Reconstructing the early evolution of Fungi using a six-gene phylogeny
Duke University1, Oregon State University2, Clark University3, Natural History Museum4, University of Minnesota5, Field Museum of Natural History6, Kaiserslautern University of Technology7, University of Arizona8, New York Botanical Garden9, University of Iowa10, Technische Universität Darmstadt11, University of Maine12, United States Department of Agriculture13, University of Georgia14, University of Alabama15, University of California, Berkeley16, University of Kansas17, Aberystwyth University18, West Virginia University19, Washington State University20, Harvard University21, University of North Carolina at Chapel Hill22, Centraalbureau voor Schimmelcultures23, University of Tennessee24, Okayama University25, University of Kassel26, Brandon University27, Pennsylvania State University28, Leibniz Association29, University of Hamburg30, Royal Botanic Garden Edinburgh31
TL;DR: It is indicated that there may have been at least four independent losses of the flagellum in the kingdom Fungi, and the enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.
Abstract: The ancestors of fungi are believed to be simple aquatic forms with flagellated spores, similar to members of the extant phylum Chytridiomycota (chytrids). Current classifications assume that chytrids form an early-diverging clade within the kingdom Fungi and imply a single loss of the spore flagellum, leading to the diversification of terrestrial fungi. Here we develop phylogenetic hypotheses for Fungi using data from six gene regions and nearly 200 species. Our results indicate that there may have been at least four independent losses of the flagellum in the kingdom Fungi. These losses of swimming spores coincided with the evolution of new mechanisms of spore dispersal, such as aerial dispersal in mycelial groups and polar tube eversion in the microsporidia (unicellular forms that lack mitochondria). The enigmatic microsporidia seem to be derived from an endoparasitic chytrid ancestor similar to Rozella allomycis, on the earliest diverging branch of the fungal phylogenetic tree.
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Conrad L. Schoch1, Keith A. Seifert, Sabine M. Huhndorf2, Vincent Robert3 +157 more•Institutions (59)
TL;DR: Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter- and intraspecific variation.
Abstract: Six DNA regions were evaluated as potential DNA barcodes for Fungi, the second largest kingdom of eukaryotic life, by a multinational, multilaboratory consortium. The region of the mitochondrial cytochrome c oxidase subunit 1 used as the animal barcode was excluded as a potential marker, because it is difficult to amplify in fungi, often includes large introns, and can be insufficiently variable. Three subunits from the nuclear ribosomal RNA cistron were compared together with regions of three representative protein-coding genes (largest subunit of RNA polymerase II, second largest subunit of RNA polymerase II, and minichromosome maintenance protein). Although the protein-coding gene regions often had a higher percent of correct identification compared with ribosomal markers, low PCR amplification and sequencing success eliminated them as candidates for a universal fungal barcode. Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter- and intraspecific variation. The nuclear ribosomal large subunit, a popular phylogenetic marker in certain groups, had superior species resolution in some taxonomic groups, such as the early diverging lineages and the ascomycete yeasts, but was otherwise slightly inferior to the ITS. The nuclear ribosomal small subunit has poor species-level resolution in fungi. ITS will be formally proposed for adoption as the primary fungal barcode marker to the Consortium for the Barcode of Life, with the possibility that supplementary barcodes may be developed for particular narrowly circumscribed taxonomic groups.
4,116 citations
Cites background from "Reconstructing the early evolution ..."
...Some also contributed sequences from regions of two additional optional genes, namely the second largest subunit of RNA polymerase II (RPB2; also an AFToL marker) (39) and a gene encoding aminichromosomemaintenance protein (MCM7), which were chosen based on their usefulness in phylogenetic studies and ease of amplification across Ascomycota (40–42)....
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TL;DR: An enhanced understanding of the skin microbiome is necessary to gain insight into microbial involvement in human skin disorders and to enable novel promicrobial and antimicrobial therapeutic approaches for their treatment.
Abstract: The skin is the human body's largest organ, colonized by a diverse milieu of microorganisms, most of which are harmless or even beneficial to their host. Colonization is driven by the ecology of the skin surface, which is highly variable depending on topographical location, endogenous host factors and exogenous environmental factors. The cutaneous innate and adaptive immune responses can modulate the skin microbiota, but the microbiota also functions in educating the immune system. The development of molecular methods to identify microorganisms has led to an emerging view of the resident skin bacteria as highly diverse and variable. An enhanced understanding of the skin microbiome is necessary to gain insight into microbial involvement in human skin disorders and to enable novel promicrobial and antimicrobial therapeutic approaches for their treatment.
2,279 citations
TL;DR: It is shown that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts, and key questions for future work in endophyte biology are highlighted.
Abstract: Summary 1 Summary All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.
2,278 citations
Cites background from "Reconstructing the early evolution ..."
...Interestingly, numerous ascomycetous plant pathogens and saprotrophs are derived from these same lineages (Lutzoni et al., 2004; James et al., 2006)....
