Quantitative trait locus (qtl) mapping reveals a role for unstudied genes in aspergillus virulence

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Christians, Julian K ^a   Cheema, Manjinder S ^a   Vergara, Ismael A ^a   Watt, Cortney A ^a   Pinto, Linda J ^a   Chen, Nansheng ^a   Moore, Margo M ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD LARVA; ARTICLE; ASPERGILLUS NIDULANS; CHROMOSOME 5; CHROMOSOME INVERSION; CONTROLLED STUDY; DNA BASE COMPOSITION; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; GALLERIA MELLONELLA; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC DISTANCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME SIZE; GENOTYPE; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; LINKAGE ANALYSIS; MOTH; NONHUMAN; PROGENY; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; ASPERGILLUS; BIOLOGICAL MODEL; CHROMOSOME MAP; CROSS BREEDING; GENETIC LINKAGE; GENETICS; MICROBIOLOGY; PATHOGENICITY; QUANTITATIVE TRAIT LOCUS; VIRULENCE;

ANIMALIA; ASPERGILLUS; FUNGI; GALLERIA MELLONELLA; LEPIDOPTERA;

ANIMALS; ASPERGILLUS; CHROMOSOME MAPPING; CROSSES, GENETIC; GENETIC LINKAGE; GENOTYPE; LOD SCORE; MODELS, GENETIC; MOTHS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RECOMBINATION, GENETIC; VIRULENCE;

EID: 79955778824     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019325     Document Type: Article

References (74)

