Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi

BackgroundIn eukaryotic cells, directional transport between different compartments of the endomembrane system is mediated by vesicles that bud from a donor organelle and then fuse with an acceptor organelle. A family of integral membrane proteins, termed soluble N-ethylmaleimide-sensitive factor attachment receptor (SNARE) proteins, constitute the key machineries of these different membrane fusion events. Over the past 30 years, the yeast Saccharomyces cerevisiae has served as a powerful model organism for studying the organization of the secretory and endocytic pathways, and a few years ago, its entire set of SNAREs was compiled.ResultsHere, we make use of the increasing amount of genomic data to investigate the history of the SNARE family during fungi evolution. Moreover, since different SNARE family members are thought to demarcate different organelles and vesicles, this approach allowed us to compare the organization of the endomembrane systems of yeast and animal cells. Our data corroborate the notion that fungi generally encompass a relatively simple set of SNARE proteins, mostly comprising the SNAREs of the proto-eukaryotic cell. However, all fungi contain a novel soluble SNARE protein, Vam7, which carries an N-terminal PX-domain that acts as a phosphoinositide binding module. In addition, the points in fungal evolution, at which lineage-specific duplications and diversifications occurred, could be determined. For instance, the endosomal syntaxins Pep12 and Vam3 arose from a gene duplication that occurred within the Saccharomycotina clade.ConclusionAlthough the SNARE repertoire of baker's yeast is highly conserved, our analysis reveals that it is more deviated than the ones of basal fungi. This highlights that the trafficking pathways of baker's yeast are not only different to those in animal cells but also are somewhat different to those of many other fungi.

• Publication year

  2009

• Venue

  BMC Evolutionary Biology

• Publication date

  2009-01-23

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1186/1471-2148-9-19PMID 19166604PMCID 2639358
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• Baker's yeast has a SNARE repertoire that is more derived than that of basal fungi, indicating that its trafficking pathways differ from those of many other fungi and from animal cells.

  Confidence 0.90

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• Pep12 and Vam3 trace to a gene duplication that occurred within the Saccharomycotina clade.

  Confidence 0.92

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• All fungi examined contain Vam7, a soluble SNARE that carries an N-terminal PX domain.

  Confidence 0.97

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• Fungi generally retain a relatively simple SNARE repertoire that mostly reflects the SNARE set of the proto-eukaryotic cell.

  Confidence 0.94

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review

• baker's yeast

  organism, model organism

  Saccharomyces cerevisiae, the yeast model organism whose SNARE repertoire is compared with other fungi.

  Aliases: Saccharomyces cerevisiae, yeast

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• basal fungi

  fungal group, comparison set

  Early-branching fungal groups used as a comparison set for SNARE repertoire conservation.

  Aliases: early-branching fungi

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• pep12

  protein, SNARE

  An endosomal syntaxin SNARE found in fungi and used in the phylogenetic comparison.

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• proto-eukaryotic cell

  evolutionary reference, cell state

  The inferred ancestral eukaryotic cell state used here as a reference for early SNARE complement composition.

  Aliases: ancestral eukaryotic cell

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• px domain

  protein domain, binding module

  A phosphoinositide-binding protein domain found at the N-terminus of Vam7.

  Aliases: phox homology domain

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• saccharomycotina clade

  clade, fungal lineage

  A fungal lineage within which the duplication giving rise to Pep12 and Vam3 is placed.

  Aliases: Saccharomycotina

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• snare proteins

  protein family, membrane fusion machinery

  A family of membrane fusion proteins that mediate vesicle fusion between compartments of the endomembrane system.

  Aliases: soluble N-ethylmaleimide-sensitive factor attachment receptor proteins, SNAREs

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• vam3

  protein, SNARE

  An endosomal syntaxin SNARE found in fungi and used in the phylogenetic comparison.

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review
• vam7

  protein, SNARE

  A fungal soluble SNARE protein that contains an N-terminal PX domain.

