Signature Gene Expression Reveals Novel Clues to the Molecular Mechanisms of Dimorphic Transition in Penicillium marneffei

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Yang, Ence ^a   Chow, Wang Ngai ^b   Wang, Gang ^a   Woo, Patrick C Y ^b   Lau, Susanna K P ^b   Yuen, Kwok Yung ^b   Lin, Xiaorong ^c   Cai, James J ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MADS DOMAIN PROTEIN; FUNGAL PROTEIN; FUNGAL RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; DNA HYBRIDIZATION; FUNGAL GENE; FUNGAL GENETICS; FUNGAL GENOME; FUNGAL LIFE CYCLE STAGE; FUNGAL STRAIN; FUNGI BY OUTER APPEARANCE; FUNGUS CULTURE; GENE CLUSTER; GENE CONSTRUCT; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC DATABASE; GENETIC VARIABILITY; GENOME ANALYSIS; INCUBATION TEMPERATURE; MADSA GENE; MYCELIAL GROWTH; MYCELIUM; NONHUMAN; PENICILLIUM MARNEFFEI; PHASE TRANSITION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; RNA STRUCTURE; SYSTEMIC DIMORPHIC FUNGUS; TEMPERATURE ACCLIMATIZATION; TEMPERATURE SENSITIVITY; TRANSCRIPTION REGULATION; TRANSITION TEMPERATURE; VALIDATION STUDY; WILD TYPE; YEAST; YEAST MYCELIUM TRANSITION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MULTIGENE FAMILY; PATHOGENICITY; PENICILLIUM; SECRETION (PROCESS); TEMPERATURE;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENOME, FUNGAL; MADS DOMAIN PROTEINS; MULTIGENE FAMILY; MYCELIUM; PENICILLIUM; RNA, FUNGAL; TEMPERATURE; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84908310937     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004662     Document Type: Article

References (60)

1. Cooney NM, Klein BS, (2008) Fungal adaptation to the mammalian host: it is a new world, after all. Current Opinion in Microbiology 11: 511–516.
2. Rappleye CA, Goldman WE, (2006) Defining virulence genes in the dimorphic fungi. Annual Review of Microbiology 60: 281–303.
3. Klein BS, Tebbets B, (2007) Dimorphism and virulence in fungi. Current Opinion in Microbiology 10: 314–319.
4. Mandell GL, Bennett JE, Dolin R (2010) Mandell, Douglas, and Bennett's principles and practice of infectious diseases. Philadelphia, PA: Churchill Livingstone/Elsevier.
5. Nemecek JC, Wuthrich M, Klein BS, (2006) Global control of dimorphism and virulence in fungi. Science 312: 583–588.
6. Cooper CR, Vanittanakom N, (2008) Insights into the pathogenicity of Penicillium marneffei. Future Microbiology 3: 43–55.
7. Samson RA, Yilmaz N, Houbraken J, Spierenburg H, Seifert KA, et al. (2011) Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium. Studies in Mycology 159–183.
8. Boyce KJ, Andrianopoulos A, (2013) Morphogenetic circuitry regulating growth and development in the dimorphic pathogen Penicillium marneffei. Eukaryotic Cell 12: 154–160.
9. Xi LY, Xu XR, Liu W, Li XQ, Liu YL, et al. (2007) Differentially expressed proteins of pathogenic Penicillium marneffei in yeast and mycelial phases. Journal of Medical Microbiology 56: 298–304.
10. Chandler JM, Treece ER, Trenary HR, Brenneman JL, Flickner TJ, et al. (2008) Protein profiling of the dimorphic, pathogenic fungus, Penicillium marneffei. Proteome Science 6: 17.
11. Lin X, Ran Y, Gou L, He F, Zhang R, et al. (2012) Comprehensive transcription analysis of human pathogenic fungus Penicillium marneffei in mycelial and yeast cells. Medical Mycology 50: 835–842.
12. Pasricha S, Payne M, Canovas D, Pase L, Ngaosuwankul N, et al. (2013) Cell-type-specific transcriptional profiles of the dimorphic pathogen Penicillium marneffei reflect distinct reproductive, morphological, and environmental demands. G3-Genes Genomes Genetics 3: 1997–2014.