1. Perfect JR, Cox GM, Lee JY, Kauffman CA, de Repentigny L, et al. (2001) The impact of culture isolation of Aspergillus species: A hospital-based survey of aspergillosis. Clin Infect Dis 33: 1824-1833.
2. Singh N, Pursell KJ, (2008) Combination therapeutic approaches for the management of invasive aspergillosis in organ transplant recipients. Mycoses 51: 99-108.
3. Munoz P, Singh N, Bouza E, (2006) Treatment of solid organ transplant patients with invasive fungal infections: should a combination of antifungal drugs be used? Curr Opin Infect Dis 19: 365-370.
4. Brakhage AA, (2005) Systemic fungal infections caused by Aspergillus species: Epidemiology, infection process and virulence determinants. Curr Drug Targets 6: 875-886.
5. Latge JP, (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
6. Perfect JR, Casadevall A, (2006) Fungal Molecular Pathogenesis: What Can It Do and Why Do We Need It? In: Heitman J, Filler SG, Edwards JE, Mitchell AP, editors. Molecular Principles of Fungal Pathogenesis Washington, DC ASM Press pp. 3-12.
7. Hohl TM, Feldmesser M, (2007) Aspergillus fumigatus: principles of pathogenesis and host defense. Eukaryot Cell 6: 1953-1963.
8. Keller NP, (2006) Aspergillus nidulans: a Model for Elucidation of Aspergillus fumigatus Secondary Metabolism. In: Heitman J, Filler SG, Edwards JE, Mitchell AP, editors. Molecular Principles of Fungal Pathogenesis Washington, DC ASM Press pp. 235-244.
9. Latge JP, (2001) The pathobiology of Aspergillus fumigatus. Trends Microbiol 9: 382-389.
10. Wasylnka JA, Moore MM, (2000) Adhesion of Aspergillus species to extracellular matrix proteins: Evidence for involvement of negatively charged carbohydrates on the conidial surface. Infect Immun 68: 3377-3384.
11. Wasylnka JA, Simmer MI, Moore MM, (2001) Differences in sialic acid density in pathogenic and non-pathogenic Aspergillus species. Microbiology 147: 869-877.
12. Blanco JL, Hontecillas R, Bouza E, Blanco I, Pelaez T, et al. (2002) Correlation between the elastase activity index and invasiveness of clinical isolates of Aspergillus fumigatus. J Clin Microbiol 40: 1811-1813.
13. Kothary MH, Chase T, Macmillan JD, (1984) Correlation of elastase production by some strains of Aspergillus fumigatus with ability to cause pulmonary invasive aspergillosis in mice. Infect Immun 43: 320-325.
14. Pastor A, Gafa V, Boutonnat J, Grillot R, Ambroise-Thomas P, et al. (2006) Intracellular oxidative response of human monocytes and granulocytes to different strains of Aspergillus fumigatus. Mycoses 49: 73-79.
15. Reeves EP, Messina CGM, Doyle S, Kavanagh K, (2004) Correlation between gliotoxin production and virulence of Aspergillus fumigatus in Galleria mellonella. Mycopathologia 158: 73-79.
16. Steinmetz LM, Sinha H, Richards DR, Spiegelman JI, Oefner PJ, et al. (2002) Dissecting the architecture of a quantitative trait locus in yeast. Nature 416: 326-330.
17. Lin XR, Huang JC, Mitchell TG, Heitman J, (2006) Virulence attributes and hyphal growth of C. neoformans are quantitative traits and the MAT alpha allele enhances filamentation. PLoS Genet 2: 1801-1814.
18. O'Gorman CM, Fuller HT, Dyer PS, (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471-474.
19. Araujo R, Pina-Vaz C, Rodrigues AG, (2007) Susceptibility of environmental versus clinical strains of pathogenic Aspergillus. Int J Antimicrob Ag 29: 108-111.
20. Kontoyiannis DP, Lewis RE, May GS, Osherov N, Rinaldi MG, (2002) Aspergillus nidulans is frequently resistant to amphotericin B. Mycoses 45: 406-407.
21. Akpogheneta O, Gil-Lamaignere C, Maloukou A, Roilides E, (2003) Antifungal activity of human polymorphonuclear and mononuclear phagocytes against non-fumigatus Aspergillus species. Mycoses 46: 77-83.
22. Segal BH, DeCarlo ES, Kwon-Chung KJ, Malech HL, Gallin JI, et al. (1998) Aspergillus nidulans infection in chronic granulomatous disease. Medicine 77: 345-354.
23. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
24. Mylonakis E, Casadevall A, Ausubel FM, (2007) Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog 3: 859-865.
25. Chamilos G, Bignell EM, Schrettl M, Lewis RE, Leventakos K, et al. (2010) Exploring the concordance of Aspergillus fumigatus pathogenicity in mice and Toll-deficient flies. Med Mycol 48: 506-510.
26. Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, et al. (2010) Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol 12: 473-488.
27. Steinbach WJ, Cramer RA, Perfect BZ, Asfaw YG, Sauer TC, et al. (2006) Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5: 1091-1103.
28. Brennan M, Thomas DY, Whiteway M, Kavanagh K, (2002) Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Mic 34: 153-157.
29. Champion OL, Cooper IAM, James SL, Ford D, Karlyshev A, et al. (2009) Galleria mellonella as an alternative infection model for Yersinia pseudotuberculosis. Microbiology 155: 1516-1522.
30. Hissen AHT, Wan ANC, Warwas ML, Pinto LJ, Moore MM, (2005) The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N-5-oxygenase, is required for virulence. Infect Immun 73: 5493-5503.
31. Schrettl M, Beckmann N, Varga J, Heinekamp T, Jacobsen ID, et al. (2010) HapX-Mediated Adaption to Iron Starvation Is Crucial for Virulence of Aspergillus fumigatus. PLoS Pathog 6: e1001124.
32. Clutterbuck AJ, (1997) The validity of the Aspergillus nidulans linkage map. Fungal Genet Biol 21: 267-277.
33. Clutterbuck AJ, The Aspergillus nidulans Linkage Map. Available: http://www.gla.ac.uk/ibls/molgen/aspergillus/index.html. Accessed 2010 June.
34. CADRE The Central Aspergillus Data REpository, Aspergillus nidulans database. Available: www.cadre-genomes.org.uk/Aspergillus_nidulans/. Accessed J2011 January.
35. Clutterbuck AJ, Farman M, (2008) Aspergillus nidulans linkage map and genome sequence: closing gaps and adding telomeres. In: Goldman GH, Osmani SA, editors. The Aspergilli: genomics, medical aspects, biotechnology, and research methods Boca Raton CRC Press pp. 57-73.