  박진우 (dztg5apj7m) extraction뀨 (7c402c1b98) reviewmexicorea (qjvnbu8xg3) review

• The Ypt/Rab Family and the Evolution of Trafficking in Fungi

  2008cited by this paper
• Comparative genomics of the Rab protein family in Apicomplexan parasites

  2008cited by this paper
• The Structure of the Yeast Plasma Membrane SNARE Complex Reveals Destabilizing Water-filled Cavities*

  2008cited by this paper
• Ustilago maydis, a new fungal model system for cell biology.

  2008cited by this paper
• Yeast vacuole fusion: A model system for eukaryotic endomembrane dynamics

  2008cited by this paper
• SNAREing the basis of multicellularity: consequences of protein family expansion during evolution.

  2008cited by this paper
• Mechanisms of membrane fusion: disparate players and common principles

  2008cited by this paper
• Synaptic vesicle fusion

  2008cited by this paper
• Budding insights on cell polarity

  2007cited by this paper
• Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies

  2007cited by this paper
• Orchestrating organelle inheritance in Saccharomyces cerevisiae.

  2007cited by this paper
• Structure of the yeast polarity protein Sro7 reveals a SNARE regulatory mechanism

  2007cited by this paper
• Increases in the Number of SNARE Genes Parallels the Rise of Multicellularity among the Green Plants1[W][OA]

  2007influential reference
• Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode

  2007influential reference
• Yeast genome evolution—the origin of the species

  2007cited by this paper
• Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication

  2007cited by this paper
• Systematic analysis of SNARE localization in the filamentous fungus Aspergillus oryzae.

  2007cited by this paper
• TBestDB: a taxonomically broad database of expressed sequence tags (ESTs)

  2007cited by this paper
• Spatially Segregated SNARE Protein Interactions in Living Fungal Cells*

  2007influential reference
• Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle.

  2007cited by this paper
• Opinion: On the move: endosomes in fungal growth and pathogenicity

  2007cited by this paper
• An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system.

  2007cited by this paper
• Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution.

  2006cited by this paper
• Lethal giant larvae take on a life of their own.

  2006cited by this paper
• Endocytosis Is Essential for Pathogenic Development in the Corn Smut Fungus Ustilago maydis[W]

  2006cited by this paper
• Application of phylogenetic networks in evolutionary studies.

  2006cited by this paper
• A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis

  2006cited by this paper
• Identification of the yeast R-SNARE Nyv1p as a novel longin domain-containing protein.

  2006cited by this paper
• Reconstructing the early evolution of Fungi using a six-gene phylogeny

  2006cited by this paper
• Phylogenetics of Saccharomycetales, the ascomycete yeasts.

  2006cited by this paper
• Organelles on the move: insights from yeast vacuole inheritance

  2006cited by this paper
• Lethal Giant Puzzle of Lgl

  2006cited by this paper
• SNAREs — engines for membrane fusion

  2006cited by this paper
• Extracting Sequence Motifs and the Phylogenetic Features of SNARE‐Dependent Membrane Traffic

  2006cited by this paper
• SNAREs and traffic.

  2005cited by this paper
• SNAREs and traffic.

  2005cited by this paper
• Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex.

  2005cited by this paper
• The diversity of Rab GTPases in Entamoeba histolytica.

  2005cited by this paper
• Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis.

  2005cited by this paper
• Ascospore Formation in the Yeast Saccharomyces cerevisiae

  2005cited by this paper
• Genomics of the fungal kingdom: insights into eukaryotic biology.

  2005cited by this paper
• Molecular and phylogenetic characterization of syntaxin genes from parasitic protozoa.

  2004cited by this paper
• A Complete Set of SNAREs in Yeast

  2004cited by this paper
• Structural Basis for the Inhibitory Role of Tomosyn in Exocytosis*♦

  2004cited by this paper
• MUSCLE: a multiple sequence alignment method with reduced time and space complexity

  2004cited by this paper
• Mapping of sporulation-specific functions in the yeast syntaxin gene SSO1

  2004cited by this paper
• Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators.

  2004cited by this paper
• 23 genes, 23 years later.