13. Yang E, Wang G, Woo PCY, Lau SKP, Chow WN, et al. (2013) Unraveling the molecular basis of temperature-dependent genetic regulation in Penicillium marneffei. Eukaryotic Cell 12: 1214–1224.
14. Woo PCY, Lau SKP, Liu B, Cai JJ, Chong KTK, et al. (2011) Draft genome sequence of Penicillium marneffei strain PM1. Eukaryotic Cell 10: 1740–1741.
15. Koren S, Schatz MC, Walenz BP, Martin J, Howard JT, et al. (2012) Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nature Biotechnology 30: 693–700.
16. Miller JR, Delcher AL, Koren S, Venter E, Walenz BP, et al. (2008) Aggressive assembly of pyrosequencing reads with mates. Bioinformatics 24: 2818–2824.
17. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, et al. (2009) ABySS: A parallel assembler for short read sequence data. Genome Research 19: 1117–1123.
18. Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Research 20: 265–272.
19. Mortazavi A, Schwarz EM, Williams B, Schaeffer L, Antoshechkin I, et al. (2010) Scaffolding a Caenorhabditis nematode genome with RNA-seq. Genome Research 20: 1740–1747.
20. Supek F, Bosnjak M, Skunca N, Smuc T, (2011) REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms. PLoS One 6: e21800.
21. Barrera LO, Ren B, (2006) The transcriptional regulatory code of eukaryotic cells insights from genome-wide analysis of chromatin organization and transcription factor binding. Current Opinion in Cell Biology 18: 291–298.
22. Heintzman ND, Ren B, (2007) The gateway to transcription: identifying, characterizing and understanding promoters in the eukaryotic genome. Cellular and Molecular Life Sciences 64: 386–400.
23. Elble R, Tye BK, (1991) Both activation and repression of a-mating-type-specific genes in yeast require transcription factor Mcm1. Proceedings of the National Academy of Sciences of the United States of America 88: 10966–10970.
24. Nielsen O, Friis T, Kjaerulff S, (1996) The Schizosaccharomyces pombe map1 gene encodes an SRF/MCM1-related protein required for P-cell specific gene expression. Molecular & General Genetics 253: 387–392.
25. Yabana N, Yamamoto M, (1996) Schizosaccharomyces pombe map1+ encodes a MADS-box-family protein required for cell-type-specific gene expression. Molecular and Cellular Biology 16: 3420–3428.
26. Lau SKP, Tse H, Chan JSY, Zhou AC, Curreem SOT, et al. (2013) Proteome profiling of the dimorphic fungus Penicillium marneffei extracellular proteins and identification of glyceraldehyde-3-phosphate dehydrogenase as an important adhesion factor for conidial attachment. FEBS Journal 280: 6613–6626.
27. Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
28. Meerupati T, Andersson KM, Friman E, Kumar D, Tunlid A, et al. (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genetics 9: e1003909.
29. Wan Y, Kertesz M, Spitale RC, Segal E, Chang HY, (2011) Understanding the transcriptome through RNA structure. Nature Reviews Genetics 12: 641–655.
30. Reineke LC, Komar AA, Caprara MG, Merrick WC, (2008) A small stem loop element directs internal initiation of the URE2 internal ribosome entry site in Saccharomyces cerevisiae. Journal of Biological Chemistry 283: 19011–19025.
31. Wan Y, Qu K, Ouyang ZQ, Kertesz M, Li J, et al. (2012) Genome-wide Measurement of RNA Folding Energies. Molecular Cell 48: 169–181.
32. Mortimer SA, Kidwell MA, Doudna JA, (2014) Insights into RNA structure and function from genome-wide studies. Nat Rev Genet 15: 469–479.
33. Lorenz R, Bernhart SH, Siederdissen CHZ, Tafer H, Flamm C, et al. (2011) ViennaRNA Package 2.0. Algorithms for Molecular Biology 6: 26.
34. Nakagawa S, Niimura Y, Gojobori T, Tanaka H, Miura K, (2008) Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes. Nucleic Acids Research 36: 861–871.
