             to identify species within sections Peltigera and
             Retifoveatae. Most newly delimited species are restricted to
             a single biogeographic region, however, up to ten species
             have a nearly cosmopolitan distribution. The specificity of
             mycobionts in their association with Nostoc cyanobionts
             ranges from strict specialists (associate with only one
             Nostoc phylogroup) to broad generalists (up to eight Nostoc
             phylogroups uncovered), with widespread species recruiting a
             broader selection of Nostoc phylogroups than species with
             limited distributions. In contrast, species from the P.
             didactyla clade characterized by small thalli and asexual
             vegetative propagules (soredia) associate with fewer Nostoc
             phylogroups (i.e., are more specialized) despite their broad
             distributions, and show significantly higher rates of
             nucleotide substitutions.},
   Doi = {10.12705/675.3},
   Key = {fds339618}
}

@article{fds336998,
   Author = {Lu, J and Magain, N and Miadlikowska, J and Coyle, JR and Truong, C and Lutzoni, F},
   Title = {Bioclimatic factors at an intrabiome scale are more limiting
             than cyanobiont availability for the lichen-forming genus
             Peltigera.},
   Journal = {American Journal of Botany},
   Volume = {105},
   Number = {7},
   Pages = {1198-1211},
   Year = {2018},
   Month = {July},
   url = {http://dx.doi.org/10.1002/ajb2.1119},
   Abstract = {PREMISE OF THE STUDY:Factors shaping spatiotemporal patterns
             of associations in mutualistic systems are poorly
             understood. We used the lichen-forming fungi Peltigera and
             their cyanobacterial partners Nostoc to investigate the
             spatial structure of this symbiosis at an intrabiome scale
             and to identify potential factors shaping these
             associations. METHODS:Ninety-three thalli were sampled in
             Québec, Canada, along a south-north and an east-west
             transect of ~1300 km each. We identified the two main
             partners (Peltigera species and Nostoc phylogroups) using
             molecular markers and modeled the effects of environmental
             variables and partner occurrence on Peltigera-Nostoc
             distributions. KEY RESULTS:Peltigera species showed a high
             degree of specialization toward cyanobionts, whereas two
             Nostoc phylogroups dominated both transects by associating
             with several Peltigera species. Peltigera species had
             narrower ranges than these two main cyanobionts.
             Distributions of three Peltigera species were highly
             associated with precipitation and temperature variables,
             which was not detected for Nostoc phylogroups at this
             spatial scale. CONCLUSIONS:For these cyanolichens, factors
             driving patterns of symbiotic associations are scale
             dependent. Contrary to global-scale findings, generalist
             Peltigera species were not more widespread within the boreal
             biome than specialists. Nostoc availability was not the only
             driver of Peltigera species' geographic ranges;
             environmental factors also contributed to their intrabiome
             distributions. Climatic conditions (especially
             precipitation) limited the range of some Peltigera species
             more than the range of their cyanobacterial partners at an
             intrabiome (boreal) scale.},
   Doi = {10.1002/ajb2.1119},
   Key = {fds336998}
}

@article{fds336262,
   Author = {Chagnon, PL and Magain, N and Miadlikowska, J and Lutzoni,
             F},
   Title = {Strong specificity and network modularity at a very fine
             phylogenetic scale in the lichen genus Peltigera.},
   Journal = {Oecologia},
   Volume = {187},
   Number = {3},
   Pages = {767-782},
   Publisher = {Springer Nature},
   Year = {2018},
   Month = {July},
   url = {http://dx.doi.org/10.1007/s00442-018-4159-6},
   Abstract = {Identifying the drivers and evolutionary consequences of
             species interactions is a major goal of community ecology.
             Network-based analyses can provide mathematical tools to
             detect non-random patterns of interactions, and potentially
             help predicting the consequences of such patterns on
             evolutionary dynamics of symbiotic systems. Here, we
             characterize the structure of a lichen network at a very
             fine phylogenetic scale, by identifying the photosynthetic
             partners (i.e., cyanobacteria of the genus Nostoc) of
             lichenized fungi belonging to a monophyletic section of a
             single genus (i.e., section Polydactylon of the genus
             Peltigera), worldwide. Even at such a fine phylogenetic
             scale, we found that interactions were highly modular and
             anti-nested, indicating strong preferences in interactions.
             When considering local Peltigera communities, i.e., datasets
             at small spatial scales with only a slightly broader
             phylogenetic range, interactions remained modular but were
             asymmetric, with generalist Nostoc partners interacting with
             specialized Peltigera species. This asymmetry was not
             detected with our global spatial scale dataset. We discuss
             these results in the light of lichen community assembly, and
             explore how such interaction patterns may influence
             coevolution in lichens and the evolutionary stability of the
             mutualism in general.},
   Doi = {10.1007/s00442-018-4159-6},
   Key = {fds336262}
}

