Evolutionary analysis of multidrug resistance genes in fungi - Impact of gene duplication and family conservation

FEBS Journal

Volumn 281, Issue 22, 2014, Pages 4967-4977

  Gossani, Cristiani ^a   Bellieny Rabelo, Daniel ^a   Venancio, Thiago M ^a  

^a UNIVERSIDADE ESTADUAL DO NORTE FLUMINENSE DARCY RIBEIRO   (Brazil)

Author keywords

chemical genetics; drug resistance; functional divergence; multidrug resistance genes; systems biology

Indexed keywords

FUNGAL DNA;

ANTIFUNGAL RESISTANCE; DNA SEQUENCE; FUNGAL GENE; GENE; GENE DUPLICATION; GENETICS; MOLECULAR EVOLUTION; MULTIDRUG RESISTANCE; NUCLEOTIDE SEQUENCE; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; CONSERVED SEQUENCE; DNA, FUNGAL; DRUG RESISTANCE, FUNGAL; DRUG RESISTANCE, MULTIPLE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENES, FUNGAL; GENES, MDR; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA;

EID: 84910137102     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13046     Document Type: Article

References (59)

1. Kellis M, Birren BW, &, Lander ES, (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428, 617-624.
2. Wolfe KH, &, Shields DC, (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708-713.
3. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, et al,. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391.
4. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, et al,. (1999) Functional characterization of the S. Cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
5. Hillenmeyer ME, Fung E, Wildenhain J, Pierce SE, Hoon S, Lee W, Proctor M, St Onge RP, Tyers M, Koller D, et al,. (2008) The chemical genomic portrait of yeast: Uncovering a phenotype for all genes. Science 320, 362-365.
6. Parsons AB, Lopez A, Givoni IE, Williams DE, Gray CA, Porter J, Chua G, Sopko R, Brost RL, Ho CH, et al,. (2006) Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126, 611-625.
7. Venancio TM, Bellieny-Rabelo D, &, Aravind L, (2012) Evolutionary and biochemical aspects of chemical stress resistance in Saccharomyces cerevisiae. Front Gen 3, 47.
8. Venancio TM, Balaji S, Geetha S, &, Aravind L, (2010) Robustness and evolvability in natural chemical resistance: Identification of novel systems properties, biochemical mechanisms and regulatory interactions. Mol BioSyst 6, 1475-1491.
9. Engler KH, Coker R, &, Evans IH, (1999) A novel colorimetric yeast bioassay for detecting trichothecene mycotoxins. J Microbiol Methods 35, 207-218.
10. Ooi SL, Shoemaker DD, &, Boeke JD, (2003) DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat Genet 35, 277-286.
11. Parsons AB, Brost RL, Ding H, Li Z, Zhang C, Sheikh B, Brown GW, Kane PM, Hughes TR, &, Boone C, (2004) Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat Biotechnol 22, 62-69.
12. Warringer J, Ericson E, Fernandez L, Nerman O, &, Blomberg A, (2003) High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci USA 100, 15724-15729.
13. Roemer T, Davies J, Giaever G, &, Nislow C, (2012) Bugs, drugs and chemical genomics. Nat Chem Biol 8, 46-56.
14. Shoemaker DD, Lashkari DA, Morris D, Mittmann M, &, Davis RW, (1996) Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy. Nat Genet 14, 450-456.
15. Smith AM, Heisler LE, Mellor J, Kaper F, Thompson MJ, Chee M, Roth FP, Giaever G, &, Nislow C, (2009) Quantitative phenotyping via deep barcode sequencing. Genome Res 19, 1836-1842.
16. Venancio TM, Balaji S, &, Aravind L, (2010) High-confidence mapping of chemical compounds and protein complexes reveals novel aspects of chemical stress response in yeast. Mol BioSyst 6, 175-181.
17. Levy SF, &, Siegal ML, (2008) Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 6, e264.
18. Blake WJ, Balazsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, Cantor CR, Walt DR, &, Collins JJ, (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24, 853-865.
19. Basehoar AD, Zanton SJ, &, Pugh BF, (2004) Identification and distinct regulation of yeast TATA box-containing genes. Cell 116, 699-709.
20. Gabaldon T, &, Koonin EV, (2013) Functional and evolutionary implications of gene orthology. Nat Rev Genet 14, 360-366.
21. Fares MA, Keane OM, Toft C, Carretero-Paulet L, &, Jones GW, (2013) The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae genes. PLoS Genet 9, e1003176.
22. Lynch M, O'Hely M, Walsh B, &, Force A, (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159, 1789-1804.
23. Conant GC, &, Wolfe KH, (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9, 938-950.
24. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, &, Li WH, (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421, 63-66.
25. Force A, Lynch M, Pickett FB, Amores A, Yan YL, &, Postlethwait J, (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
26. He X, &, Zhang J, (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157-1164.
27. Gu Z, Nicolae D, Lu HH, &, Li WH, (2002) Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Gen 18, 609-613.
28. VanderSluis B, Bellay J, Musso G, Costanzo M, Papp B, Vizeacoumar FJ, Baryshnikova A, Andrews B, Boone C, &, Myers CL, (2010) Genetic interactions reveal the evolutionary trajectories of duplicate genes. Mol Syst Biol 6, 429.
29. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, et al,. (2010) The genetic landscape of a cell. Science 327, 425-431.
30. Litchfield DW, (2003) Protein kinase CK2: Structure, regulation and role in cellular decisions of life and death. Biochem J 369, 1-15.
31. Toczyski DP, Galgoczy DJ, &, Hartwell LH, (1997) CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90, 1097-1106.
32. Glover CV 3rd, (1998) On the physiological role of casein kinase II in Saccharomyces cerevisiae. Prog Nucleic Acid Res Mol Biol 59, 95-133.
33. Bibby AC, &, Litchfield DW, (2005) The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2beta. Int J Biol Sci 1, 67-79.
34. Brown CA, Murray AW, &, Verstrepen KJ, (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20, 895-903.
35. Novak S, Zechner-Krpan V, &, Maric V, (2004) Regulation of maltose transport and metabolism in Saccharomyces cerevisiae. Food Technol Biotech 42, 213-218.
36. Cannon RD, Lamping E, Holmes AR, Niimi K, Baret PV, Keniya MV, Tanabe K, Niimi M, Goffeau A, &, Monk BC, (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22, 291-321, Table of Contents.
37. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, &, Desai MM, (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500, 571-574.
38. Dixon DM, (2001) Coccidioides immitis as a select agent of bioterrorism. J Appl Microbiol 91, 602-605.
39. Schwarzmuller T, Ma B, Hiller E, Istel F, Tscherner M, Brunke S, Ames L, Firon A, Green B, Cabral V, et al,. (2014) Systematic phenotyping of a large-scale Candida glabrata deletion collection reveals novel antifungal tolerance genes. PLoS Pathog 10, e1004211.
40. Kapitzky L, Beltrao P, Berens TJ, Gassner N, Zhou C, Wuster A, Wu J, Babu MM, Elledge SJ, Toczyski D, et al,. (2010) Cross-species chemogenomic profiling reveals evolutionarily conserved drug mode of action. Mol Syst Biol 6, 451.
41. Oh J, Fung E, Schlecht U, Davis RW, Giaever G, St Onge RP, Deutschbauer A, &, Nislow C, (2010) Gene annotation and drug target discovery in Candida albicans with a tagged transposon mutant collection. PLoS Pathog 6, e1001140.
42. Xu D, Jiang B, Ketela T, Lemieux S, Veillette K, Martel N, Davison J, Sillaots S, Trosok S, Bachewich C, et al,. (2007) Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog 3, e92.
43. Blackman RK, Cheung-Ong K, Gebbia M, Proia DA, He S, Kepros J, Jonneaux A, Marchetti P, Kluza J, Rao PE, et al,. (2012) Mitochondrial electron transport is the cellular target of the oncology drug elesclomol. PLoS One 7, e29798.
44. Jaime MD, Lopez-Llorca LV, Conesa A, Lee AY, Proctor M, Heisler LE, Gebbia M, Giaever G, Westwood JT, &, Nislow C, (2012) Identification of yeast genes that confer resistance to chitosan oligosaccharide (COS) using chemogenomics. BMC Gen 13, 267.
45. 2-dependent DNA breaks. PLoS One 7, e36343.
46. Barreto L, Canadell D, Petrezselyova S, Navarrete C, Maresova L, Perez-Valle J, Herrera R, Olier I, Giraldo J, Sychrova H, et al,. (2011) A genomewide screen for tolerance to cationic drugs reveals genes important for potassium homeostasis in Saccharomyces cerevisiae. Eukaryot Cell 10, 1241-1250.
47. Hoon S, Gebbia M, Costanzo M, Davis RW, Giaever G, &, Nislow C, (2011) A global perspective of the genetic basis for carbonyl stress resistance. G3 (Bethesda) 1, 219-231.
48. de Castro PA, Savoldi M, Bonatto D, Barros MH, Goldman MH, Berretta AA, &, Goldman GH, (2011) Molecular characterization of propolis-induced cell death in Saccharomyces cerevisiae. Eukaryot Cell 10, 398-411.
49. Alamgir M, Erukova V, Jessulat M, Azizi A, &, Golshani A, (2010) Chemical-genetic profile analysis of five inhibitory compounds in yeast. BMC Chem Biol 10, 6.
50. Uluisik I, Kaya A, Unlu ES, Avsar K, Karakaya HC, Yalcin T, &, Koc A, (2011) Genome-wide identification of genes that play a role in boron stress response in yeast. Genomics 97, 106-111.
51. Dias PJ, Teixeira MC, Telo JP, &, Sa-Correia I, (2010) Insights into the mechanisms of toxicity and tolerance to the agricultural fungicide mancozeb in yeast, as suggested by a chemogenomic approach. OMICS 14, 211-227.
52. Byrne KP, &, Wolfe KH, (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15, 1456-1461.
53. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, et al,. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
54. Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, Young J, Berriz GF, Brost RL, Chang M, et al,. (2004) Global mapping of the yeast genetic interaction network. Science 303, 808-813.
55. Chatr-Aryamontri A, Breitkreutz BJ, Heinicke S, Boucher L, Winter A, Stark C, Nixon J, Ramage L, Kolas N, O'Donnell L, et al,. (2013) The BioGRID interaction database: 2013 update. Nucleic Acids Res 41, D816-D823.
56. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, &, Lipman DJ, (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
57. Dongen SV, (2000) Graph Clustering by Flow Simulation. PhD thesis. University of Utrecht, http://dspace.library.uu.nl/handle/1874/848.
58. Eddy SR, (2009) A new generation of homology search tools based on probabilistic inference. Genome Inform 23, 205-211.
59. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al,. (2014) Pfam: The protein families database. Nucleic Acids Res 42, D222-D230.