1887

Abstract

Microarray studies have examined global gene expression in over 20 species of filamentous fungi encompassing a wide variety of research areas. The majority have addressed aspects of metabolism or pathogenicity. Metabolic studies have revealed important differences in the transcriptional regulation of genes for primary metabolic pathways between filamentous fungi and yeast. Transcriptional profiles for genes involved in secondary metabolism have also been established. Genes required for the biosynthesis of both useful and detrimental secondary metabolites have been identified. Due to the economic, ecological and medical implications, it is not surprising that many studies have used microarray analysis to examine gene expression in pathogenic filamentous fungi. Genes involved in various stages of pathogenicity have been identified, including those thought to be important for adaptation to the host environment. While most of the studies have simulated pathogenic conditions , a small number have also reported fungal gene expression within their plant hosts. This review summarizes the first 50 microarray studies in filamentous fungi and highlights areas for future investigation.

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2007-01-01
2020-04-04
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References

  1. Aign V., Hoheisel J. D. 2003; Analysis of nutrient-dependent transcript variations in Neurospora crassa . Fungal Genet Biol40:225–233[CrossRef]
    [Google Scholar]
  2. Allen T. D., Nuss D. L. 2004a; Specific and common alterations in host gene transcript accumulation following infection of the chestnut blight fungus by mild and severe hypoviruses. J Virol78:4145–4155[CrossRef]
    [Google Scholar]
  3. Allen T. D., Nuss D. L. 2004b; Linkage between mitochondrial hypovirulence and viral hypovirulence in the chestnut blight fungus revealed by cDNA microarray analysis. Eukaryot Cell3:1227–1232[CrossRef]
    [Google Scholar]
  4. Allen T. D., Dawe A. L., Nuss D. L. 2003; Use of cDNA microarrays to monitor transcriptional responses of the chestnut blight fungus Cryphonectria parasitica to infection by virulence-attenuating hypoviruses. Eukaryot Cell2:1253–1265[CrossRef]
    [Google Scholar]
  5. Bähler J. 2005; Cell-cycle control of gene expression in budding and fission yeast. Annu Rev Genet39:69–94[CrossRef]
    [Google Scholar]
  6. Bell-Pedersen D., Shinohara M. L., Loros J. J., Dunlap J. C. 1996; Circadian clock-controlled genes isolated from Neurospora crassa are late night- to early morning-specific. Proc Natl Acad Sci U S A93:13096–13101[CrossRef]
    [Google Scholar]
  7. Bok J. W., Hoffmeister D., Maggio-Hall L. A., Murillo R., Glasner J. D., Keller N. P. 2006; Genomic mining for Aspergillus natural products. Chem Biol13:31–37[CrossRef]
    [Google Scholar]
  8. Bonaccorsi E. D., Ferreira A. J. S., Chambergo F. S., Ramos S. P., Mantovani M. C., Farah J. P. S., Sorio C. S., Gombert A. K., Tonso A., El-Dorry H. 2006; Transcriptional response of the obligatory aerobe Trichoderma reesei to hypoxia and transient anoxia: implications for energy production and survival in the absence of oxygen. Biochemistry45:3912–3924[CrossRef]
    [Google Scholar]
  9. Both M., Eckert S. E., Csukai M., Muller E., Dimopoulos G., Spanu P. D. 2005a; Transcript profiles of Blumeria graminis development during infection reveal a cluster of genes that are potential virulence determinants. Mol Plant Microbe Interact18:125–133[CrossRef]
    [Google Scholar]
  10. Both M., Csukai M., Stumpf M. P. H., Spanu P. D. 2005b; Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell17:2107–2122[CrossRef]
    [Google Scholar]
  11. Chambergo F. S., Bonaccorsi E. D., Ferreira A. J. S., Ramos A. S. P., Junior J. R. F., Abrahao-Neto J., Farah J. P. S., El-Dorry H. 2002; Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. J Biol Chem277:13983–13988[CrossRef]
