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Factors driving metabolic diversity in the budding yeast subphylum.
Opulente DA, Rollinson EJ, Bernick-Roehr C, Hulfachor AB, Rokas A, Kurtzman CP, Hittinger CT
(2018) BMC Biol 16: 26
MeSH Terms: Biological Evolution, Genetic Variation, Metabolic Networks and Pathways, Phylogeny, Saccharomycetales
Show Abstract · Added March 21, 2018
BACKGROUND - Associations between traits are prevalent in nature, occurring across a diverse range of taxa and traits. Individual traits may co-evolve with one other, and these correlations can be driven by factors intrinsic or extrinsic to an organism. However, few studies, especially in microbes, have simultaneously investigated both across a broad taxonomic range. Here we quantify pairwise associations among 48 traits across 784 diverse yeast species of the ancient budding yeast subphylum Saccharomycotina, assessing the effects of phylogenetic history, genetics, and ecology.
RESULTS - We find extensive negative (traits that tend to not occur together) and positive (traits that tend to co-occur) pairwise associations among traits, as well as between traits and environments. These associations can largely be explained by the biological properties of the traits, such as overlapping biochemical pathways. The isolation environments of the yeasts explain a minor but significant component of the variance, while phylogeny (the retention of ancestral traits in descendant species) plays an even more limited role. Positive correlations are pervasive among carbon utilization traits and track with chemical structures (e.g., glucosides and sugar alcohols) and metabolic pathways, suggesting a molecular basis for the presence of suites of traits. In several cases, characterized genes from model organisms suggest that enzyme promiscuity and overlapping biochemical pathways are likely mechanisms to explain these macroevolutionary trends. Interestingly, fermentation traits are negatively correlated with the utilization of pentose sugars, which are major components of the plant biomass degraded by fungi and present major bottlenecks to the production of cellulosic biofuels. Finally, we show that mammalian pathogenic and commensal yeasts have a suite of traits that includes growth at high temperature and, surprisingly, the utilization of a narrowed panel of carbon sources.
CONCLUSIONS - These results demonstrate how both intrinsic physiological factors and extrinsic ecological factors drive the distribution of traits present in diverse organisms across macroevolutionary timescales.
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5 MeSH Terms
Drivers of genetic diversity in secondary metabolic gene clusters within a fungal species.
Lind AL, Wisecaver JH, Lameiras C, Wiemann P, Palmer JM, Keller NP, Rodrigues F, Goldman GH, Rokas A
(2017) PLoS Biol 15: e2003583
MeSH Terms: Alleles, Aspergillus fumigatus, Biological Evolution, Fungal Proteins, Fungi, Genetic Variation, Genome, Fungal, Genomics, Metabolic Networks and Pathways, Multigene Family, Mutation, Polymorphism, Genetic, Secondary Metabolism
Show Abstract · Added March 21, 2018
Filamentous fungi produce a diverse array of secondary metabolites (SMs) critical for defense, virulence, and communication. The metabolic pathways that produce SMs are found in contiguous gene clusters in fungal genomes, an atypical arrangement for metabolic pathways in other eukaryotes. Comparative studies of filamentous fungal species have shown that SM gene clusters are often either highly divergent or uniquely present in one or a handful of species, hampering efforts to determine the genetic basis and evolutionary drivers of SM gene cluster divergence. Here, we examined SM variation in 66 cosmopolitan strains of a single species, the opportunistic human pathogen Aspergillus fumigatus. Investigation of genome-wide within-species variation revealed 5 general types of variation in SM gene clusters: nonfunctional gene polymorphisms; gene gain and loss polymorphisms; whole cluster gain and loss polymorphisms; allelic polymorphisms, in which different alleles corresponded to distinct, nonhomologous clusters; and location polymorphisms, in which a cluster was found to differ in its genomic location across strains. These polymorphisms affect the function of representative A. fumigatus SM gene clusters, such as those involved in the production of gliotoxin, fumigaclavine, and helvolic acid as well as the function of clusters with undefined products. In addition to enabling the identification of polymorphisms, the detection of which requires extensive genome-wide synteny conservation (e.g., mobile gene clusters and nonhomologous cluster alleles), our approach also implicated multiple underlying genetic drivers, including point mutations, recombination, and genomic deletion and insertion events as well as horizontal gene transfer from distant fungi. Finally, most of the variants that we uncover within A. fumigatus have been previously hypothesized to contribute to SM gene cluster diversity across entire fungal classes and phyla. We suggest that the drivers of genetic diversity operating within a fungal species shown here are sufficient to explain SM cluster macroevolutionary patterns.