@article{fds335251,
   Author = {Chen, K-H and Liao, H-L and Arnold, AE and Bonito, G and Lutzoni,
             F},
   Title = {RNA-based analyses reveal fungal communities structured by a
             senescence gradient in the moss Dicranum scoparium and the
             presence of putative multi-trophic fungi.},
   Journal = {The New Phytologist},
   Volume = {218},
   Number = {4},
   Pages = {1597-1611},
   Publisher = {WILEY},
   Year = {2018},
   Month = {June},
   url = {http://dx.doi.org/10.1111/nph.15092},
   Abstract = {Diverse plant-associated fungi are thought to have
             symbiotrophic and saprotrophic states because they can be
             isolated from both dead and living plant tissues. However,
             such tissues often are separated in time and space, and
             fungal activity at various stages of plant senescence is
             rarely assessed directly in fungal community studies. We
             used fungal ribosomal RNA metatranscriptomics to detect
             active fungal communities across a natural senescence
             gradient within wild-collected gametophytes of Dicranum
             scoparium (Bryophyta) to understand the distribution of
             active fungal communities in adjacent living, senescing and
             dead tissues. Ascomycota were active in all tissues across
             the senescence gradient. By contrast, Basidiomycota were
             prevalent and active in senescing and dead tissues. Several
             fungi were detected as active in living and dead tissues,
             suggesting their capacity for multi-trophy. Differences in
             community assembly detected by metatranscriptomics were
             echoed by amplicon sequencing of cDNA and compared to
             culture-based inferences and observation of fungal fruit
             bodies in the field. The combination of amplicon sequencing
             of cDNA and metatranscriptomics is promising for studying
             symbiotic systems with complex microbial diversity, allowing
             for the simultaneous detection of their presence and
             activity.},
   Doi = {10.1111/nph.15092},
   Key = {fds335251}
}

@article{fds335252,
   Author = {Kauff, F and Bachran, A and Schultz, M and Hofstetter, V and Lutzoni, F and Büdel, B},
   Title = {Molecular data favours a monogeneric Peltulaceae
             (Lichinomycetes)},
   Journal = {Lichenologist},
   Volume = {50},
   Number = {3},
   Pages = {313-327},
   Publisher = {Cambridge University Press (CUP)},
   Year = {2018},
   Month = {May},
   url = {http://dx.doi.org/10.1017/S0024282918000105},
   Abstract = {© British Lichen Society, 2018. The family Peltulaceae is
             currently composed of the three genera Peltula,
             Phyllopeltula and Neoheppia. The last two genera, both with
             two species, are distinguished from Peltula only by a small
             number of morphological characters. The morphology of the
             genus Peltula varies from peltate-umbilicate thalli to
             squamulose-semifruticose or squamulose-compound types, as
             well as subfoliose-compound and crustose types. All types
             have an upper epinecral layer and possess medullary cavities
             of various sizes; a lower cortex is normally present but is
             usually not developed in the subfoliose and crustose types.
             The genera Neoheppia and Phyllopeltula differ from the
             common Peltula morphology by crustose-areolate and
             subfoliose-compound thalli, respectively. Both Neoheppia and
             Phyllopeltula are additionally characterized by the absence
             of medullary cavities and lower cortices. To investigate the
             phylogenetic validity of Phyllopeltula and Neoheppia, we
             sequenced six loci from representatives of these two genera
             together with 37 species from Peltula. Despite the
             relatively high amount of conflict among loci, the results
             clearly indicate that both Phyllopeltula and Neoheppia are
             not monophyletic, and are nested within the genus Peltula.
             Consequently, we subsumed species of these two genera within
             the genus Peltula.},
   Doi = {10.1017/S0024282918000105},
   Key = {fds335252}
}


