Generators of Phenotypic Diversity in the Evolution of Pathogenic Microorganisms

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Calo, Silvia ^a   Billmyre, R Blake ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 90; PRION PROTEIN;

ANEUPLOIDY; ARTICLE; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CRYPTOCOCCUS NEOFORMANS; EVOLUTION; HUMAN; MICROBIAL DIVERSITY; NONHUMAN; PHENOTYPE; PRION; PSEUDOMONAS AERUGINOSA; REPRODUCTION; SACCHAROMYCES CEREVISIAE; TELOMERE;

ADAPTATION, BIOLOGICAL; BACTERIA; BIODIVERSITY; EVOLUTION, MOLECULAR; FUNGI; GENETIC VARIATION; PHENOTYPE; REPRODUCTION;

EID: 84875991011     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003181     Document Type: Article

References (43)

1. Rutherford SL, Lindquist S, (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
2. Queitsch C, Sangster TA, Lindquist S, (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
3. Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Brenière SF, et al. (1991) Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci U S A 88: 5129-5133.
4. Tibayrenc M, Kjellberg F, Ayala FJ, (1990) A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proc Natl Acad Sci U S A 87: 2414-2418.
5. Heitman J, (2006) Sexual reproduction and the evolution of microbial pathogens. Curr Biol 16: R711-725.
6. Heitman J, (2010) Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8: 86-99.
7. Pontecorvo G, (1956) The parasexual cycle in fungi. Annu Rev Microbiol 10: 393-400.
8. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, et al. (2008) The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6: e110 doi:10.1371/journal.pbio.0060110.
9. Schoustra SE, Debets AJM, Slakhorst M, Hoekstra RF, (2007) Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLoS Genet 3: e68 doi:10.1371/journal.pgen.0030068.
10. Lin X, Hull CM, Heitman J, (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434: 1017-1021.
11. Alby K, Schaefer D, Bennett RJ, (2009) Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890-893.
12. Poxleitner MK, Carpenter ML, Mancuso JJ, Wang CJ, Dawson SC, et al. (2008) Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science 319: 1530-1533.
13. Wendte JM, Miller MA, Lambourn DM, Magargal SL, Jessup DA, et al. (2010) Self-mating in the definitive host potentiates clonal outbreaks of the apicomplexan parasites Sarcocystis neurona and Toxoplasma gondii. PLoS Genet 6: e1001261 doi:10.1371/journal.pgen.1001261.
14. Selmecki A, Forche A, Berman J, (2006) Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367-370.
15. Sionov E, Lee H, Chang YC, Kwon-Chung KJ, (2010) Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog 6: e1000848 doi:10.1371/journal.ppat.1000848.
16. Rancati G, Pavelka N, Fleharty B, Noll A, Trimble R, et al. (2008) Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 5: 879-893.
17. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, et al. (2007) Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
18. Torres EM, Dephoure N, Panneerselvam A, Tucker CM, Whittaker CA, et al. (2010) Identification of aneuploidy-tolerating mutations. Cell 143: 71-83.
19. Mannaert A, Downing T, Imamura H, Dujardin JC, (2012) Adaptive mechanisms in pathogens: universal aneuploidy in Leishmania. Trends Parasitol 28: 370-376.
20. Ubeda JM, Légaré D, Raymond F, Ouameur AA, Boisvert S, et al. (2008) Modulation of gene expression in drug resistant Leishmania is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol 9: R115.
21. Sterkers Y, Lachaud L, Bourgeois N, Crobu L, Bastien P, et al. (2012) Novel insights into genome plasticity in eukaryotes: mosaic aneuploidy in Leishmania. Mol Microbiol 86: 15-23.
22. Jarosz DF, Lindquist S, (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330: 1820-1824.
23. Cowen LE, Lindquist S, (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
24. Wickner RB, (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264: 566-569.
25. Kelly AC, Shewmaker FP, Kryndushkin D, Wickner RB, (2012) Sex, prions, and plasmids in yeast. Proc Natl Acad Sci U S A 109: E2683-2690.
26. True HL, Lindquist S, (2000) A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407: 477-483.
27. True HL, Berlin I, Lindquist SL, (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431: 184-187.
28. Halfmann R, Lindquist S, (2010) Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330: 629-632.
29. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, et al. (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
30. Hovel-Miner GA, Boothroyd CE, Mugnier M, Dreesen O, Cross GAM, et al. (2012) Telomere length affects the frequency and mechanism of antigenic variation in Trypanosoma brucei. PLoS Pathog 8: e1002900 doi:10.1371/journal.ppat.1002900.
31. De Las Peñas A, Pan S-J, Castaño I, Alder J, Cregg R, et al. (2003) Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev17: 2245-2258.
32. Farman ML, (2007) Telomeres in the rice blast fungus Magnaporthe oryzae: the world of the end as we know it. FEMS Microbiol Lett 273: 125-132.
33. Starnes JH, Thornbury DW, Novikova OS, Rehmeyer CJ, Farman ML, (2012) Telomere-targeted retrotransposons in the rice blast fungus Magnaporthe oryzae: agents of telomere instability. Genetics 191: 389-406.
34. Fijalkowska IJ, Dunn RL, Schaaper RM, (1997) Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J Bacteriol 179: 7435-7445.
35. Ninio J, (1991) Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics 129: 957-962.
36. Oliver A, Canton R, Campo P, Baquero F, Blazquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1253.
37. Strand M, Prolla TA, Liskay RM, Petes TD, (1993) Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365: 274-276.
38. Verstrepen KJ, Jansen A, Lewitter F, Fink GR, (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
39. Levdansky E, Romano J, Shadkchan Y, Sharon H, Verstrepen KJ, et al. (2007) Coding tandem repeats generate diversity in Aspergillus fumigatus genes. Eukaryot Cell 6: 1380-1391.
40. Magditch DA, Liu T-B, Xue C, Idnurm A, (2012) DNA mutations mediate microevolution between host-adapted forms of the pathogenic fungus Cryptococcus neoformans. PLoS Pathog 8: e1002936 doi:10.1371/journal.ppat.1002936.
41. Fishel R, Lescoe MK, Rao MR, Copeland NG, Jenkins NA, et al. (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75: 1027-1038.
42. Parsons R, Li GM, Longley MJ, Fang WH, Papadopoulos N, et al. (1993) Hypermutability and mismatch repair deficiency in RER+ tumor cells. Cell 75: 1227-1236.
43. Drake JW, Bebenek A, Kissling GE, Peddada S, (2005) Clusters of mutations from transient hypermutability. Proc Natl Acad Sci U S A 102: 12849-12854.