35. Metzker ML, (2010) Sequencing technologies - the next generation. Nature Reviews Genetics 11: 31–46.
36. Niu BF, Fu LM, Sun SL, Li WZ, (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinformatics 11: 187.
37. Dohm JC, Lottaz C, Borodina T, Himmelbauer H, (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Research 36: e105.
38. Kingsford C, Schatz MC, Pop M, (2010) Assembly complexity of prokaryotic genomes using short reads. BMC Bioinformatics 11: 21.
39. Schadt EE, Turner S, Kasarskis A, (2010) A window into third-generation sequencing. Human Molecular Genetics 19: R227–R240.
40. Bashir A, Klammer AA, Robins WP, Chin CS, Webster D, et al. (2012) A hybrid approach for the automated finishing of bacterial genomes. Nature Biotechnology 30: 701–707.
41. Gifford TD, Cooper CR, (2009) Karyotype determination and gene mapping in two clinical isolates of Penicillium marneffei. Medical Mycology 47: 286–295.
42. Yuen K, Pascal G, Wong SSY, Glaser P, Woo PCY, et al. (2003) Exploring the Penicillium marneffei genome. Archives of Microbiology 179: 339–353.
43. Frangeul L, Nelson KE, Buchrieser C, Danchin A, Glaser P, et al. (1999) Cloning and assembly strategies in microbial genome projects. Microbiology 145: 2625–2634.
44. Solovyev V, Kosarev P, Seledsov I, Vorobyev D, (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biology 7: S10.
45. Jones P, Binns D, Chang H-Y, Fraser M, Li W, et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30: 1236–1240.
46. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14: R36.
47. Xu G, Deng N, Zhao Z, Judeh T, Flemington E, et al. (2011) SAMMate: a GUI tool for processing short read alignments in SAM/BAM format. Source Code for Biology and Medicine 6: 2.
48. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5: 621–628.
49. Kummasook A, Tzarphmaag A, Thirach S, Pongpom M, Cooper CR, et al. (2011) Penicillium marneffei actin expression during phase transition, oxidative stress, and macrophage infection. Molecular Biology Reports 38: 2813–2819.
50. Thirach S, Cooper CR, Vanittanakom N, (2008) Molecular analysis of the Penicillium marneffei glyceraldehyde-3-phosphate dehydrogenase-encoding gene (gpdA) and differential expression of gpdA and the isocitrate lyase-encoding gene (acuD) upon internalization by murine macrophages. Journal of Medical Microbiology 57: 1322–1328.
51. Woo PCY, Chong KTK, Lau CCY, Wong SSY, Lau SKP, et al. (2006) A novel approach for screening immunogenic proteins in Penicillium marneffei using the ΔAFMP1 ΔAFMP2 deletion mutant of Aspergillus fumigatus. FEMS Microbiology Letters 262: 138–147.
52. Woo PCY, Lam CW, Tam EWT, Leung CKF, Wong SSY, et al. (2012) First discovery of two polyketide synthase genes for mitorubrinic acid and mitorubrinol yellow pigment biosynthesis and implications in virulence of Penicillium marneffei. PLoS Neglected Tropical Diseases 6: e1871.
53. Lau SKP, Chow WN, Wong AYP, Yeung JMY, Bao J, et al. (2013) Identification of microRNA-like RNAs in mycelial and yeast phases of the thermal dimorphic fungus Penicillium marneffei. PLoS Neglected Tropical Diseases 7: e2398.
54. Min XJ, (2010) Evaluation of computational methods for secreted protein prediction in different Eukaryotes. Journal of Proteomics & Bioinformatics 3: 143–147.
55. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Research 35: W585–W587.
56. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785–786.
57. Kall L, Krogh A, Sonnhammer ELL, (2007) Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Research 35: W429–W432.
58. do Amaral AM, Antoniw J, Rudd JJ, Hammond-Kosack KE, (2012) Defining the predicted protein secretome of the fungal wheat leaf pathogen Mycosphaerella graminicola. PLoS One 7: e49904.
59. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL, (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305: 567–580.
60. de Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, et al. (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research 34: W362–W365.