%% Miadlikowska, Jolanta M.   
@article{fds346584,
   Author = {U'Ren, JM and Lutzoni, F and Miadlikowska, J and Zimmerman, NB and Carbone, I and May, G and Arnold, AE},
   Title = {Host availability drives distributions of fungal endophytes
             in the imperilled boreal realm.},
   Journal = {Nature Ecology and Evolution},
   Volume = {3},
   Number = {10},
   Pages = {1430-1437},
   Year = {2019},
   Month = {October},
   url = {http://dx.doi.org/10.1038/s41559-019-0975-2},
   Abstract = {Boreal forests represent the world's largest terrestrial
             biome and provide ecosystem services of global importance.
             Highly imperilled by climate change, these forests host
             Earth's greatest phylogenetic diversity of endophytes, a
             hyperdiverse group of symbionts that are defined by their
             occurrence within living, symptomless plant and lichen
             tissues. Endophytes shape the ecological and evolutionary
             trajectories of plants and are therefore key to the function
             and resilience of terrestrial ecosystems. A critical step in
             linking the ecological functions of endophytes with those of
             their hosts is to understand the distributions of these
             symbionts at the global scale; however, turnover in host
             taxa with geography and climate can confound insights into
             endophyte biogeography. As a result, global drivers of
             endophyte diversity and distributions are not known. Here,
             we leverage sampling from phylogenetically diverse boreal
             plants and lichens across North America and Eurasia to show
             that host filtering in distinctive environments, rather than
             turnover with geographical or environmental distance, is the
             main determinant of the community composition and diversity
             of endophytes. We reveal the distinctiveness of boreal
             endophytes relative to soil fungi worldwide and endophytes
             from diverse temperate biomes, highlighting a high degree of
             global endemism. Overall, the distributions of endophytes
             are directly linked to the availability of compatible hosts,
             highlighting the role of biotic interactions in shaping
             fungal communities across large spatial scales, and the
             threat that climate change poses to biological diversity and
             function in the imperilled boreal realm.},
   Doi = {10.1038/s41559-019-0975-2},
   Key = {fds346584}
}

@article{fds345378,
   Author = {Carbone, I and White, JB and Miadlikowska, J and Arnold, AE and Miller,
             MA and Magain, N and U'Ren, JM and Lutzoni, F},
   Title = {T-BAS Version 2.1: Tree-Based Alignment Selector Toolkit for
             Evolutionary Placement of DNA Sequences and Viewing
             Alignments and Specimen Metadata on Curated and Custom
             Trees.},
   Journal = {Microbiology Resource Announcements},
   Volume = {8},
   Number = {29},
   Year = {2019},
   Month = {July},
   url = {http://dx.doi.org/10.1128/MRA.00328-19},
   Abstract = {The Tree-Based Alignment Selector (T-BAS) toolkit combines
             phylogenetic-based placement of DNA sequences with alignment
             and specimen metadata visualization tools in an integrative
             pipeline for analyzing microbial biodiversity. The release
             of T-BAS version 2.1 makes available reference phylogenies,
             supports multilocus sequence placements and permits
             uploading and downloading trees, alignments, and specimen
             metadata.},
   Doi = {10.1128/MRA.00328-19},
   Key = {fds345378}
}

