Environmental regulation of reproductive phase change in Agaricus bisporus by 1-octen-3-ol, temperature and CO2

Fungal Genetics and Biology

Volumn 55, Issue , 2013, Pages 54-66

  Eastwood, Daniel C ^a,b   Herman, Bram ^b,e   Noble, Ralph ^c   Dobrovin Pennington, Andreja ^c   Sreenivasaprasad, S ^b,d   Burton, Kerry S ^c  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c EAST MALLING RESEARCH   (United Kingdom)

^d UNIVERSITY OF BEDFORDSHIRE   (United Kingdom)

^e AGILENT TECHNOLOGIES   (United Kingdom)

Author keywords

Agaricus bisporus; Cultivated mushroom; Fruiting regulation; Microarray; Reproductive phase change

Indexed keywords

1 OCTEN 3 OL; CARBON DIOXIDE;

AGARICUS BISPORUS; ARTICLE; CARBON METABOLISM; CELL STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENVIRONMENTAL PARAMETERS; ENVIRONMENTAL REGULATION; FRUITING BODY; FUNGAL GENOME; FUNGAL PHENOMENA AND FUNCTIONS; FUNGUS HYPHAE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; NITROGEN METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; REPRODUCTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENTIATION; TEMPERATURE SENSITIVITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; VEGETATIVE STAGE;

AGARICUS; CARBON DIOXIDE; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; MICROARRAY ANALYSIS; MULTIGENE FAMILY; OCTANOLS; TEMPERATURE; TRANSCRIPTOME;

AGARICUS BISPORUS;

EID: 84879012417     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.01.001     Document Type: Article

References (80)

