Hsp90s, members of the Heat Shock Protein class, protect the structure and function of proteins and play a significant task in cellular homeostasis and signal transduction. In order to determine the number of hsp90 gene copies and encoded proteins in fungal and animal lineages and through that key duplication events that this family has undergone, we collected and evaluated Hsp90 protein sequences and corresponding Expressed Sequence Tags and analyzed available genomes from various taxa. We provide evidence for duplication events affecting either single species or wider taxonomic groups. With regard to Fungi, duplicated genes have been detected in several lineages. In invertebrates, we demonstrate key duplication events in certain clades of Arthropoda and Mollusca, and a possible gene loss event in a hymenopteran family. Finally, we infer that the duplication event responsible for the two (a and b) isoforms in vertebrates occurred probably shortly after the split of Hyperoartia and Gnathostomata.

Department of Genetics Development and Molecular Biology School of Biology Faculty of Sciences Aristotle University of Thessaloniki Thessaloniki Greece ; Department of Transcriptional Regulation Institute of Molecular Genetics Prague Czech Republic

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Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C (2007) Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 81: 15–27. PubMed

Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45: 247–255. PubMed

Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the Heat Shock Response and Protein Chaperones: Budding Yeast (Saccharomyces cerevisiae) as a Model System. Microbiol Mol Biol Rev 76: 115–158. PubMed PMC

Jackson SE (2013) Hsp90: Structure and Function. In: Jackson SE, editor. Molecular Chaperones. Berlin Heidelberg: Springer-Verlag, 155–240.

Zuehlke A, Johnson JL (2010) Hsp90 and co-chaperones twist the functions of diverse client proteins. Biopolymers 93: 211–217. PubMed PMC

Pearl LH, Prodromou C, Workman P (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410: 439–453. PubMed

Hartson SD, Matts RL (2012) Approaches for defining the Hsp90-dependent proteome. Biochim Biophys Acta – Molecular Cell Research 1823: 656–667. PubMed PMC

Echeverrí­a PC, Bernthaler A, Dupuis P, Mayer B, Picard D (2011) An Interaction Network Predicted from Public Data as a Discovery Tool: Application to the Hsp90 Molecular Chaperone Machine. PLoS ONE 6: e26044. PubMed PMC

Brown MA, Zhu L, Schmidt C, Tucker PW (2007) Hsp90-From signal transduction to cell transformation. Biochem Biophys Res Commun 363: 241–246. PubMed PMC

Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5: 761–772. PubMed

Trepel J, Mollapour M, Giaccone G, Neckers L (2010) Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10: 537–549. PubMed PMC

Bardwell JC, Craig EA (1988) Ancient heat shock gene is dispensable. J Bacteriol 170: 2977–2983. PubMed PMC

Versteeg S, Mogk A, Schumann W (1999) The Bacillus subtilis htpG gene is not involved in thermal stress management. Mol Genet Genomics 261: 582–588. PubMed

Laksanalamai P, Whitehead TA, Robb FT (2004) Minimal protein-folding systems in hyperthermophilic archaea. Nat Rev Microbiol 2: 315–324. PubMed

Gupta RS (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol Biol Evol 12: 1063–1073. PubMed

Csermely P, Schnaider T, Soti C, Prohászka Z, Nardai G (1998) The 90-kDa molecular chaperone family: Structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 79: 129–168. PubMed

Emelyanov VV (2002) Phylogenetic relationships of organellar Hsp90 homologs reveal fundamental differences to organellar Hsp70 and Hsp60 evolution. Gene 299: 125–133. PubMed

Chen B, Zhong D, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7: 156. PubMed PMC

Chen B, Piel WH, Gui L, Bruford E, Monteiro A (2005) The HSP90 family of genes in the human genome: Insights into their divergence and evolution. Genomics 86: 627–637. PubMed

Moore SK, Kozak C, Robinson EA, Ullrich SJ, Appella E (1989) Murine 86- and 84-kDa heat shock proteins, cDNA sequences, chromosome assignments, and evolutionary origins. J Biol Chem 264: 5343–5351. PubMed