@article{fds344599,
   Author = {Chagnon, PL and Magain, N and Miadlikowska, J and Lutzoni,
             F},
   Title = {Species diversification and phylogenetically constrained
             symbiont switching generated high modularity in the lichen
             genus Peltigera},
   Journal = {Journal of Ecology},
   Volume = {107},
   Number = {4},
   Pages = {1645-1661},
   Year = {2019},
   Month = {July},
   url = {http://dx.doi.org/10.1111/1365-2745.13207},
   Abstract = {© 2019 The Authors. Journal of Ecology © 2019 British
             Ecological Society Ecological interactions range from purely
             specialized to extremely generalized in nature. Recent
             research has showed very high levels of specialization in
             the cyanolichens involving Peltigera (mycobionts) and their
             Nostoc photosynthetic partners (cyanobionts). Yet, little is
             known about the mechanisms contributing to the establishment
             and maintenance of such high specialization levels. Here, we
             characterized interactions between Peltigera and Nostoc
             partners at a global scale, using more than one thousand
             thalli. We used tools from network theory, community
             phylogenetics and biogeographical history reconstruction to
             evaluate how these symbiotic interactions may have evolved.
             After splitting the interaction matrix into modules of
             preferentially interacting partners, we evaluated how module
             membership might have evolved along the mycobionts’
             phylogeny. We also teased apart the contributions of
             geographical overlap vs phylogeny in driving interaction
             establishment between Peltigera and Nostoc taxa. Module
             affiliation rarely evolves through the splitting of large
             ancestral modules. Instead, new modules appear to emerge
             independently, which is often associated with a fungal
             speciation event. We also found strong phylogenetic signal
             in these interactions, which suggests that partner switching
             is constrained by conserved traits. Therefore, it seems that
             a high rate of fungal diversification following a switch to
             a new cyanobiont can lead to the formation of large modules,
             with cyanobionts associating with multiple closely retated
             Peltigera species. Finally, when restricting our analyses to
             Peltigera sister species, the latter differed more through
             partner acquisition/loss than replacement (i.e., switching).
             This pattern vanishes as we look at sister species that have
             diverged longer ago. This suggests that fungal speciation
             may be accompanied by a stepwise process of (a) novel
             partner acquisition and (b) loss of the ancestral partner.
             This could explain the maintenance of high specialization
             levels in this symbiotic system where the transmission of
             the cyanobiont to the next generation is assumed to be
             predominantly horizontal. Synthesis. Overall, our study
             suggests that oscillation between generalization and
             ancestral partner loss may maintain high specialization
             within the lichen genus Peltigera, and that partner
             selection is not only driven by partners’ geographical
             overlap, but also by their phylogenetically conserved
             traits.},
   Doi = {10.1111/1365-2745.13207},
   Key = {fds344599}
}

@article{fds340628,
   Author = {Lutzoni, F and Nowak, MD and Alfaro, ME and Reeb, V and Miadlikowska, J and Krug, M and Arnold, AE and Lewis, LA and Swofford, DL and Hibbett, D and Hilu, K and James, TY and Quandt, D and Magallón,
             S},
   Title = {Contemporaneous radiations of fungi and plants linked to
             symbiosis.},
   Journal = {Nature Communications},
   Volume = {9},
   Number = {1},
   Pages = {5451},
   Year = {2018},
   Month = {December},
   url = {http://dx.doi.org/10.1038/s41467-018-07849-9},
   Abstract = {Interactions between fungi and plants, including parasitism,
             mutualism, and saprotrophy, have been invoked as key to
             their respective macroevolutionary success. Here we evaluate
             the origins of plant-fungal symbioses and saprotrophy using
             a time-calibrated phylogenetic framework that reveals linked
             and drastic shifts in diversification rates of each kingdom.
             Fungal colonization of land was associated with at least two
             origins of terrestrial green algae and preceded embryophytes
             (as evidenced by losses of fungal flagellum, ca. 720 Ma),
             likely facilitating terrestriality through endomycorrhizal
             and possibly endophytic symbioses. The largest radiation of
             fungi (Leotiomyceta), the origin of arbuscular mycorrhizae,
             and the diversification of extant embryophytes occurred ca.
             480 Ma. This was followed by the origin of extant lichens.
             Saprotrophic mushrooms diversified in the Late Paleozoic as
             forests of seed plants started to dominate the landscape.
             The subsequent diversification and explosive radiation of
             Agaricomycetes, and eventually of ectomycorrhizal mushrooms,
             were associated with the evolution of Pinaceae in the
             Mesozoic, and establishment of angiosperm-dominated biomes
             in the Cretaceous.},
   Doi = {10.1038/s41467-018-07849-9},
   Key = {fds340628}
}