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Clark University1, National Institutes of Health2, Louisiana State University3, CABI4, Umeå University5, Field Museum of Natural History6, Duke University7, University of Minnesota8, University of Alabama9, Oregon State University10, Centraalbureau voor Schimmelcultures11, United States Department of Agriculture12, University of Tübingen13, Max Planck Society14, University of Florida15, Pennsylvania State University16, Aberystwyth University17, Complutense University of Madrid18, University of Oslo19, University of Hong Kong20, University of Tartu21, University of Gothenburg22, University of Kansas23, University of Maine24, University of Illinois at Urbana–Champaign25, Royal Ontario Museum26, Georgia State University27, Estonian University of Life Sciences28, Washington State University29, Nova Southeastern University30, Ludwig Maximilian University of Munich31, University of Western Ontario32, Uppsala University33, Brandon University34, Royal Botanic Garden Edinburgh35, State University of New York at Purchase36, Boise State University37, Cornell University38
TL;DR: A comprehensive phylogenetic classification of the kingdom Fungi is proposed, with reference to recent molecular phylogenetic analyses, and with input from diverse members of the fungal taxonomic community.
2,096 citations
Cites background or methods or result from "Reconstructing the early evolution ..."
...6) LSU, SSU, 5.8S, rpb2, tef1 119 BPP¼ 1 MPBS¼ 95 James et al. (2006) LSU, SSU, 5.8S, rpb1, rpb2, tef1 37 BPP¼ 1 MLBS¼ 92 Subclass Agaricomycetidae Matheny et al. (2007b, fig....
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...The recent multilocus analyses of James et al. (2006) and others now provide the sampling, resolution, and support necessary to structure new classifications of these early-diverging groups, although significant questions remain....
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...The clade containing the Ascomycota and Basidiomycota is classified as the subkingdom Dikarya (as used in James et al. 2006), reflecting the putative synapomorphy of dikaryotic hyphae (Tehler 1988)....
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...Dikarya is used here, because it is more descriptive and is consistent with recent use (James et al. 2006; Tehler et al. 2003; Kendrick 1985)....
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...…Glomerales, Entomophthorales and Harpellales) was suggested by a recent study by Liu et al. (2006) using rpb1 and rpb2, but that finding conflicts with results of analyses that included additional loci and taxa, which suggested that the traditional Zygomycota is polyphyletic (James et al. 2006)....
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Clark University1, United States Department of Energy2, University of Minnesota3, Aix-Marseille University4, Spanish National Research Council5, Oregon State University6, University of Cincinnati Academic Health Center7, Utrecht University8, University of Zaragoza9, Duke University10, United States Department of Agriculture11, University of Warsaw12, University of Tokyo13, Nancy-Université14, University of Göttingen15, Pontifical Catholic University of Chile16, University of Helsinki17, Concordia University Wisconsin18, Vanderbilt University19, University of Wisconsin-Madison20, Swedish University of Agricultural Sciences21, Universidad Pública de Navarra22, Swansea University23
TL;DR: Comparative analyses of 31 fungal genomes suggest that lignin-degrading peroxidases expanded in the lineage leading to the ancestor of the Agaricomycetes, which is reconstructed as a white rot species, and then contracted in parallel lineages leading to brown rot and mycorrhizal species.
Abstract: Wood is a major pool of organic carbon that is highly resistant to decay, owing largely to the presence of lignin. The only organisms capable of substantial lignin decay are white rot fungi in the Agaricomycetes, which also contains non-lignin-degrading brown rot and ectomycorrhizal species. Comparative analyses of 31 fungal genomes (12 generated for this study) suggest that lignin-degrading peroxidases expanded in the lineage leading to the ancestor of the Agaricomycetes, which is reconstructed as a white rot species, and then contracted in parallel lineages leading to brown rot and mycorrhizal species. Molecular clock analyses suggest that the origin of lignin degradation might have coincided with the sharp decrease in the rate of organic carbon burial around the end of the Carboniferous period.
1,396 citations
Cites background from "Reconstructing the early evolution ..."
...Twenty-six were selected based on their inclusion in broad-scale eukaryotic phylogenetic studies (21, 39) and other projects (40, 41)....
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References
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TL;DR: The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo, and an executable is available at http://brahms.rochester.edu/software.html.
Abstract: Summary: The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. Availability: MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
20,627 citations
TL;DR: The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data.
Abstract: Summary: The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data. Availability: The MODELTEST package, including the source code and some documentation is available at http://bioag.byu.edu/zoology/crandall―lab/modeltest.html. Contact: dp47@email.byu.edu.
20,105 citations
TL;DR: This work has used extensive and realistic computer simulations to show that the topological accuracy of this new method is at least as high as that of the existing maximum-likelihood programs and much higher than the performance of distance-based and parsimony approaches.