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13 MeSH Terms
Embracing Uncertainty in Reconstructing Early Animal Evolution.
King N, Rokas A
(2017) Curr Biol 27: R1081-R1088
MeSH Terms: Animals, Biological Evolution, Classification, Evolution, Molecular, Invertebrates, Phylogeny, Uncertainty
Show Abstract · Added March 21, 2018
The origin of animals, one of the major transitions in evolution, remains mysterious. Many key aspects of animal evolution can be reconstructed by comparing living species within a robust phylogenetic framework. However, uncertainty remains regarding the evolutionary relationships between two ancient animal lineages - sponges and ctenophores - and the remaining animal phyla. Comparative morphology and some phylogenomic analyses support the view that sponges represent the sister lineage to the rest of the animals, while other phylogenomic analyses support ctenophores, a phylum of carnivorous, gelatinous marine organisms, as the sister lineage. Here, we explore why different studies yield different answers and discuss the implications of the two alternative hypotheses for understanding the origin of animals. Reconstruction of ancient evolutionary radiations is devilishly difficult and will likely require broader sampling of sponge and ctenophore genomes, improved analytical strategies and critical analyses of the phylogenetic distribution and molecular mechanisms underlying apparently conserved traits. Rather than staking out positions in favor of the ctenophores-sister or the sponges-sister hypothesis, we submit that research programs aimed at understanding the biology of the first animals should instead embrace the uncertainty surrounding early animal evolution in their experimental designs.
Copyright © 2017 Elsevier Ltd. All rights reserved.
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7 MeSH Terms
Transposable Element Exaptation into Regulatory Regions Is Rare, Influenced by Evolutionary Age, and Subject to Pleiotropic Constraints.
Simonti CN, Pavlicev M, Capra JA
(2017) Mol Biol Evol 34: 2856-2869
MeSH Terms: Animals, Biological Evolution, DNA Transposable Elements, Gene Expression Regulation, Genetic Pleiotropy, Humans, Mice, Promoter Regions, Genetic, Regulatory Sequences, Nucleic Acid
Show Abstract · Added March 14, 2018
Transposable element (TE)-derived sequences make up approximately half of most mammalian genomes, and many TEs have been co-opted into gene regulatory elements. However, we lack a comprehensive tissue- and genome-wide understanding of how and when TEs gain regulatory activity in their hosts. We evaluated the prevalence of TE-derived DNA in enhancers and promoters across hundreds of human and mouse cell lines and primary tissues. Promoters are significantly depleted of TEs in all tissues compared with their overall prevalence in the genome (P < 0.001); enhancers are also depleted of TEs, though not as strongly as promoters. The degree of enhancer depletion also varies across contexts (1.5-3×), with reproductive and immune cells showing the highest levels of TE regulatory activity in humans. Overall, in spite of the regulatory potential of many TE sequences, they are significantly less active in gene regulation than expected from their prevalence. TE age is predictive of the likelihood of enhancer activity; TEs originating before the divergence of amniotes are 9.2 times more likely to have enhancer activity than TEs that integrated in great apes. Context-specific enhancers are more likely to be TE-derived than enhancers active in multiple tissues, and young TEs are more likely to overlap context-specific enhancers than old TEs (86% vs. 47%). Once TEs obtain enhancer activity in the host, they have similar functional dynamics to one another and non-TE-derived enhancers, likely driven by pleiotropic constraints. However, a few TE families, most notably endogenous retroviruses, have greater regulatory potential. Our observations suggest a model of regulatory co-option in which TE-derived sequences are initially repressed, after which a small fraction obtains context-specific enhancer activity, with further gains subject to pleiotropic constraints.
© The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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9 MeSH Terms
Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes.