Krone PH, Sass JB (1994) Hsp90α and hsp90β genes are present in the zebrafish and are differentially regulated in developing embryos. Biochem Biophys Res Commun 204: 746–752. PubMed

Konstantopoulou I, Scouras ZG (1998) The Heat-Shock Gene hsp83 of Drosophila auraria: Genomic Organization, Nucleotide Sequence, and Long Antiparallel Coupled ORFs (LAC ORFs). J Mol Evol 46: 334–343. PubMed

Birnby DA, Link EM, Vowels JJ, Tian H, Colacurcio PL, et al. (2000) A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans . Genetics 155: 85–104. PubMed PMC

Inoue T, Takamura K, Yamae H, Ise N, Kawakami M, et al. (2003) Caenorhabditis elegans DAF-21 (HSP90) is characteristically and predominantly expressed in germline cells: Spatial and temporal analysis. Dev Growth Differ 45: 369–376. PubMed

Thompson FJ, Cockroft AC, Wheatley I, Britton C, Devaney E (2001) Heat shock and developmental expression of hsp83 in the filarial nematode Brugia pahangi . Eur J Biochem 268: 5808–5815. PubMed

Benedict MQ, Levine BJ, Ke ZX, Cockburn AF, Seawright JA (1996) Precise limitation of concerted evolution to ORFs in mosquito Hsp82 genes. Insect Mol Biol 5: 73–79. PubMed

Pantzartzi CN, Kourtidis A, Drosopoulou E, Yiangou M, Scouras ZG (2009) Isolation and characterization of two cytoplasmic hsp90s from Mytilus galloprovincialis (Mollusca: Bivalvia) that contain a complex promoter with a p53 binding site. Gene 431: 47–54. PubMed

Zhang XY, Zhang MZ, Zheng CJ, Liu J, Hu HJ (2009) Identification of two hsp90 genes from the marine crab, Portunus trituberculatus and their specific expression profiles under different environmental conditions. Comp Biochem Physiol C Toxicol Pharmacol 150: 465–473. PubMed

Minchiotti G, Gargano S, Maresca B (1991) The intron-containing hsp82 gene of the dimorphic pathogenic fungus Histoplasma capsulatum is properly spliced in severe heat shock conditions. Mol Cell Biol 11: 5624–5630. PubMed PMC

Swoboda RK, Bertram G, Budge S, Gooday GW, Gow NAR, et al. (1995) Structure and regulation of the HSP90 gene from the pathogenic fungus Candida albicans . Infect Immun 63: 4506–4514. PubMed PMC

Pugliese L, Georg RC, Fietto LG, Gomes SL (2008) Expression of genes encoding cytosolic and endoplasmic reticulum HSP90 proteins in the aquatic fungus Blastocladiella emersonii . Gene 411: 59–68. PubMed

Farrelly FW, Finkelstein DB (1984) Complete sequence of the heat shock-inducible HSP90 gene of Saccharomyces cerevisiae . J Biol Chem 259: 5745–5751. PubMed

Erkine AM, Adams CC, Gao M, Gross DS (1995) Multiple protein-DNA interactions over the yeast HSC82 heat shock gene promoter. Nucleic Acids Res 23: 1822–1829. PubMed PMC

Erkine AM, Magrogan SF, Sekinger EA, Gross DS (1999) Cooperative binding of heat shock factor to the yeast HSP82 promoter in vivo and in vitro . Mol Cell Biol 19: 1627–1639. PubMed PMC

Maere S, Van de Peer Y (2010) Duplicate retention After Small- and Large-Scale Duplications. In: Dittmar K, Liberles D, editors. Evolution after gene duplication. Hoboken, New Jersey: Wiley-Blackwell, 31–56.