Abstract: The increase in the number of large data sets and the complexity of current probabilistic sequence evolution models necessitates fast and reliable phylogeny reconstruction methods. We describe a new approach, based on the maximum- likelihood principle, which clearly satisfies these requirements. The core of this method is a simple hill-climbing algorithm that adjusts tree topology and branch lengths simultaneously. This algorithm starts from an initial tree built by a fast distance-based method and modifies this tree to improve its likelihood at each iteration. Due to this simultaneous adjustment of the topology and branch lengths, only a few iterations are sufficient to reach an optimum. We used extensive and realistic computer simulations to show that the topological accuracy of this new method is at least as high as that of the existing maximum-likelihood programs and much higher than the performance of distance-based and parsimony approaches. The reduction of computing time is dramatic in comparison with other maximum-likelihood packages, while the likelihood maximization ability tends to be higher. For example, only 12 min were required on a standard personal computer to analyze a data set consisting of 500 rbcL sequences with 1,428 base pairs from plant plastids, thus reaching a speed of the same order as some popular distance-based and parsimony algorithms. This new method is implemented in the PHYML program, which is freely available on our web page: http://www.lirmm.fr/w3ifa/MAAS/. (Algorithm; computer simulations; maximum likelihood; phylogeny; rbcL; RDPII project.) The size of homologous sequence data sets has in- creased dramatically in recent years, and many of these data sets now involve several hundreds of taxa. More- over, current probabilistic sequence evolution models (Swofford et al., 1996 ; Page and Holmes, 1998 ), notably those including rate variation among sites (Uzzell and Corbin, 1971 ; Jin and Nei, 1990 ; Yang, 1996 ), require an increasing number of calculations. Therefore, the speed of phylogeny reconstruction methods is becoming a sig- nificant requirement and good compromises between speed and accuracy must be found. The maximum likelihood (ML) approach is especially accurate for building molecular phylogenies. Felsenstein (1981) brought this framework to nucleotide-based phy- logenetic inference, and it was later also applied to amino acid sequences (Kishino et al., 1990). Several vari- ants were proposed, most notably the Bayesian meth- ods (Rannala and Yang 1996; and see below), and the discrete Fourier analysis of Hendy et al. (1994), for ex- ample. Numerous computer studies (Huelsenbeck and Hillis, 1993; Kuhner and Felsenstein, 1994; Huelsenbeck, 1995; Rosenberg and Kumar, 2001; Ranwez and Gascuel, 2002) have shown that ML programs can recover the cor- rect tree from simulated data sets more frequently than other methods can. Another important advantage of the ML approach is the ability to compare different trees and evolutionary models within a statistical framework (see Whelan et al., 2001, for a review). However, like all optimality criterion-based phylogenetic reconstruction approaches, ML is hampered by computational difficul- ties, making it impossible to obtain the optimal tree with certainty from even moderate data sets (Swofford et al., 1996). Therefore, all practical methods rely on heuristics that obtain near-optimal trees in reasonable computing time. Moreover, the computation problem is especially difficult with ML, because the tree likelihood not only depends on the tree topology but also on numerical pa- rameters, including branch lengths. Even computing the optimal values of these parameters on a single tree is not an easy task, particularly because of possible local optima (Chor et al., 2000). The usual heuristic method, implemented in the pop- ular PHYLIP (Felsenstein, 1993 ) and PAUP ∗ (Swofford, 1999 ) packages, is based on hill climbing. It combines stepwise insertion of taxa in a growing tree and topolog- ical rearrangement. For each possible insertion position and rearrangement, the branch lengths of the resulting tree are optimized and the tree likelihood is computed. When the rearrangement improves the current tree or when the position insertion is the best among all pos- sible positions, the corresponding tree becomes the new current tree. Simple rearrangements are used during tree growing, namely "nearest neighbor interchanges" (see below), while more intense rearrangements can be used once all taxa have been inserted. The procedure stops when no rearrangement improves the current best tree. Despite significant decreases in computing times, no- tably in fastDNAml (Olsen et al., 1994 ), this heuristic becomes impracticable with several hundreds of taxa. This is mainly due to the two-level strategy, which sepa- rates branch lengths and tree topology optimization. In- deed, most calculations are done to optimize the branch lengths and evaluate the likelihood of trees that are finally rejected. New methods have thus been proposed. Strimmer and von Haeseler (1996) and others have assembled four- taxon (quartet) trees inferred by ML, in order to recon- struct a complete tree. However, the results of this ap- proach have not been very satisfactory to date (Ranwez and Gascuel, 2001 ). Ota and Li (2000, 2001) described
16,261 citations
TL;DR: TREE-PUZZLE is a program package for quartet-based maximum-likelihood phylogenetic analysis that provides methods for reconstruction, comparison, and testing of trees and models on DNA as well as protein sequences to reduce waiting time for larger datasets.
Abstract: SUMMARY TREE-PUZZLE is a program package for quartet-based maximum-likelihood phylogenetic analysis (formerly PUZZLE, Strimmer and von Haeseler, Mol. Biol. Evol., 13, 964-969, 1996) that provides methods for reconstruction, comparison, and testing of trees and models on DNA as well as protein sequences. To reduce waiting time for larger datasets the tree reconstruction part of the software has been parallelized using message passing that runs on clusters of workstations as well as parallel computers. AVAILABILITY http://www.tree-puzzle.de. The program is written in ANSI C. TREE-PUZZLE can be run on UNIX, Windows and Mac systems, including Mac OS X. To run the parallel version of PUZZLE, a Message Passing Interface (MPI) library has to be installed on the system. Free MPI implementations are available on the Web (cf. http://www.lam-mpi.org/mpi/implementations/).
2,581 citations