    [Google Scholar]
  12. Conesa A., Jeenes D., Archer D. B., Punt P. J, van den Hondel C. A.. 2002; Calnexin overexpression increases manganese peroxidase production in Aspergillus niger . Appl Environ Microbiol68:846–851[CrossRef]
    [Google Scholar]
  13. Correa A., Lewis A. Z., Greene A. V., March I. J., Gomer R. H., Bell-Pedersen D. 2003; Multiple oscillators regulate circadian gene expression in Neurospora . Proc Natl Acad Sci U S A100:13597–13602[CrossRef]
    [Google Scholar]
  14. Dawe A. L., Segers G. C., Allen T. D., McMains V. C., Nuss D. L. 2004; Microarray analysis of Cryphonectria parasitica G α - and G βγ -signalling pathways reveals extensive modulation by hypovirus infection. Microbiology150:4033–4043[CrossRef]
    [Google Scholar]
  15. DeRisi J. L., Iyer V. R., Brown P. O. 1997; Exploring the metabolic and genetic control of gene expression on a genomic scale. Science278:680–686[CrossRef]
    [Google Scholar]
  16. Divon H. H., Rothan-Denoyes B., Davydov O., Di Pietro A., Fluhr R. 2005; Nitrogen-responsive genes are differentially regulated in planta during Fusarium oxysporum f.sp. lycopersici infection. Mol Plant Pathol6:459–470[CrossRef]
    [Google Scholar]
  17. Doddapaneni H., Yadav J. S. 2005; Microarray-based global differential expression profiling of P450 monooxygenases and regulatory proteins for signal transduction pathways in the white rot fungus Phanerochaete chrysosporium . Mol Genet Genomics274:454–466[CrossRef]
    [Google Scholar]
  18. Felitti S., Shields K., Ramsperger M., Tian P., Sawbridge T., Webster T., Logan E., Erwin T., Forster J.. other authors 2006; Transcriptome analysis of Neotyphodium and Epichloë grass endophytes. Fungal Genet Biol43:465–475[CrossRef]
    [Google Scholar]
  19. Ferreira M. E. D., Malavazi I., Savoldi M., Brakhage A. A., Goldman M. H. S., Kim H. S., Nierman W. C., Goldman G. H. 2006; Transcriptome analysis of Aspergillus fumigatus exposed to voriconazole. Curr Genet50:32–44[CrossRef]
    [Google Scholar]
  20. Flipphi M., Kocialkowska J., Felenbok B. 2002; Characteristics of physiological inducers of the ethanol utilization (alc) pathway in Aspergillus nidulans . Biochem J364:25–31
    [Google Scholar]
  21. Flipphi M., Ruijter G. J., Visser J., Felenbok B, van de Vondervoort P. J., Arst H. N. Jr. 2003; Onset of carbon catabolite repression in Aspergillus nidulans . Parallel involvement of hexokinase and glucokinase in sugar signaling. J Biol Chem278:11849–11857[CrossRef]
    [Google Scholar]
  22. Foreman P. K., Brown D., Dankmeyer L., Dean R., Diener S., Dunn-Coleman N. S., Goedegebuur F., Houfek T. D., England G. J. other authors 2003; Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei . J Biol Chem278:31988–31997[CrossRef]
    [Google Scholar]
  23. Freimoser F. M., Hu G., St Leger R. J. 2005; Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro . Microbiology151:361–371[CrossRef]
    [Google Scholar]
  24. Güldener U.. Seong K. Y., Boddu J., Cho S., Trail F., Xu J., Adam G., Mewes H., Muehlbauer G. J., Kistler H. C. 2006; Development of a Fusarium graminearum Affymetrix GeneChip for profiling fungal gene expression in vitro and in planta . Fungal Genet Biol43:316–325[CrossRef]
    [Google Scholar]
  25. Hromatka B. S., Noble S. M., Johnson A. D. 2005; Transcriptional response of Candida albicans to nitric oxide and the role of the YHB1 gene in nitrosative stress and virulence. Mol Biol Cell16:4814–4826[CrossRef]
    [Google Scholar]
  26. Hwang C. S., Flaishman M. A., Kolattukudy P. E. 1995; Cloning of a gene expressed during appressorium formation by Colletotrichum gloeosporioides and a marked decrease in virulence by disruption of this gene. Plant Cell7:183–193[CrossRef]