Bergthorsson U, Andersson DI, Roth JR (2007) Ohno's dilemma: Evolution of new genes under continuous selection. Proc Natl Acad Sci U S A 104: 17004–17009. PubMed PMC

Gao Q, Zhao J, Song L, Qiu L, Yu Y, et al. (2008) Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians . Fish Shellfish Immunol 24: 379–385. PubMed

Gao Q, Song L, Ni D, Wu L, Zhang H, et al. (2007) cDNA cloning and mRNA expression of heat shock protein 90 gene in the haemocytes of Zhikong scallop Chlamys farreri . Comp Biochem Physiol B Biochem Mol Biol 147: 704–715. PubMed

Wu LT, Chu KH (2008) Characterization of heat shock protein 90 in the shrimp Metapenaeus ensis: Evidence for its role in the regulation of vitellogenin synthesis. Mol Reprod Dev 75: 952–959. PubMed

Echeverrí a PC, Matrajt M, Harb OS, Zappia MP, Costas MA, et al. (2005) Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. J Mol Biol 350: 723–734. PubMed

Gupta RS (1998) Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62: 1435–1491. PubMed PMC

Stechmann A, Cavalier-Smith T (2003) Phylogenetic Analysis of Eukaryotes Using Heat-Shock Protein Hsp90. J Mol Evol 57: 408–419. PubMed

Stechmann A, Cavalier-Smith T (2004) Evolutionary Origins of Hsp90 Chaperones and a Deep Paralogy in their Bacterial Ancestors. J Eukaryot Microbiol 51: 364–373. PubMed

Magrane M, Consortium U (2011) UniProt Knowledgebase: a hub of integrated protein data. Database (Oxford) 2011: bar009. PubMed PMC

Galperin MY, Fernández-Suárez XM (2012) The 2012 Nucleic Acids Research Database Issue and the online Molecular Biology Database Collection. Nucleic Acids Res 40: D1–D8. PubMed PMC

Sigrist CJA, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, et al. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38: D161–D166. PubMed PMC

Suen G, Teiling C, Li L, Holt C, Abouheif E, et al. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet 7: e1002007. PubMed PMC

Gauthier J, Legeai F, Zasadzinski A, Rispe C, Tagu D (2007) AphidBase: a database for aphid genomic resources. Bioinformatics 23: 783–784. PubMed

Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, et al. (2009) VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Res 37: D583–D587. PubMed PMC

Kersey PJ, Staines DM, Lawson D, Kulesha E, Derwent P, et al. (2012) Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res 40: D91–D97. PubMed PMC

Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, et al. (2012) GenBank. Nucleic Acids Res 40: D48–D53. PubMed PMC

Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al. (2012) The Genome Portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26–D32. PubMed PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. PubMed

Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268: 78–94. PubMed

Rogozin IB, Milanesi L (1997) Analysis of donor splice sites in different eukaryotic organisms. J Mol Evol 45: 50–59. PubMed

Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, et al. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38: W695–W699. PubMed PMC

Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16: 276–277. PubMed

Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680. PubMed PMC

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. PubMed

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop, GCE 2010. 10.1109/GCE.2010.5676129. 25 June 2013.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. PubMed PMC

Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 17: 368–376. PubMed

Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791. PubMed

Nakao Y, Kanamori T, Itoh T, Kodama Y, Rainieri S, et al. (2009) Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Res 16: 115–129. PubMed PMC

Langkjær RB, Cliften PF, Johnston M, Piškur J (2003) Yeast genome duplication was followed by asynchronous differentiation of duplicated genes. Nature 421: 848–852. PubMed

Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae . Nature 428: 617–624. PubMed

Van Hoek MJA, Hogeweg P (2009) Metabolic adaptation after whole genome duplication. Mol Biol Evol 26: 2441–2453. PubMed

Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708–713. PubMed

Nardi T, Remize F, Alexandre H (2010) Adaptation of yeasts Saccharomyces cerevisiae and Brettanomyces bruxellensis to winemaking conditions: A comparative study of stress genes expression. Appl Microbiol Biotechnol 88: 925–937. PubMed

Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54–61. PubMed

Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, et al. (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet 5: e1000549. PubMed PMC

Xu PJ, Xiao JH, Xia QY, Murphy B, Huang DW (2010) Apis mellifera has two isoforms of cytoplasmic HSP90. Insect Mol Biol 19: 593–597. PubMed

Zhao L, Jones WA (2012) Expression of heat shock protein genes in insect stress responses. Invertebrate Surviv J 9: 93–101.

