Frequent Assembly of Chimeric Complexes in the Protein Interaction Network of an Interspecies Yeast Hybrid

Hybrids between species often show extreme phenotypes, including some that take place at the molecular level. In this study, we investigated the phenotypes of an interspecies diploid hybrid in terms of protein-protein interactions inferred from protein correlation profiling. We used two yeast species, Saccharomyces cerevisiae and Saccharomyces uvarum, which are interfertile, but yet have proteins diverged enough to be differentiated using mass spectrometry. Most of the protein-protein interactions are similar between hybrid and parents, and are consistent with the assembly of chimeric complexes, which we validated using an orthogonal approach for prefoldin complex. We also identify instances of altered protein-protein interactions in the hybrid, for instance in complexes related to proteostasis and in mitochondrial protein complexes. Overall, this study uncovers likely frequent occurrence of chimeric protein complexes with few exceptions, which may result from incompatibilities or imbalances between the parental proteins.

[1]  I. Dunham,et al.  Rapid assessment of S. cerevisiae mating type by PCR. , 1990, Trends in genetics : TIG.

[2]  F. Maytag Evolution , 1996, Arch. Mus. Informatics.

[3]  L. Rieseberg,et al.  Transgressive segregation, adaptation and speciation , 1999, Heredity.

[4]  G. Church,et al.  Correlation between transcriptome and interactome mapping data from Saccharomyces cerevisiae , 2001, Nature Genetics.

[5]  R. Ozawa,et al.  A comprehensive two-hybrid analysis to explore the yeast protein interactome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. Mann,et al.  Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. , 2003, Analytical chemistry.

[7]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[8]  Nichole L. King,et al.  The PeptideAtlas Project , 2010, Proteome Bioinformatics.

[9]  Hye-Jung E. Chun,et al.  Genomic Convergence toward Diploidy in Saccharomyces cerevisiae , 2006, PLoS genetics.

[10]  Eric W. Deutsch,et al.  The PeptideAtlas project , 2005, Nucleic Acids Res..

[11]  Sean R. Collins,et al.  Global landscape of protein complexes in the yeast Saccharomyces cerevisiae , 2006, Nature.

[12]  A. Querol,et al.  Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. , 2006, FEMS yeast research.

[13]  D. Hartl,et al.  Genome clashes in hybrids: insights from gene expression , 2007, Heredity.

[14]  C. Landry,et al.  An in Vivo Map of the Yeast Protein Interactome , 2008, Science.

[15]  M. Mann,et al.  MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification , 2008, Nature Biotechnology.

[16]  J. Leu,et al.  Incompatibility of Nuclear and Mitochondrial Genomes Causes Hybrid Sterility between Two Yeast Species , 2008, Cell.

[17]  S. Bottani,et al.  Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. , 2008, Trends in genetics : TIG.

[18]  D. Greig Reproductive isolation in Saccharomyces , 2009, Heredity.

[19]  Rachael P. Huntley,et al.  QuickGO: a web-based tool for Gene Ontology searching , 2009, Bioinform..

[20]  Naama Barkai,et al.  Divergence of nucleosome positioning between two closely related yeast species: genetic basis and functional consequences , 2010, Molecular systems biology.

[21]  C. Landry,et al.  A toolkit of protein-fragment complementation assays for studying and dissecting large-scale and dynamic protein-protein interactions in living cells. , 2010, Methods in enzymology.

[22]  S. Maheshwari,et al.  The genetics of hybrid incompatibilities. , 2011, Annual review of genetics.

[23]  Michael B. Eisen,et al.  The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus , 2011, G3: Genes | Genomes | Genetics.

[24]  A. Kristjuhan,et al.  Extraction of genomic DNA from yeasts for PCR-based applications. , 2011, BioTechniques.

[25]  Naama Barkai,et al.  Inferring regulatory mechanisms from patterns of evolutionary divergence , 2011, Molecular systems biology.

[26]  L. Foster,et al.  A high-throughput approach for measuring temporal changes in the interactome , 2012, Nature Methods.

[27]  Robert P. St.Onge,et al.  Multiplex assay for condition-dependent changes in protein–protein interactions , 2012, Proceedings of the National Academy of Sciences.

[28]  Andrei L. Turinsky,et al.  A Census of Human Soluble Protein Complexes , 2012, Cell.

[29]  Edith D. Wong,et al.  Saccharomyces Genome Database: the genomics resource of budding yeast , 2011, Nucleic Acids Res..

[30]  B. Dujon,et al.  Evolutionary Role of Interspecies Hybridization and Genetic Exchanges in Yeasts , 2012, Microbiology and Molecular Reviews.

[31]  Alexandre K. Dubé,et al.  Evidence for the Robustness of Protein Complexes to Inter-Species Hybridization , 2012, PLoS genetics.

[32]  Eitan Rubin,et al.  Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility , 2012, Proceedings of the National Academy of Sciences.

[33]  Amparo Querol,et al.  Metabolomic Comparison of Saccharomyces cerevisiae and the Cryotolerant Species S. bayanus var. uvarum and S. kudriavzevii during Wine Fermentation at Low Temperature , 2013, PloS one.

[34]  T. Walther,et al.  Native SILAC: Metabolic Labeling of Proteins in Prototroph Microorganisms Based on Lysine Synthesis Regulation* , 2013, Molecular & Cellular Proteomics.

[35]  D. Delneri,et al.  Chimeric Protein Complexes in Hybrid Species Generate Novel Phenotypes , 2012, PLoS genetics.

[36]  C. Landry,et al.  qPCA: a scalable assay to measure the perturbation of protein-protein interactions in living cells. , 2013, Molecular bioSystems.

[37]  O. Griffith,et al.  SGD (Saccharomyces Genome Database) , 2014 .