    [Google Scholar]
  27. Jakupović M., Heintz M.. Reichmann P., Mendgen K., Hahn M. 2006; Microarray analysis of expressed sequence tags from haustoria of the rust fungus Uromyces fabae . Fungal Genet Biol43:8–19[CrossRef]
    [Google Scholar]
  28. Johansson T., Ahren D., Erlandsson R., Lundeberg J., Tunlid A, Le Quéré A., Söderström B., Uhlén M.. 2004; Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microbe Interact17:202–215[CrossRef]
    [Google Scholar]
  29. Kasuga T., Townsend J. P., Tian C. G., Gilbert L. B., Mannhaupt G., Taylor J. W., Glass N. L. 2005; Long-oligomer microarray profiling in Neurospora crassa reveals the transcriptional program underlying biochemical and physiological events of conidial germination. Nucleic Acids Res33:6469–6485[CrossRef]
    [Google Scholar]
  30. Kim Y. K., Wang Y., Liu Z. M., Kolattukudy P. E. 2002; Identification of a hard surface contact-induced gene in Colletotrichum gloeosporioides conidia as a sterol glycosyl transferase, a novel fungal virulence factor. Plant J30:177–187[CrossRef]
    [Google Scholar]
  31. Kwast K. E., Lai L. C., Menda N., Aref S., Burke P. V, James D. T. III. 2002; Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae : functional roles of Rox1 and other factors in mediating the anoxic response. J Bacteriol184:250–265[CrossRef]
    [Google Scholar]
  32. Lashkari D. A., DeRisi J. L., McCusker J. H., Namath A. F., Gentile C., Hwang S. Y., Brown P. O., Davis R. W. 1997; Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci U S A94:13057–13062[CrossRef]
    [Google Scholar]
  33. Lee S. H., Lee S., Choi D., Lee Y. W., Yun S. H. 2006; Identification of the down-regulated genes in a mat1-2- deleted strain of Gibberella zeae , using cDNA subtraction and microarray analysis. Fungal Genet Biol43:295–310[CrossRef]
    [Google Scholar]
  34. Lepak A., Nett J., Lincoln L., Marchillo K., Andes D. 2006; Time course of microbiologic outcome and gene expression in Candida albicans during and following in vitro and in vivo exposure to fluconazole. Antimicrob Agents Chemother50:1311–1319[CrossRef]
    [Google Scholar]
  35. Le Quéré A., Schützendübel A.. Rajashekar B., Hedh J., Erland S., Johansson T., Tunlid A, Canbäck B.. 2004; Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus. Mol Ecol13:3809–3819[CrossRef]
    [Google Scholar]
  36. Le Quéré A.. Wright D. P., Tunlid A., Johansson T, Söderström B.. 2005; Global patterns of gene regulation associated with the development of ectomycorrhiza between birch ( Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol Plant Microbe Interact18:659–673[CrossRef]
    [Google Scholar]
  37. Le Quéré A.. Eriksen K. A., Rajashekar B., Johansson T., Tunlid A, Schützenbübel A., Canbäck B.. 2006; Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Mol Ecol15:535–550
    [Google Scholar]
  38. Lewis Z. A., Correa A., Schwerdtfeger C., Link K. L., Xie X., Gomer R. H., Thomas T., Ebbole D. J., Bell-Pedersen D. 2002; Overexpression of White Collar-1 (WC-1) activates circadian clock-associated genes, but is not sufficient to induce most light-regulated gene expression in Neurospora crassa . Mol Microbiol45:917–931[CrossRef]
    [Google Scholar]
  39. Li D., Bobrowicz P., Wilkinson H. H., Ebbole D. J. 2005; A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa . Genetics170:1091–1104[CrossRef]
    [Google Scholar]
  40. MacKenzie D. A., Guillemette T., Al-Sheikh H., Watson A. J., Jeenes D. J., Wongwathanarat P., Dunn-Coleman N. S., Archer D. B, van Peij N.. 2005; UPR-independent dithiothreitol stress-induced genes in Aspergillus niger . Mol Genet Genomics274:410–418[CrossRef]
    [Google Scholar]