Benoit JB, Lopez-Martinez G, Phillips ZP, Patrick KR, Denlinger DL (2010) Heat shock proteins contribute to mosquito dehydration tolerance. J Insect Physiol 56: 151–156. PubMed PMC

Sinclair BJ, Gibbs AG, Roberts SP (2007) Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster . Insect Mol Biol 16: 435–443. PubMed

Spassky B, Richmond RC, Pérez-Salas S, Pavlovsky O, Mourão CA, et al. (1971) Geography of the sibling species related to Drosophila willistoni, and the semi-species of the Drosophila paulistorum complex. Evolution 25: 129–143. PubMed

Parsons PA (1991) Evolutionary Rates: Stress and Species Boundaries. Annu Rev Ecol Syst 22: 1–18.

Aamodt RM (2008) The caste- and age-specific expression signature of honeybee heat shock genes shows an alternative splicing-dependent regulation of Hsp90. Mech Ageing Dev 129: 632–637. PubMed

Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128: 13–34.

Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: Insights from argentine ants. Proc Natl Acad Sci U S A 98: 1095–1100. PubMed PMC

Smith CD, Zimin A, Holt C, Abouheif E, Benton R, et al. (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci U S A 108: 5673–5678. PubMed PMC

Long M, Betrán E, Thornton K, Wang W (2003) The origin of new genes: Glimpses from the young and old. Nat Rev Gen 4: 865–875. PubMed

Kidwell MG, Lisch DR (2001) Perspective: Transposable elements, parasitic DNA, and genome evolution. Evolution 55: 1–24. PubMed

Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63. PubMed

Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, et al. (2005) Combined Evidence Annotation of Transposable Elements in Genome Sequences. PLoS Comput Biol 1: e22. PubMed PMC

Sassi AK, Herédia F, Loreto EL, Valente VL, Rohde C (2005) Transposable elements P and gypsy in natural populations of Drosophila willistoni . Genet Mol Biol 28: 734–739.

Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218. PubMed

Zdobnov EM, Von Mering C, Letunic I, Torrents D, Suyama M, et al. (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster . Science 298: 149–159. PubMed

Holt RA, Subramanian MG, Halpern A, Sutton GG, Charlab R, et al. (2002) The Genome Sequence of the Malaria Mosquito Anopheles gambiae . Science 298: 129–149. PubMed

Nene V, Wortman JR, Lawson D, Haas B, Kodira C, et al. (2007) Genome Sequence of Aedes aegypti, a Major Arbovirus Vector. Science 316: 1718–1723. PubMed PMC

Pantzartzi C, Drosopoulou E, Yiangou M, Drozdov I, Tsoka S, et al.. (2010) Promoter complexity and tissue-specific expression of stress response components in Mytilus galloprovincialis, a sessile marine invertebrate species. PLoS Comput Biol 6. PubMed PMC

Yoshida MA, Ishikura Y, Moritaki T, Shoguchi E, Shimizu KK, et al. (2011) Genome structure analysis of molluscs revealed whole genome duplication and lineage specific repeat variation. Gene 483: 63–71. PubMed

Van de Peer Y (2004) Tetraodon genome confirms Takifugu findings: Most fish are ancient polyploids. Genome Biol 5: 250. PubMed PMC

Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, et al. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946–957. PubMed

Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U, et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071. PubMed

Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez È, Blow MJ, et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18: 1100–1111. PubMed PMC

Edger PP, Pires JC (2009) Gene and genome duplications: The impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res 17: 699–717. PubMed