@article{fds340996,
   Author = {Miadlikowska, J and Magain, N and Pardo-De La Hoz and CJ and Niu, D and Goward, T and Sérusiaux, E and Lutzoni, F},
   Title = {Species in section Peltidea (aphthosa group) of the genus
             Peltigera remain cryptic after molecular phylogenetic
             revision},
   Journal = {Plant and Fungal Systematics},
   Volume = {63},
   Number = {2},
   Pages = {45-64},
   Year = {2018},
   Month = {December},
   url = {http://dx.doi.org/10.2478/pfs-2018-0007},
   Abstract = {© 2018 Jolanta Miadlikowska et al., published by Sciendo
             2018. Closely related lichen-forming fungal species
             circumscribed using phenotypic traits (morphospecies) do not
             always align well with phylogenetic inferences based on
             molecular data. Using multilocus data obtained from a
             worldwide sampling, we inferred phylogenetic relationships
             among five currently accepted morphospecies of Peltigera
             section Peltidea (P. aphthosa group). Monophyletic
             circumscription of all currently recognized morphospecies
             (P. britannica, P. chionophila, P. frippii and P. malacea)
             except P. aphthosa, which contained P. britannica, was
             confirmed with high bootstrap support. Following their
             re-delimitation using bGMYC and Structurama, BPP validated
             14 putative species including nine previously unrecognized
             potential species (five within P. malacea, five within P.
             aphthosa, and two within P. britannica). Because none of the
             undescribed potential species are corroborated
             morphologically, chemically, geographically or ecologically,
             we concluded that these monophyletic entities represent
             intraspecific phylogenetic structure, and, therefore, should
             not be recognized as new species. Cyanobionts associated
             with Peltidea mycobionts (51 individuals) represented 22
             unique rbcLX haplotypes from five phylogroups in Clade II
             subclades 2 and 3. With rare exceptions, Nostoc taxa
             involved in trimembered and bimembered associations are
             phylogenetically closely related (subclade 2) or identical,
             suggesting a mostly shared cyanobiont pool with infrequent
             switches. Based on a broad geographical sampling, we confirm
             a high specificity of Nostoc subclade 2 with their
             mycobionts, including a mutualistically exclusive
             association between phylogroup III and specific lineages of
             P. malacea.},
   Doi = {10.2478/pfs-2018-0007},
   Key = {fds340996}
}