1. Alspaugh J.A., Pukkila-Worley R., Harashima T., Cavallo L.M., Funnell D., Cox G.M., et al. Adenylyl cyclase functions downstream of the Gα protein Gpa1 and controls mating and pathogenicity in Cryptococcus neoformans. Eukaryot. Cell 2002, 1:75-84.
2. Angelini C., Cutillo L., De Canditiis D., Mutarelli M., Pensky M. BATS: a Bayesian user-friendly software for Analyzing Time Series microarray experiments. BMC Bioinformat. 2008, 9:415.
3. Baars J.J., Op den Camp H.J.M., Hermans J.M.H., Mikes V., van der Drift C., et al. Nitrogen assimilating enzymes in the white button mushroom Agaricus bisporus. Microbiology 1994, 140:1161-1168.
4. 2-acceptoren. Archiv für Mikrobiologie 1968, 60(3):217-234.
5. Bahn Y-.S., Xue C.Y., Idnurm A., Rutherford J.C., Heitman J., Cardenas M.E. Sensing the environment: lessons from fungi. Nat. Rev. Microbiol. 2007, 5:57-69.
6. 2 sensing during Cryptococcus neoformans growth, differentiation and virulence. Curr. Biol. 2005, 15:2013-2026.
7. 2 sensing in fungi and beyond. Curr. Opin. Microbiol. 2006, 9:572-578.
8. Barnett C.L., Beresford N.A., Self P.J.L., Howard B.J., Frankland J.C., Fulker M.J., et al. Radiocaesium activity concentrations in the fruit-bodies of marcofungi in Great Britain and an assessment of dietary intake habits. Sci. Total Environ. 1999, 231(1):67-83.
9. Bertossa R.C., Kües U., Aebi M., Kunzler M. Promoter analysis of cgl2, a galectin encoding gene transcribed during fruiting body formation in Coprinopsis cinerea (Coprinus cinereus). Fung. Genet. Biol. 2004, 41:1120-1131.
10. Casselton, L.A., Challen, M.P., 2006. The mating type genes of the basidiomycetes. In: Kües, U., Fisher, R. (Eds.), The Mycota, growth, differentiation and sexuality, second ed., vol. 1, Springer, Berlin, Germany, pp. 352-368.
11. Chen H., McCormick D.B. Riboflavin 5'-hydroxymethyl oxidation: molecular cloning, expression and glycoprotein nature of the 5'-aldehyde-forming enzyme from Schizophyllum commune. J. Biol. Chem. 1997, 272(32):20077-20081.
12. Chitarra G.S., Abee T., Rombouts F.M., Posthumus M.A., Dijksterhuis J. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl. Environ. Microbiol. 2004, 70:2823-2829.
13. Chum W.W.Y., Ng K.T.P., Shih R.S.M., Au C.H., Kwan H.S. Gene expression studies of the dikaryotic mycelium and primordium of Lentinula edodes by serial analysis of gene expression. Mycol. Res. 2008, 112:950-964.
14. Combet E., Henderson J., Eastwood D.C., Burton K.S. Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 2006, 47:317-326.
15. Combet E., Henderson J., Eastwood D.C., Burton K.S. Influence of sporophore development, damage, storage, and tissue specificity on the enzymic formation of volatiles in mushrooms (Agaricus bisporus). J. Agric. Food Chem. 2009, 13:3709-3717.
16. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. BLAST2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
17. Conkright M.D., Guzman E., Flechner L., Su L., Hogenesch J.B., Montiminy M. Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol. Cell 2003, 11:1101-1108.
18. Cubero B., Scazzocchio C. Two different, adjacent and divergent zinc finger binding sites are necessary for CREA-mediated catabolite repression in the proline gene cluster of Aspergillus nidulans. EMBO J. 1994, 13:407-415.
19. De Groot P.W.J., Roeven R.T.P., Van Griensven L.J.L.D., Visser J., Schaap P.J. Different temporal and spatial expression of two hydrophobin-encoding genes of the edible mushroom Agaricus bisporus. Microbiology 1999, 145:1105-1113.
20. De Groot P.W.J., Schaap P.J., Sonnenberg A.S.M., Visser J., Van Griensven L.J.L.D. The Agaricus bisporus hypA gene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J. Mol. Biol. 1996, 257:1008-1018.
21. Dutta S., Gerhold D.L., Rice M., Germann M., Kmiec E.B. The cloning and over expression of a cruciform binding protein from Ustilago maydis. Biochim. Biophys. Acta 1997, 1352:258-266.
22. Eastwood D.C., Bains N.K., Henderson J., Burton K.S. Genome organization and transcription response to harvest of two metallothionein-like genes in Agaricus bisporus fruiting bodies. J. Microb. Biotechnol. 2011, 21(5):455-463.
23. Eastwood D.C., Kingsnorth C.S., Jones H.E., Burton K.S. Genes with increased transcript levels following harvest of the sporophore of Agaricus bisporus have multiple physiological roles. Mycol. Res. 2001, 105:1223-1230.
24. Eastwood D.C., Mead A., Sergeant M.S., Burton K.S. Statistical modelling of transcript profiles of differentially regulated genes. BMC Mol. Biol. 2008, 9:66.
25. Flegg P.B. Effect of temperature on sporophore initiation and development in Agaricus bisporus. Mushroom Sci. 1979, 10:595-602.
26. Flegg P.B., Wood D.A. Growth and Fruiting. The biology and technology of the cultivated mushroom 1985, 141-178. John Wiley and Son, Chichester, UK. P.B. Flegg, D.M. Spencer, D.A. Wood (Eds.).
27. Flipphi M.J.A., Visser J., van der Veen P., de Graaff L.H. Arabinase gene expression in Aspegillus niger: indications for coordinated regulation. Microbiology 1994, 140:2673-2682.