  41. Maeda H., Sano M., Maruyama Y., Tanno T., Akao T., Totsuka Y., Endo M., Sakurada R., Yamagata Y.. other authors 2004; Transcriptional analysis of genes for energy catabolism and hydrolytic enzymes in the filamentous fungus Aspergillus oryzae using cDNA microarrays and expressed sequence tags. Appl Microbiol Biotechnol65:74–83
    [Google Scholar]
  42. McFadden H. G., Wilson I. W., Chapple R. M., Dowd C. 2006; Fusarium wilt ( Fusarium oxysporum f. sp. vasinfectum) genes expressed during infection of cotton ( Gossypium hirsutum ). Mol Plant Pathol7:87–101[CrossRef]
    [Google Scholar]
  43. Moralejo F. J., Watson A. J., Jeenes D. J., Archer D. B., Martin J. F. 2001; A defined level of protein disulfide isomerase expression is required for optimal secretion of thaumatin by Aspergillus awamori . Mol Genet Genomics266:246–253[CrossRef]
    [Google Scholar]
  44. Nicolaisen M., Justesen A. F., Thrane U., Skouboe P., Holmstrom K. 2005; An oligonucleotide microarray for the identification and differentiation of trichothecene producing and non-producing Fusarium species occurring on cereal grain. J Microbiol Methods62:57–69[CrossRef]
    [Google Scholar]
  45. Nierman W. C., Pain A., Anderson M. J., Wortman J. R., Kim H. S., Arroyo J., Berriman M., Abe K., Archer D. B.. other authors 2005; Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus . Nature438:1151–1156[CrossRef]
    [Google Scholar]
  46. Nowrousian M., Duffield G. E., Loros J. J., Dunlap J. C. 2003; The frequency gene is required for temperature-dependent regulation of many clock-controlled genes in Neurospora crassa . Genetics164:923–933
    [Google Scholar]
  47. Nowrousian M., Ringelberg C., Dunlap J. C., Loros J. L., Kuck U. 2005; Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora . Mol Genet Genomics273:137–149[CrossRef]
    [Google Scholar]
  48. O'Brian G. R., Fakhoury A. M., Payne G. A. 2003; Identification of genes differentially expressed during aflatoxin biosynthesis in Aspergillus flavus and Aspergillus parasiticus . Fungal Genet Biol39:118–127[CrossRef]
    [Google Scholar]
  49. Peng X., Karuturi R. K., Miller L. D., Lin K., Jia Y., Kondu P., Wang L., Wong L., Liu E. T.. other authors 2005; Identification of cell cycle-regulated genes in fission yeast. Mol Biol Cell16:1026–1042[CrossRef]
    [Google Scholar]
  50. Pirttilä A. M.. McIntyre L. M., Payne G. A., Woloshuk C. P. 2004; Expression profile analysis of wild-type and fec1 mutant strains of Fusarium verticillioides during fumonisin biosynthesis. Fungal Genet Biol41:647–656[CrossRef]
    [Google Scholar]
  51. Pöggeler S.. Nowrousian M., Ringelberg C., Loros J. J., Dunlap J. C., Kuck U. 2006; Microarray and real-time PCR analyses reveal mating type-dependent gene expression in a homothallic fungus. Mol Genet Genomics275:492–503[CrossRef]
    [Google Scholar]
  52. Price M. S., Shannon B. C. B., Sabrina T. B., Robert A. K. B., Payne G. A. 2005; Aflatoxin conducive and non-conducive growth conditions reveal new gene associations with aflatoxin production. Fungal Genet Biol42:506–518[CrossRef]
    [Google Scholar]
  53. Price M. S., Yu J. J., Nierman W. C., Kim H. S., Pritchard B., Jacobus C. A., Bhatnagar D., Cleveland T. E., Payne G. A. 2006; The aflatoxin pathway regulator AfIR induces gene transcription inside and outside of the aflatoxin biosynthetic cluster. FEMS Microbiol Lett255:275–279[CrossRef]
    [Google Scholar]
  54. Qi W. H., Chil K., Trail F. 2006; Microarray analysis of transcript accumulation during perithecium development in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum ). Mol Genet Genomics276:87–100[CrossRef]
    [Google Scholar]
  55. Ray A., Macwana S., Ayoubi P., Hall L. T., Prade R., Mort A. J. 2004; Negative subtraction hybridization: an efficient method to isolate large numbers of condition-specific cDNAs. BMC Genomics5:22[CrossRef]
    [Google Scholar]