@article{fds339811,
   Author = {Hoz, CJPDL and Magain, N and Lutzoni, F and Goward, T and Restrepo, S and Miadlikowska, J},
   Title = {Contrasting Symbiotic Patterns in Two Closely Related
             Lineages of Trimembered Lichens of the Genus
             Peltigera},
   Journal = {Frontiers in Microbiology},
   Volume = {9},
   Number = {NOV},
   Publisher = {FRONTIERS MEDIA SA},
   Year = {2018},
   Month = {November},
   url = {http://dx.doi.org/10.3389/fmicb.2018.02770},
   Abstract = {© 2018 Pardo-De la Hoz, Magain, Lutzoni, Goward, Restrepo
             and Miadlikowska. Species circumscription is key to the
             characterization of patterns of specificity in symbiotic
             systems at a macroevolutionary scale. Here, a worldwide
             phylogenetic framework was used to assess the biodiversity
             and symbiotic patterns of association among partners in
             trimembered lichens from the genus Peltigera, section
             Chloropeltigera. We sequenced six loci of the main fungal
             partner and performed species discovery and validation
             analyses to establish putative species boundaries. Single
             locus phylogenies were used to establish the identity of
             both photobionts, Nostoc (cyanobacterium) and Coccomyxa
             (green alga). Distribution and specificity patterns were
             compared to the closely related clade, section Peltidea,
             which includes mainly Peltigera species with trimembered
             thalli. For section Chloropeltigera, eight fungal species
             (including five newly delimited putative species) were found
             in association with nine Nostoc phylogroups and two
             Coccomyxa species. In contrast, eight fungal species
             (including three newly delimited putative species) in
             section Peltidea were found in association with only four
             Nostoc phylogroups and the same two Coccomyxa species as for
             section Chloropeltigera. This difference in cyanobiont
             biodiversity between these two sections can potentially be
             explained by a significantly higher frequency of sexual
             reproductive structures in species from section
             Chloropeltigera compared to section Peltidea. Therefore,
             horizontal transmission of the cyanobiont might be more
             prevalent in Chloropeltigera species, while vertical
             transmission might be more common in Peltidea species. All
             Peltigera species in section Chloropeltigera are generalists
             in their association with Nostoc compared to more
             specialized Peltigera species in section Peltidea.
             Constrained distributions of Peltigera species that
             associate strictly with one species of green algae
             (Coccomyxa subellipsoidea) indicate that the availability of
             the green alga and the specificity of the interaction might
             be important factors limiting geographic ranges of
             trimembered Peltigera, in addition to constraints imposed by
             their interaction with Nostoc partners and by climatic
             factors.},
   Doi = {10.3389/fmicb.2018.02770},
   Key = {fds339811}
}

@article{fds339620,
   Author = {Magain, N and Truong, C and Goward, T and Niu, D and Goffinet, B and Sérusiaux, E and Vitikainen, O and Lutzoni, F and Miadlikowska,
             J},
   Title = {Species delimitation at a global scale reveals high species
             richness with complex biogeography and patterns of symbiont
             association in peltigera section peltigera (Lichenized
             ascomycota: Lecanoromycetes)},
   Journal = {Taxon},
   Volume = {67},
   Number = {5},
   Pages = {836-870},
   Publisher = {WILEY},
   Year = {2018},
   Month = {October},
   url = {http://dx.doi.org/10.12705/675.3},
   Abstract = {© International Association for Plant Taxonomy (IAPT) 2018,
             all rights reserved. This comprehensive phylogenetic
             revision of sections Peltigera and Retifoveatae of the
             cyanolichen genus Peltigera is based on DNA sequences from
             more than 500 specimens from five continents. We amplified
             five loci (nrITS, β-tubulin and three intergenic spacers
             part of colinear orthologous regions [COR]) for the
             mycobiont, and the rbcLX locus for the cyanobacterial
             partner Nostoc. Phylogenetic inferences (RAxML, BEAST) and
             species delimitation methods (bGMYC, bPTP, bPP) suggest the
             presence of 88 species in section Peltigera, including 50
             species new to science, hence uncovering a surprisingly high
             proportion of previously unnoticed biodiversity. The
             hypervariable region in ITS1 (ITS1-HR) is a powerful marker
             to identify species within sections Peltigera and
             Retifoveatae. Most newly delimited species are restricted to
             a single biogeographic region, however, up to ten species
             have a nearly cosmopolitan distribution. The specificity of
             mycobionts in their association with Nostoc cyanobionts
             ranges from strict specialists (associate with only one
             Nostoc phylogroup) to broad generalists (up to eight Nostoc
             phylogroups uncovered), with widespread species recruiting a
             broader selection of Nostoc phylogroups than species with
             limited distributions. In contrast, species from the P.
             didactyla clade characterized by small thalli and asexual
             vegetative propagules (soredia) associate with fewer Nostoc
             phylogroups (i.e., are more specialized) despite their broad
             distributions, and show significantly higher rates of
             nucleotide substitutions.},
   Doi = {10.12705/675.3},
   Key = {fds339620}
}