  2004cited by this paper
• Phylogeny and Evolution of Medical Species of Candida and Related Taxa: a Multigenic Analysis

  2004cited by this paper
• IQPNNI: moving fast through tree space and stopping in time.

  2004cited by this paper
• A SNARE required for retrograde transport to the endoplasmic reticulum

  2003cited by this paper
• Yeast Functional Analysis: Identification of Two Essential Genes Involved in ER to Golgi Trafficking

  2003cited by this paper
• Use1p is a yeast SNARE protein required for retrograde traffic to the ER

  2003cited by this paper
• A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.

  2003cited by this paper
• Two divergent plasma membrane syntaxin-like SNAREs, nsyn1 and nsyn2, contribute to hyphal tip growth and other developmental processes in Neurospora crassa.

  2003cited by this paper
• The Plasmodium falciparum family of Rab GTPases.

  2003cited by this paper
• Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora.

  2003cited by this paper
• An approximately unbiased test of phylogenetic tree selection.

  2002cited by this paper
• A New Yeast Endosomal SNARE Related to Mammalian Syntaxin 8

  2002cited by this paper
• Characterization of temperature-sensitive mutations in the yeast syntaxin 1 homologues Sso1p and Sso2p, and evidence of a distinct function for Sso1p in sporulation.

  2002cited by this paper
• Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs

  2002cited by this paper
• The Arabidopsis Rab GTPase family: another enigma variation.

  2002cited by this paper
• Predicting the distribution, conservation, and functions of SNAREs and related proteins in fungi.

  2002cited by this paper
• Insights from yeast endosomes.

  2002cited by this paper
• Yeast vacuoles and membrane fusion pathways

  2002cited by this paper
• Longins: a new evolutionary conserved VAMP family sharing a novel SNARE domain.

  2001cited by this paper
• CONSEL: for assessing the confidence of phylogenetic tree selection

  2001cited by this paper
• A genomic perspective on membrane compartment organization

  2001cited by this paper
• An Autoinhibitory Mechanism for Nonsyntaxin SNARE Proteins Revealed by the Structure of Ykt6p

  2001cited by this paper
• Evolution of the Rab family of small GTP-binding proteins.

  2001cited by this paper
• A Novel SNARE N-terminal Domain Revealed by the Crystal Structure of Sec22b*

  2001cited by this paper
• SNAREs and the specificity of membrane fusion.

  2001cited by this paper
• Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes

  2001cited by this paper
• SNARE complexes--is there sufficient complexity for vesicle targeting specificity?

  2001cited by this paper
• A putative endosomal t‐SNARE links exo‐ and endocytosis in the phytopathogenic fungus Ustilago maydis

  2000cited by this paper
• The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors.

  2000cited by this paper
• The Arabidopsis genome

  2000cited by this paper
• Identification of domains required for developmentally regulated SNARE function in Saccharomyces cerevisiae.

  2000cited by this paper
• SNAREs and the secretory pathway-lessons from yeast.

  1999cited by this paper
• Vam7p, a SNAP-25-Like Molecule, and Vam3p, a Syntaxin Homolog, Function Together in Yeast Vacuolar Protein Trafficking

  1998cited by this paper
• Gos1p, a Saccharomyces cerevisiae SNARE protein involved in Golgi transport

  1998cited by this paper
• Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution

  1998cited by this paper
• A model for structural similarity between different SNARE complexes based on sequence relationships.

  1998cited by this paper
• Two syntaxin homologues in the TGN/endosomal system of yeast

  1998cited by this paper
• Tomosyn: a syntaxin-1-binding protein that forms a novel complex in the neurotransmitter release process.

  1998cited by this paper
• Sro7p, a Saccharomyces cerevisiae counterpart of the tumor suppressor l(2)gl protein, is related to myosins in function.

  1998cited by this paper
• Prospore Membrane Formation Defines a Developmentally Regulated Branch of the Secretory Pathway in Yeast

  1998cited by this paper
• Vam7p, a vacuolar SNAP‐25 homolog, is required for SNARE complex integrity and vacuole docking and fusion

  1998cited by this paper
• Profile hidden Markov models

  1998cited by this paper
• Tlg2p, a Yeast Syntaxin Homolog That Resides on the Golgi and Endocytic Structures*

  1998cited by this paper
• Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs.