[38]  C. Landry,et al.  Chromosomal variation segregates within incipient species and correlates with reproductive isolation , 2014, Molecular ecology.

[39]  Gemma E. May,et al.  Ribosome profiling reveals post-transcriptional buffering of divergent gene expression in yeast , 2013, Genome research.

[40]  Leonard J Foster,et al.  Protein correlation profiling-SILAC to study protein-protein interactions. , 2014, Methods in molecular biology.

[41]  S. Michnick,et al.  High-resolution mapping of protein concentration reveals principles of proteome architecture and adaptation. , 2014, Cell reports.

[42]  L. Parts,et al.  gitter: A Robust and Accurate Method for Quantification of Colony Sizes From Plate Images , 2014, G3: Genes, Genomes, Genetics.

[43]  Edmond J. Breen,et al.  Linking structural features of protein complexes and biological function , 2015, Protein science : a publication of the Protein Society.

[44]  Austin G. Meyer,et al.  Systematic humanization of yeast genes reveals conserved functions and genetic modularity , 2015, Science.

[45]  K. Verstrepen,et al.  A Large Set of Newly Created Interspecific Saccharomyces Hybrids Increases Aromatic Diversity in Lager Beers , 2015, Applied and Environmental Microbiology.

[46]  Nichollas E. Scott,et al.  Development of a computational framework for the analysis of protein correlation profiling and spatial proteomics experiments. , 2015, Journal of proteomics.

[47]  Damian Szklarczyk,et al.  Version 4.0 of PaxDb: Protein abundance data, integrated across model organisms, tissues, and cell‐lines , 2015, Proteomics.

[48]  Yosvany López,et al.  HitPredict version 4: comprehensive reliability scoring of physical protein–protein interactions from more than 100 species , 2015, Database J. Biol. Databases Curation.

[49]  P. Sulo,et al.  Post-zygotic sterility and cytonuclear compatibility limits in S. cerevisiae xenomitochondrial cybrids , 2015, Front. Genet..

[50]  Albert-László Barabási,et al.  An inter‐species protein–protein interaction network across vast evolutionary distance , 2016, Molecular systems biology.

[51]  G. Bell,et al.  Speciation driven by hybridization and chromosomal plasticity in a wild yeast , 2015, Nature Microbiology.

[52]  Jüergen Cox,et al.  The MaxQuant computational platform for mass spectrometry-based shotgun proteomics , 2016, Nature Protocols.

[53]  C. Landry,et al.  Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae , 2016, Genome biology and evolution.

[54]  D. Greig,et al.  Heterosis in hybrids within and between yeast species , 2017, Journal of evolutionary biology.

[55]  Nicholas T. Ingolia,et al.  Post-Translational Dosage Compensation Buffers Genetic Perturbations to Stoichiometry of Protein Complexes , 2017, PLoS genetics.

[56]  Isabelle Gagnon-Arsenault,et al.  Gene duplication can impart fragility, not robustness, in the yeast protein interaction network , 2017, Science.

[57]  No evidence for extrinsic post-zygotic isolation in a wild Saccharomyces yeast system , 2017, Biology Letters.

[58]  Chang Liu,et al.  Altered chromatin compaction and histone methylation drive non-additive gene expression in an interspecific Arabidopsis hybrid , 2017, Genome Biology.

[59]  N. Barkai,et al.  Hybrid vigor: The best of both parents, or a genomic clash? , 2017 .

[60]  Isabelle Gagnon-Arsenault,et al.  Extended Linkers Improve the Detection of Protein-protein Interactions (PPIs) by Dihydrofolate Reductase Protein-fragment Complementation Assay (DHFR PCA) in Living Cells* , 2017, Molecular & Cellular Proteomics.

[61]  Kara Dolinski,et al.  The BioGRID interaction database: 2017 update , 2016, Nucleic Acids Res..

[62]  Gene-Wei Li,et al.  Production of Protein-Complex Components Is Stoichiometric and Lacks General Feedback Regulation in Eukaryotes. , 2018, Cell systems.

[63]  Leonard J Foster,et al.  Genomic data integration systematically biases interactome mapping , 2018, PLoS Comput. Biol..

[64]  wannesm wannesm/dtaidistance: v1.0.1 , 2018 .

[65]  Xueying Guan,et al.  LncRNAs in polyploid cotton interspecific hybrids are derived from transposon neofunctionalization , 2018, Genome Biology.

[66]  Ben Lehner,et al.  The genetic landscape of a physical interaction , 2018, eLife.

[67]  John R Yates,et al.  Increased proteomic complexity in Drosophila hybrids during development , 2018, Science Advances.

[68]  K. Krogerus,et al.  A Unique Saccharomyces cerevisiae × Saccharomyces uvarum Hybrid Isolated From Norwegian Farmhouse Beer: Characterization and Reconstruction , 2018, Front. Microbiol..

[69]  Damian Szklarczyk,et al.  STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets , 2018, Nucleic Acids Res..

[70]  Recombining Your Way Out of Trouble: The Genetic Architecture of Hybrid Fitness under Environmental Stress , 2019, Molecular biology and evolution.

[71]  The Gene Ontology Consortium,et al.  The Gene Ontology Resource: 20 years and still GOing strong , 2018, Nucleic Acids Res..

[72]  Martin Eisenacher,et al.  The PRIDE database and related tools and resources in 2019: improving support for quantification data , 2018, Nucleic Acids Res..

[73]  Henning Hermjakob,et al.  Complex Portal 2018: extended content and enhanced visualization tools for macromolecular complexes , 2018, Nucleic Acids Res..

[74]  James C. Hu,et al.  The Gene Ontology Resource: 20 years and still GOing strong , 2019 .

[75]  Multiplex-Assay , 2019, Springer Reference Medizin.