Hockman D, Burns AJ, Schlosser G, Gates KP, Jevans B, Mongera A, Fisher S, Unlu G, Knapik EW, Kaufman CK, Mosimann C, Zon LI, Lancman JJ, Dong PDS, Lickert H, Tucker AS, Baker CV
(2017) Elife 6:
MeSH Terms: Animals, Anura, Biological Evolution, Cell Hypoxia, Cell Lineage, Lampreys, Neuroendocrine Cells, Neuroepithelial Cells, Zebrafish
Show Abstract · Added April 26, 2017
The evolutionary origins of the hypoxia-sensitive cells that trigger amniote respiratory reflexes - carotid body glomus cells, and 'pulmonary neuroendocrine cells' (PNECs) - are obscure. Homology has been proposed between glomus cells, which are neural crest-derived, and the hypoxia-sensitive 'neuroepithelial cells' (NECs) of fish gills, whose embryonic origin is unknown. NECs have also been likened to PNECs, which differentiate in situ within lung airway epithelia. Using genetic lineage-tracing and neural crest-deficient mutants in zebrafish, and physical fate-mapping in frog and lamprey, we find that NECs are not neural crest-derived, but endoderm-derived, like PNECs, whose endodermal origin we confirm. We discover neural crest-derived catecholaminergic cells associated with zebrafish pharyngeal arch blood vessels, and propose a new model for amniote hypoxia-sensitive cell evolution: endoderm-derived NECs were retained as PNECs, while the carotid body evolved via the aggregation of neural crest-derived catecholaminergic (chromaffin) cells already associated with blood vessels in anamniote pharyngeal arches.
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9 MeSH Terms
The evolutionary and phylogeographic history of woolly mammoths: a comprehensive mitogenomic analysis.
Chang D, Knapp M, Enk J, Lippold S, Kircher M, Lister A, MacPhee RD, Widga C, Czechowski P, Sommer R, Hodges E, Stümpel N, Barnes I, Dalén L, Derevianko A, Germonpré M, Hillebrand-Voiculescu A, Constantin S, Kuznetsova T, Mol D, Rathgeber T, Rosendahl W, Tikhonov AN, Willerslev E, Hannon G, Lalueza-Fox C, Joger U, Poinar H, Hofreiter M, Shapiro B
(2017) Sci Rep 7: 44585
MeSH Terms: Animal Distribution, Animals, Asia, Biological Evolution, DNA, Mitochondrial, Europe, Extinction, Biological, Female, Fossils, Gene Flow, Genome, Mitochondrial, Male, Mammoths, North America, Phylogeny, Phylogeography, Sequence Analysis, DNA
Show Abstract · Added April 26, 2017
Near the end of the Pleistocene epoch, populations of the woolly mammoth (Mammuthus primigenius) were distributed across parts of three continents, from western Europe and northern Asia through Beringia to the Atlantic seaboard of North America. Nonetheless, questions about the connectivity and temporal continuity of mammoth populations and species remain unanswered. We use a combination of targeted enrichment and high-throughput sequencing to assemble and interpret a data set of 143 mammoth mitochondrial genomes, sampled from fossils recovered from across their Holarctic range. Our dataset includes 54 previously unpublished mitochondrial genomes and significantly increases the coverage of the Eurasian range of the species. The resulting global phylogeny confirms that the Late Pleistocene mammoth population comprised three distinct mitochondrial lineages that began to diverge ~1.0-2.0 million years ago (Ma). We also find that mammoth mitochondrial lineages were strongly geographically partitioned throughout the Pleistocene. In combination, our genetic results and the pattern of morphological variation in time and space suggest that male-mediated gene flow, rather than large-scale dispersals, was important in the Pleistocene evolutionary history of mammoths.
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17 MeSH Terms
A Derived Allosteric Switch Underlies the Evolution of Conditional Cooperativity between HOXA11 and FOXO1.
Nnamani MC, Ganguly S, Erkenbrack EM, Lynch VJ, Mizoue LS, Tong Y, Darling HL, Fuxreiter M, Meiler J, Wagner GP
(2016) Cell Rep 15: 2097-2108
MeSH Terms: Allosteric Regulation, Amino Acid Sequence, Amino Acid Substitution, Animals, Biological Evolution, CREB-Binding Protein, DNA-Activated Protein Kinase, Forkhead Box Protein O1, HeLa Cells, Homeodomain Proteins, Humans, Intrinsically Disordered Proteins, Mice, Models, Biological, Models, Molecular, Phosphorylation, Protein Binding, Protein Domains, Protein Structure, Secondary, Transcriptional Activation
Show Abstract · Added April 8, 2017
Transcription factors (TFs) play multiple roles in development. Given this multifunctionality, it has been assumed that TFs are evolutionarily highly constrained. Here, we investigate the molecular mechanisms for the origin of a derived functional interaction between two TFs, HOXA11 and FOXO1. We have previously shown that the regulatory role of HOXA11 in mammalian endometrial stromal cells requires interaction with FOXO1, and that the physical interaction between these proteins evolved before their functional cooperativity. Here, we demonstrate that the derived functional cooperativity between HOXA11 and FOXO1 is due to derived allosteric regulation of HOXA11 by FOXO1. This study shows that TF function can evolve through changes affecting the functional output of a pre-existing protein complex.