  1998cited by this paper
• Tomosyn binds t-SNARE proteins via a VAMP-like coiled coil.

  1998cited by this paper
• A novel SNARE complex implicated in vesicle fusion with the endoplasmic reticulum

  1997cited by this paper
• Vam3p, a new member of syntaxin related protein, is required for vacuolar assembly in the yeast Saccharomyces cerevisiae.

  1997cited by this paper
• High expression of the yeast syntaxin‐related Vam3 protein suppresses the protein transport defects of a pep12 null mutant

  1997cited by this paper
• The Yeast v-SNARE Vti1p Mediates Two Vesicle Transport Pathways through Interactions with the t-SNAREs Sed5p and Pep12p

  1997cited by this paper
• A conserved domain is present in different families of vesicular fusion proteins: a new superfamily.

  1997cited by this paper
• A Multispecificity Syntaxin Homologue, Vam3p, Essential for Autophagic and Biosynthetic Protein Transport to the Vacuole

  1997cited by this paper
• Homotypic vacuolar fusion mediated by t- and v-SNAREs

  1997cited by this paper
• Neurotransmitter release - four years of SNARE complexes.

  1997cited by this paper

• SNARE genes CcSec22 and CcSso1 coordinate fungal growth, sporulation, cell wall stress tolerance, endocytosis and full virulence in Cytospora chrysosperma

  2025cites this paper
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  2025cites this paper
• A REVIEW ON PROTEIN PRODUCTION AND SECRETION IN EUKARYOYTES

  2024cites this paper
• mrvam7, a conserved SNARE gene involved in vacuolar fusion, is required for development and secondary metabolism in Monascus ruber M7

  2024cites this paper
• Two distinct SNARE complexes mediate vesicle fusion with the plasma membrane to ensure effective development and pathogenesis of Fusarium oxysporum f. sp. cubense

  2024cites this paper
• A look beyond the QR code of SNARE proteins

  2024influential citation
• SNARE Proteins in Synaptic Vesicle Fusion.

  2023cites this paper
• Cell polarity in the protist-to-animal transition.

  2023cites this paper
• Mechanisms of SNARE proteins in membrane fusion

  2023cites this paper
• Neuronal SNARE complex assembly guided by Munc18‐1 and Munc13‐1

  2022cites this paper
• A Phosphoinositide-Binding Protein Acts in the Trafficking Pathway of Hemoglobin in the Malaria Parasite Plasmodium falciparum

  2022cites this paper
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  2022cites this paper
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• Analysis of the SNARE Stx8 recycling reveals that the retromer-sorting motif has undergone evolutionary divergence

  2021cites this paper
• The Fusarium graminearum t-SNARE Sso2 Is Involved in Growth, Defense, and DON Accumulation and Virulence.

  2020cites this paper
• Evolution and Natural History of Membrane Trafficking in Eukaryotes.

  2020cites this paper
• Evolutionary origins of chemical synapses.

  2020cites this paper
• New Perspectives on SNARE Function in the Yeast Minimal Endomembrane System

  2020cites this paper
• The SNARE protein FolVam7 mediates intracellular trafficking to regulate conidiogenesis and pathogenicity in Fusarium oxysporum f. sp. lycopersici

  2019cites this paper
• Identifying SNAREs by Incorporating Deep Learning Architecture and Amino Acid Embedding Representation

  2019cites this paper
• Prototypic SNARE proteins are encoded in the genomes of Heimdallarchaeota, potentially bridging the gap between the prokaryotes and eukaryotes

  2019cites this paper
• Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain

  2019influential citation
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  2019cites this paper
• SNARE-CNN: a 2D convolutional neural network architecture to identify SNARE proteins from high-throughput sequencing data

  2019cites this paper
• CRISPR/Cas9-mediated endogenous gene tagging in Fusarium oxysporum.