@article{fds337995,
   Author = {Lu, J and Magain, N and Miadlikowska, J and Coyle, JR and Truong, C and Lutzoni, F},
   Title = {Bioclimatic factors at an intrabiome scale are more limiting
             than cyanobiont availability for the lichen-forming genus
             Peltigera.},
   Journal = {American Journal of Botany},
   Volume = {105},
   Number = {7},
   Pages = {1198-1211},
   Year = {2018},
   Month = {July},
   url = {http://dx.doi.org/10.1002/ajb2.1119},
   Abstract = {PREMISE OF THE STUDY:Factors shaping spatiotemporal patterns
             of associations in mutualistic systems are poorly
             understood. We used the lichen-forming fungi Peltigera and
             their cyanobacterial partners Nostoc to investigate the
             spatial structure of this symbiosis at an intrabiome scale
             and to identify potential factors shaping these
             associations. METHODS:Ninety-three thalli were sampled in
             Québec, Canada, along a south-north and an east-west
             transect of ~1300 km each. We identified the two main
             partners (Peltigera species and Nostoc phylogroups) using
             molecular markers and modeled the effects of environmental
             variables and partner occurrence on Peltigera-Nostoc
             distributions. KEY RESULTS:Peltigera species showed a high
             degree of specialization toward cyanobionts, whereas two
             Nostoc phylogroups dominated both transects by associating
             with several Peltigera species. Peltigera species had
             narrower ranges than these two main cyanobionts.
             Distributions of three Peltigera species were highly
             associated with precipitation and temperature variables,
             which was not detected for Nostoc phylogroups at this
             spatial scale. CONCLUSIONS:For these cyanolichens, factors
             driving patterns of symbiotic associations are scale
             dependent. Contrary to global-scale findings, generalist
             Peltigera species were not more widespread within the boreal
             biome than specialists. Nostoc availability was not the only
             driver of Peltigera species' geographic ranges;
             environmental factors also contributed to their intrabiome
             distributions. Climatic conditions (especially
             precipitation) limited the range of some Peltigera species
             more than the range of their cyanobacterial partners at an
             intrabiome (boreal) scale.},
   Doi = {10.1002/ajb2.1119},
   Key = {fds337995}
}

@article{fds337996,
   Author = {Chagnon, PL and Magain, N and Miadlikowska, J and Lutzoni,
             F},
   Title = {Strong specificity and network modularity at a very fine
             phylogenetic scale in the lichen genus Peltigera.},
   Journal = {Oecologia},
   Volume = {187},
   Number = {3},
   Pages = {767-782},
   Publisher = {Springer Nature},
   Year = {2018},
   Month = {July},
   url = {http://dx.doi.org/10.1007/s00442-018-4159-6},
   Abstract = {Identifying the drivers and evolutionary consequences of
             species interactions is a major goal of community ecology.
             Network-based analyses can provide mathematical tools to
             detect non-random patterns of interactions, and potentially
             help predicting the consequences of such patterns on
             evolutionary dynamics of symbiotic systems. Here, we
             characterize the structure of a lichen network at a very
             fine phylogenetic scale, by identifying the photosynthetic
             partners (i.e., cyanobacteria of the genus Nostoc) of
             lichenized fungi belonging to a monophyletic section of a
             single genus (i.e., section Polydactylon of the genus
             Peltigera), worldwide. Even at such a fine phylogenetic
             scale, we found that interactions were highly modular and
             anti-nested, indicating strong preferences in interactions.
             When considering local Peltigera communities, i.e., datasets
             at small spatial scales with only a slightly broader
             phylogenetic range, interactions remained modular but were
             asymmetric, with generalist Nostoc partners interacting with
             specialized Peltigera species. This asymmetry was not
             detected with our global spatial scale dataset. We discuss
             these results in the light of lichen community assembly, and
             explore how such interaction patterns may influence
             coevolution in lichens and the evolutionary stability of the
             mutualism in general.},
   Doi = {10.1007/s00442-018-4159-6},
   Key = {fds337996}
}


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