  56. Sandovsky-Losica H., Chauhan N., Calderone R., Segal E. 2006; Gene transcription studies of Candida albicans following infection of HEp2 epithelial cells. Med Mycol44:329–334[CrossRef]
    [Google Scholar]
  57. Sargent M. L., Briggs W. R., Woodward D. O. 1966; Circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa . Plant Physiol41:1343–1349[CrossRef]
    [Google Scholar]
  58. Sims A. H., Robson G. D., Hoyle D. C., Oliver S. G., Turner G., Prade R. A., Russell H. H., Dunn-Coleman N. S., Gent M. E. 2004; Use of expressed sequence tag analysis and cDNA microarrays of the filamentous fungus Aspergillus nidulans . Fungal Genet Biol41:199–212[CrossRef]
    [Google Scholar]
  59. Sims A. H., Gent M. E., Lanthaler K., Dunn-Coleman N. S., Oliver S. G., Robson G. D. 2005; Transcriptome analysis of recombinant protein secretion by Aspergillus nidulans and the unfolded-protein response in vivo . Appl Environ Microbiol71:2737–2747[CrossRef]
    [Google Scholar]
  60. Söderström B.. Finlay R. D., Read D. J. 1988; The structure and function of the vegetative mycelium of ectomycorrhizal plants. 4. Qualitative analysis of carbohydrate contents of mycelium interconnecting host plants. New Phytol109:163–166[CrossRef]
    [Google Scholar]
  61. Spellman P. T., Sherlock G., Zhang M. Q., Iyer V. R., Anders K., Eisen M. B., Brown P. O., Botstein D., Futcher B. 1998; Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell9:3273–3297[CrossRef]
    [Google Scholar]
  62. Sun X., Jiang M. F., Li X., Zhang Y. Z. 2004; Rapid screening of expressed genes of Trametes gallica by cDNA microarray. Prog Biochem Biophys31:356–360
    [Google Scholar]
  63. Takahashi J. S., Zatz M. 1982; Regulation of circadian rhythmicity. Science217:1104–1111[CrossRef]
    [Google Scholar]
  64. Takano Y., Choi W. B., Mitchell T. K., Okuno T., Dean R. A. 2003; Large scale parallel analysis of gene expression during infection-related morphogenesis of Magnaporthe grisea . Mol Plant Pathol4:337–346[CrossRef]
    [Google Scholar]
  65. Wang C. S., Leger R. J. S. 2005; Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum . Eukaryot Cell4:937–947[CrossRef]
    [Google Scholar]
  66. Wang C. S., Hu G., St Leger R. J. 2005a; Differential gene expression by Metarhizium anisopliae growing in root exudate and host ( Manduca sexta ) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol42:704–718[CrossRef]
    [Google Scholar]
  67. Wang C. S., Butt T. M., St Leger R. J. 2005b; Colony sectorization of Metarhizium anisopliae is a sign of ageing. Microbiology151:3223–3236[CrossRef]
    [Google Scholar]
  68. Wright D. P., Johansson T., Soderstrom B., Tunlid A, Le Quéré A.. 2005; Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch ( Betula pendula ) seedlings in soil microcosms. New Phytol167:579–596[CrossRef]
    [Google Scholar]
  69. Xie X., Wilkinson H. H., Correa A., Lewis Z. A., Bell-Pedersen D., Ebbole D. J. 2004; Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa . Fungal Genet Biol41:1104–1119[CrossRef]
    [Google Scholar]
  70. Xu Q., Ibarra M., Mahadeo D., Shaw C., Huang E., Kuspa A., Cotter D., Shaulsky G. 2004; Transcriptional transitions during Dictyostelium spore germination. Eukaryot Cell3:1101–1110[CrossRef]
    [Google Scholar]
  71. Young M. W., Kay S. A. 2001; Time zones: a comparative genetics of circadian clocks. Nat Rev Genet2:702–715[CrossRef]
    [Google Scholar]
  72. Yu J. H., Butchko R. A., Fernandes M., Keller N. P., Leonard T. J., Adams T. H. 1996; Conservation of structure and function of the aflatoxin regulatory gene aflR from Aspergillus nidulans and A. flavus . Curr Genet29:549–555[CrossRef]
    [Google Scholar]
  73. Zahiri A. R., Babu M. R., Saville B. J. 2005; Differential gene expression during teliospore germination in Ustilago maydis . Mol Genet Genomics273:394–403[CrossRef]
    [Google Scholar]
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