  2019cites this paper
• Hybridization in bottlenose dolphins—A case study of Tursiops aduncus × T. truncatus hybrids and successful backcross hybridization events

  2018cites this paper
• Phylogenetic Analysis of the vesicular fusion SNARE machinery revealing its functional divergence across Eukaryotes

  2018cites this paper
• Fungal Growth on Solid Substrates

  2018cites this paper
• Evolutionary Cell Biology of Proteins from Protists to Humans and Plants

  2018cites this paper
• SNARE-Encoding Genes VdSec22 and VdSso1 Mediate Protein Secretion Required for Full Virulence in Verticillium dahliae.

  2018cites this paper
• Seeing the endomembrane system for the trees: Evolutionary analysis highlights the importance of plants as models for eukaryotic membrane-trafficking.

  2017cites this paper
• The ubiquitin-proteasome system functionally links neuronal Tomosyn-1 to dendritic morphology

  2017cites this paper
• Evolution of the endomembrane systems of trypanosomatids – conservation and specialisation

  2017influential citation
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  2017cites this paper
• The Aspergillus nidulans syntaxin PepAPep12 is regulated by two Sec1/Munc‐18 proteins to mediate fusion events at early endosomes, late endosomes and vacuoles

  2016cites this paper
• Whole Genome Sequencing Identifies a Novel Factor Required for Secretory Granule Maturation in Tetrahymena thermophila

  2016cites this paper
• Evolution of vesicular transport in kinetoplastids: dynamics and novel gene products

  2016influential citation
• 3 Hyphal Tip Growth in Filamentous Fungi

  2016cites this paper
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  2015cites this paper
• Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi.

  2014cites this paper
• Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission

  2014cites this paper
• Molecular genetic analysis of vesicular transport in Aspergillus niger reveals partial conservation of the molecular mechanism of exocytosis in fungi.

  2014cites this paper
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  2014cites this paper
• Morphogenesis and protein production in Aspergillus niger

  2014cites this paper
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  2013cites this paper
• Genome-Wide Identification, Phylogeny and Expression Profile of Vesicle Fusion Components in Verticillium dahliae

  2013cites this paper
• The secretory pathway: exploring yeast diversity.

  2013cites this paper
• Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: structures, functions and roles in disease.

  2012cites this paper
• Growth-inhibition effects of pacifastin-like peptides on a pest insect: the desert locust, Schistocerca gregaria.

  2012cites this paper
• A perturbation in glutathione biosynthesis disrupts endoplasmic reticulum morphology and secretory membrane traffic in Arabidopsis thaliana.

  2012cites this paper
• The cargo and the transport system: secreted proteins and protein secretion in Trichoderma reesei (Hypocrea jecorina).

  2012cites this paper
• Epsin N-terminal homology domains bind on opposite sides of two SNAREs

  2011cites this paper
• Vacuole dynamics in fungi

  2010cites this paper
• The role of mVps45 in regulating GLUT4 trafficking in 3T3L1 adipocytes

  2010cites this paper
• Patterns and processes in the evolution of the eukaryotic endomembrane system

  2010influential citation
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  2010cites this paper
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  2010cites this paper
• Dissecting comimetic radiations in Heliconius reveals divergent histories of convergent butterflies

  2010cites this paper
• Astragalar morphology of Afradapis, a large adapiform primate from the earliest late Eocene of Egypt.

  2010cites this paper
• Cryptococcus neoformans and Cryptococcus gattii genes preferentially expressed during rat macrophage infection.

  2010cites this paper
• A Coiled Coil Trigger Site Is Essential for Rapid Binding of Synaptobrevin to the SNARE Acceptor Complex*

  2010cites this paper
• Genes diferencialmente expressos por Cryptococcus neoformans e Cryptococcus gattii durante a infecção de macrófagos

  2009cites this paper
• A computationally guided protein-interaction screen uncovers coiled-coil interactions involved in vesicular trafficking.

  2009cites this paper
• Evolutionary origins of the purinergic signalling system

  2009cites this paper
• Differences in the SNARE evolution of fungi and metazoa.

  2009cites this paper