28. Frieman M.B., Cormack B.P. Multiple sequence signals determine the distribution of glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology 2004, 150(10):3105-3114.
29. Fu Y.H., Marzluf G.A. Cys-3, the positive-acting sulphur regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. J. Biol. Chem. 1990, 256(20):11942-11947.
30. Hammond J.B.W., Nichols R. Carbohydrate metabolism in Agaricus bisporus (Lange) Sing.: changes in soluble carbohydrates during growth of mycelium and sporophore. J. Gen. Microbiol. 1976, 93(2):309-320.
31. Horton J.S., Palmer G.E., Smith W.J. Regulation of dikaryon-expressed genes by FRT1 in the basidiomycete Schizophyllum commune. Fungal Gen. Biol. 1999, 26:33-47.
32. Herrero-Garcia E., Garzia A., Cordobes S., Espeso E.A., Ugalde U. 8-Carbon oxylipins inhibit germination and growth and stimulate aerial conidiation in Aspergillus nidulans. Fungal Biol. 2011, 115:393-400.
33. Hynes J., Muller C.T., Hefin-Jones T., Boddy L. Changes in volatile production during the course of fungal mycelia interactions between Hypholoma fasciculare and Resinicium bicolour. J. Chem. Ecol. 2007, 33(1):43-57.
34. Inada K., Morimoto Y., Arima T., Murata Y., Kamada T. The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics 2001, 157:133-140.
35. Kerr M.K., Martin M., Churchill G.A. Analysis of variance for gene expression microarray data. J. Comput. Biol. 2001, 7(6):819-837.
36. Kinoshita H., Sen K., Iwama H., Samadder P.P., Kurosawa S., Shibai H. Effects of indole and caffeine on cAMP in the ind1 and cfn1 mutant strains of Schizophyllum commune. FEMS Microbiol. Lett. 2002, 206:247-251.
37. 2 sensing with cAMP signalling and virulence. Curr. Biol. 2005, 15:2021-2026.
38. Klis F.M., Caro L.H., Vossen J.H., Kapteyn J.C., Ram A.F., Montijn R.C., et al. Identification and characterization of a major building block in the cell wall of Saccahromyces cerevisiae. Biochem. Soc. Trans. 1997, 25:856-860.
39. Li X.Y., He Z.L., Zhou J.Z. Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation. Nucl Acids Res. 2005, 33:6114-6123.
40. 2 on soil microbial biomass, activity, and diversity in a Chaparral ecosystem. Appl. Environ. Microbiol. 2005, 71:8573-8580.
41. Lugones L.G., Wosten H.A., Wewssels J.G. A hydrophobin (ABH3) specifically secreted by vegetatively growing hyphae of Agaricus bisporus (common white button mushroom). Microbiology 1998, 144:2345-2353.
42. Maeda Y., Tanaka S., Hino J., Kangawa K., Kinoshita T. Human dolichol-phosphate-mannose synthase consists of 3 subunits, DMP1, DMP2 and DMP3. EMBO J. 2000, 19(11):2475-2482.
43. Mehra R.K., Tarbet E.B., Gray W.R., Winge D.R. Metal-specific synthesis of two metallothioneins and y-glutamyl peptides in Candida glabrata. Proc. Nat. Acad. Sci. USA 1988, 85:8815-8819.
44. Mol P.C., Wessels J.G.H. Differences in the wall structure between substrate hyphae and hyphae of fruit-body stipes in Agaricus bisporus. Mycol. Res. 1990, 94:472-479.
45. Moore D., Al-Gharawi A. An elevated level of NADP-linked glutamate dehydrogenase is not a general feature of the caps of agaric sporophores. Trans. Brit. Mycol. Soc. 1976, 66:149-150.
46. Moore D., Ewaze J.O. Activities of some enzymes involved in metabolism of carbohydrate during sporophore development in Coprinus cinereus. J. Gen. Microbiol. 1985, 97:313-322.
47. 2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot. Cell 2006, 5:103-111.
48. Morin E., Kohler A., Baker A., Foulongne-Oriol M., Lombard V., Nagy L.G., et al. The genome sequence of the Button Mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc. Nat. Acad. Sci. USA 2012, 109(43):17501-17506.
49. Muniz M., Riezman H. Intracellular transport of GPI-anchored proteins. EMBO J. 2000, 19:10-15.
50. Mutarelli M., Cicatiello L., Ferraro L., Grober O.M., Ravo M., Facchiano A.M., et al. Time-course analysis of genome-wide gene expression data from hormone-responsive human breast cancer cells. BMC Bioinformat. 2008, 9(2):S12.
51. Nakazawa T., Miyazaki Y., Kaneko S., Shishido K. Stimulative effects of light and a temperature downshift on transcriptional expressions of developmentally regulated genes in the initial stages of fruiting-body formation of the basidiomycetous mushroom Lentiunula edodes. FEMS Microbiol. Lett. 2008, 289:67-71.
52. Nemčovič M., Jakubikova J., Víden I., Farka V. Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol. Lett. 2008, 284:231-236.
53. Niederpruem D.J. Role of carbon dioxide in the fruiting of Schizophyllum commune. J. Bacteriol. 1963, 85:1300-1308.
54. Noble R., Dobrovin-Pennington A., Hobbs P., Rodger A., Pederby J. Volatile C8 compounds and pseudomonads influence primordium formation of Agaricus bisporus. Mycologia 2009, 101:591-593.
55. Noble R., Fermor T.R., Lincoln S., Dobrovin-Pennington A., Evered C., Mead A., et al. Primordia initiation of mushroom (Agaricus bisporus) strains on axenic casing materials. Mycologia 2003, 95:620-629.
56. Noor S., Punekar N.S. Allosteric NADP-glutamate dehydrogenase from aspergilla: purification, characterization and implications for metabolic regulation at the carbon-nitrogen interface. Microbiology 2005, 151:1409-1419.