36. Ensembl Genomes. Available: ftp://ftp.ensemblgenomes.org/pub/fungi/release-5/fasta/aspergillus_nidul ans/dna/. Accessed 2009 October.
37. Lynch M, Walsh B, (1998) Genetics and Analysis of Quantitative Traits. Sunderland Sinauer Associates, Inc.
38. Broad Institute of Harvard and MIT Aspergillus Comparative Sequencing Project. Available: www.broadinstitute.org/annotation/genome/aspergillus_group/MultiDownload s.html. Accessed 2009 October.
39. Mayorga ME, Timberlake WE, (1990) Isolation and molecular characterization of the Aspergillus nidulans wA gene. Genetics 126: 73-79.
40. Tilburn J, Roussel F, Scazzocchio C, (1990) Insertional inactivation and cloning of the wA gene of Aspergillus nidulans. Genetics 126: 81-90.
41. Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, et al. (2005) Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 1: 232-240.
42. Steele C, Rapaka RR, Metz A, Pop SM, Williams DL, et al. (2005) The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog 1: 323-334.
43. Mouyna I, Morelle W, Vai M, Monod M, Lechenne B, et al. (2005) Deletion of GEL2 encoding for a beta(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol Microbiol 56: 1675-1688.
44. Mora-Montes HM, Bates S, Netea MG, Diaz-Jimenez DF, Lopez-Romero E, et al. (2007) Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal host-fungus interaction. Eukaryot Cell 6: 2184-2193.
45. Zhang L, Zhou H, Ouyang HM, Li YJ, Jin C, (2008) Afcwh41 is required for cell wall synthesis, conidiation, and polarity in Aspergillus fumigatus. FEMS Microbiol Lett 289: 155-165.
46. Coleman JJ, Mylonakis E, (2009) Efflux in Fungi: La Piece de Resistance. PLoS Pathog 5: e1000486.
47. Theiss S, Kretschmar M, Nichterlein T, Hof H, Agabian N, et al. (2002) Functional analysis of a vacuolar ABC transporter in wild-type Candida albicans reveals its involvement in virulence. Mol Microbiol 43: 571-584.
48. Sun S, Xu JP, (2007) Genetic analyses of a hybrid cross between serotypes A and D strains of the human pathogenic fungus Cryptococcus neoformans. Genetics 177: 1475-1486.
49. Marra RE, Huang JC, Fung E, Nielsen K, Heitman J, et al. (2004) A genetic linkage map of Cryptococcus neoformans variety neoformans serotype D (Filobasidiella neoformans). Genetics 167: 619-631.
50. Cheema MS, Christians JK, (2010) Virulence in an insect model differs between mating types in Aspergillus fumigatus. Med Mycol Sep. 6, Epub ahead of print.
51. Leger RJS, Screen SE, Shams-Pirzadeh B, (2000) Lack of host specialization in Aspergillus flavus. Appl Environ Microb 66: 320-324.
52. Jackson JC, Higgins LA, Lin XR, (2009) Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One 4: e4224.
53. Croft JH, Jinks JL, (1977) Aspects of the Population Genetics of Aspergillus nidulans. In: Smith JE, Pateman JA, editors. Genetics and Physiology of Aspergillus London Academic Press pp. 339-360.
54. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O, et al. (2007) Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog 3: 1195-1207.
55. Haas H, Eisendle M, Turgeon BG, (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46: 149-187.
56. Aleksenko A, Nielsen ML, Clutterbuck AJ, (2001) Genetic and physical mapping of two centromere-proximal regions of chromosome IV in Aspergillus nidulans. Fungal Genet Biol 32: 45-54.
57. Birdsell JA, (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19: 1181-1197.
58. Marsolier-Kergoat MC, Yeramian E, (2009) GC content and recombination: Reassessing the causal effects for the Saccharomyces cerevisiae genome. Genetics 183: 31-38.
59. Keurentjes JJB, Bentsink L, Alonso-Blanco C, Hanhart CJ, Vries HBD, et al. (2007) Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175: 891-905.
60. McCluskey K, Wiest A, Plamann M, (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosciences 35: 119-126.
61. Grindle M, (1963) Heterokaryon compatibility of unrelated strains in the Aspergillus nidulans group. Heredity 18: 191-204.
62. Bruggeman J, Debets AJM, Swart K, Hoekstra RF, (2003) Male and female roles in crosses of Aspergillus nidulans as revealed by vegetatively incompatible parents. Fungal Genet Biol 39: 136-141.
63. Butcher AC, (1968) The relationship between sexual outcrossing and heterokaryon incompatibility in Aspergillus nidulans. Heredity 23: 443-452.
64. Jin J, Lee YK, Wickes BL, (2004) Simple chemical extraction method for DNA isolation from Aspergillus fumigatus and other Aspergillus species. J Clin Microbiol 42: 4293-4296.
65. Wortman JR, Gilsenan JM, Joardar V, Deegan J, Clutterbuck J, et al. (2009) The 2008 update of the Aspergillus nidulans genome annotation: A community effort. Fungal Genet Biol 46: S2-S13.
66. Li H, Ruan J, Durbin R, (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851-1858.
67. Lorieux M, (2006) MapDisto, a tool for easy mapping of genetic markers, Poster P886. Plant and Animal Genome XIV conference, San Diego, CA. Available: http://mapdisto.free.fr/. Accessed 2010 July.
68. Egel-Mitani M, Olson LW, Egel R, (1982) Meiosis in Aspergillus nidulans: Another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 97: 179-187.
69. Tripathi N, Hoffmann M, Willing EM, Lanz C, Weigel D, et al. (2009) Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. P Roy Soc B-Biol Sci 276: 2195-2208.
70. Neilands JB, (1981) Microbial iron transport compounds (siderophores) as chelating agents. In: Martell AE, Anderson WF, Badman DG, editors. Development of Iron Chelators for Clinical Use New York Elsevier/North Holland pp. 13-31.
71. Dutsky SR, Thompson JV, Cantwell GE, (1962) A technique for mass rearing the greater wax moth (Lepidoptera, Galleridae). P Entomol Soc Wash 64: 56-58.
72. Wang S, Basten CJ, Zeng ZB, (2010) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. Available: http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. Accessed: 2010 August.
73. Churchill GA, Doerge RW, (1994) Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
74. Henikoff S, Henikoff JG, (1992) Amino acid substitution matrices from protein blocks. P Natl Acad Sci USA 89: 10915-10919.