Copyright © 2016 The Author(s). Published by Elsevier Inc. All rights reserved.
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20 MeSH Terms
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes.
Wisecaver JH, Alexander WG, King SB, Hittinger CT, Rokas A
(2016) Mol Biol Evol 33: 1979-87
MeSH Terms: Adaptation, Biological, Amino Acid Sequence, Bacteria, Bacterial Proteins, Biological Evolution, Computational Biology, Databases, Nucleic Acid, Dihydropteridine Reductase, Escherichia coli Proteins, Eukaryota, Evolution, Molecular, Fungi, Gene Duplication, Gene Transfer, Horizontal, Hemeproteins, NADH, NADPH Oxidoreductases, Nitric Oxide, Phylogeny
Show Abstract · Added April 6, 2017
Due to their functional independence, proteins that comprise standalone metabolic units, which we name single-protein metabolic modules, may be particularly prone to gene duplication (GD) and horizontal gene transfer (HGT). Flavohemoglobins (flavoHbs) are prime examples of single-protein metabolic modules, detoxifying nitric oxide (NO), a ubiquitous toxin whose antimicrobial properties many life forms exploit, to nitrate, a common source of nitrogen for organisms. FlavoHbs appear widespread in bacteria and have been identified in a handful of microbial eukaryotes, but how the distribution of this ecologically and biomedically important protein family evolved remains unknown. Reconstruction of the evolutionary history of 3,318 flavoHb protein sequences covering the family's known diversity showed evidence of recurrent HGT at multiple evolutionary scales including intrabacterial HGT, as well as HGT from bacteria to eukaryotes. One of the most striking examples of HGT is the acquisition of a flavoHb by the dandruff- and eczema-causing fungus Malassezia from Corynebacterium Actinobacteria, a transfer that growth experiments show is capable of mediating NO resistance in fungi. Other flavoHbs arose via GD; for example, many filamentous fungi possess two flavoHbs that are differentially targeted to the cytosol and mitochondria, likely conferring protection against external and internal sources of NO, respectively. Because single-protein metabolic modules such as flavoHb function independently, readily undergo GD and HGT, and are frequently involved in organismal defense and competition, we suggest that they represent "plug-and-play" proteins for ecological arms races.
© The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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18 MeSH Terms
Editorial overview: Genomes and evolution: "Seq-ing" answers in life's genomes.
Rokas A, Soltis PS
(2015) Curr Opin Genet Dev 35: iv-vi
MeSH Terms: Animals, Bacteria, Biodiversity, Biological Evolution, Chromosome Mapping, Genetic Variation, Genome, High-Throughput Nucleotide Sequencing, Humans, Plants
Added February 22, 2016
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10 MeSH Terms
The evolution of the human genome.
Simonti CN, Capra JA
(2015) Curr Opin Genet Dev 35: 9-15
MeSH Terms: Biological Evolution, Evolution, Molecular, Gene Expression Regulation, Genetic Variation, Genetics, Population, Genome, Human, Humans, Regulatory Sequences, Nucleic Acid, Selection, Genetic
Show Abstract · Added April 29, 2016
Human genomes hold a record of the evolutionary forces that have shaped our species. Advances in DNA sequencing, functional genomics, and population genetic modeling have deepened our understanding of human demographic history, natural selection, and many other long-studied topics. These advances have also revealed many previously underappreciated factors that influence the evolution of the human genome, including functional modifications to DNA and histones, conserved 3D topological chromatin domains, structural variation, and heterogeneous mutation patterns along the genome. Using evolutionary theory as a lens to study these phenomena will lead to significant breakthroughs in understanding what makes us human and why we get sick.
Copyright © 2015 Elsevier Ltd. All rights reserved.
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9 MeSH Terms