57. Oakley A.J., Yamada T., Liu D., Coggan M., Clark A.G., Board P.G. The identification and structural characterization of C7orf24 as γ-glutamyl cyclotransferase. J. Biol. Chem. 2008, 283(32):22031-22042.
58. Ohm R.A., de Jong J.F., de Bekker C., Wosten H.A.B., Lugones L.G. Transcription factor genes of Schizophyllum commune involved in the regulation of mushroom formation. Mol. Microbiol. 2011, 81(6):1433-1445.
59. Ohtaki S., Maeda H., Tanknhashi T., Yamagata Y., Hasegawa F., Gomi K., et al. Novel hydrophobic surface binding protein, HsbA, produced by Aspergillus oryzae. Appl. Environ. Microbiol. 2006, 72(4):2407-2413.
60. Okumura T., Makiguchi H., Makita Y., Yamashita R., Nakai K. Melina II: a web tool for comparisons among several predictive algorithms to find potential motifs from promoter regions. Nucl. Acid Res. 2007, 35:227-231.
61. Palmer G.E., Horton J.S. Mushrooms by magic: making connections between signal transduction and fruiting body development in the basidiomycete fungus Schizophyllum commune. FEMS Microbiol. Lett. 2006, 262:1-8.
62. Piquemal M., Latche J.C., Baldy P. Importance de l'aide glutamique dans la nutrition et la metabolisme d'Agaricus bisporus Lge. Mushroom Sci. 1972, 8:413-424.
63. Rocha C.R., Schroppel K., Harcus D., Marcil A., Dignard D., Taylor B.N., et al. Signalling through adenylyl cyclase is essential for hyphal growth and virulence in the pathogenic fungus Candida albicans. Mol. Biol. Cell 2001, 12:3631-3643.
64. Rosen K.M., Villa-Kormaroff L. An alternative method for the visualisation of RNA in formaldehyde agarose gels. Focus 1993, 12:23-24.
65. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual, 3 2001, Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
66. Sreenivasaprasad S., Eastwood D.C., Browning N., Lewis S.M.J., Burton K.S. Differential expression of a putative riboflavin-aldehyde-forming enzyme (raf) gene during development and post-harvest storage and in different tissue of the sporophore in Agaricus bisporus. Appl. Microbiol. Biotechnol. 2006, 70:470-476.
67. Takagi Y., Katayose Y., Shishido K., 1988. Intracellular levels of cyclic AMP and adenylate cyclase activity during mycelia development in fruiting-body formation in L. edodes. FEMS.
68. Thompson D.S., Carlisle P.L., Kadosh D. Coevolution of morphology and virulence in Candida species. Eukaryot. Cell 2011, 10(9):1173-1182.
69. Tlalka M., Bebber D.P., Darrah P.R., Watkinson S.C., Fricker M.D. Quantifying dynamic resource allocation illuminates foraging strategy in Phanerochaete veluntina. Fungal Genet. Biol. 2008, 45:1111-1121.
70. Tüzen M., Özdemuir, Demirbaş A. Heavy metal bioaccumulation by cultivated Agaricus bisporus from artificially enriched substrates. Z. Lebensm. Unters. Forsch. A. 1998, 206:417-419.
71. Umar M.H., Van Griensven L.J.L.D. Morphological studies on the life span, developmental stages, senescence and death of fruit bodies of Agaricus bisporus. Mycol. Res. 1997, 101:1409-1422.
72. Wagemaker M.J.M., Eastwood D.C., van der Drift C., Jetten M.S.M., Burton K., Van Griensven L.J.L.D., et al. Expression of the urease gene of Agaricus bisporus: a tool for studying fruit body formation and post-harvest development. Appl. Microbiol. Biotechnol. 2006, 71:486-492.
73. Wagemaker M.J.M., Eastwood D.C., van der Drift C., Jetten M.S.M., Burton K., Van Griensven L.J.L.D., et al. Argininosuccinate synthetase and argininosuccinate lyase: two ornithine cycle enzymes from Agaricus bisporus. Mycol. Res. 2007, 111:493-502.
74. Wagemaker M.J.M., Eastwood D.C., Welagen J., van der Drift C., Jetten M.S.M., Burton K., et al. The role of ornithine aminotransferase in fruiting body formation of the mushroom Agaricus bisporus. Mycol. Res. 2007, 111:909-918.
75. Wang X.W., Seed B. Selection of oligonucleotide probes for protein coding sequences. Bioinformatics 2003, 19:796-802.
76. Wosten, H.A.B., Wessels, J.G.H., 2006. The emergence of fruiting bodies in basidiomycetes. In Kües, U., Fisher, R. (Eds.), The Mycota, second ed., Growth differentiation and sexuality. vol. I. Springer, Berlin, Germany, pp. 393-408.
77. Yamada M., Sakuraba S., Shibata K., Taguchi G., Inatomi S., Okazaki M., et al. Isolation and analysis of genes specifically expressed during fruiting body development in the basidiomycete Flammulina velutipes by fluorescence differential display. FEMS Microbiol. Lett. 2006, 254:165-172.
78. Yoon J.-J., Hattori T., Shimada M. A metabolic role of the glyoxylate and tricarboxylic acid cycles for development of copper-tolerant brown-rot fungus Fomitopsis palustris. FEMS Microbiol. Lett. 2002, 217:9-14.
79. Yoon J.-J., Munir E., Miyasou H., Hattori T., Terashita T., Shimada M. A possible role of the key enzymes of the glyoxylate and gluconeogenesis pathways for fruit-body formation of the wood-rotting basidiomycete Flammulina velutipes. Mycoscience 2002, 43:327-332.
80. Zahurak M., Parmigiani G., Yu W., Scharpf R.B., Berman D., Schaeffer E., et al. Pre-processing Agilent microarray data. BMC Bioinformat. 2007, 8:142.