Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Genome Organization and Transcription Response to Harvest of Two Metallothionein-Like Genes in Agaricus bisporus Fruiting Bodies

  • Eastwood, Daniel C. (Department of Bioscience, College of Science, University of Swansea) ;
  • Bains, Navdeep K. (Warwick HRI, University of Warwick) ;
  • Henderson, Janey (School of Natural and Environmental Sciences, Coventry University) ;
  • Burton, Kerry S. (Warwick HRI, University of Warwick)
  • Received : 2010.07.19
  • Accepted : 2011.03.02
  • Published : 2011.05.28
Download PDF
⟨ Previous Next ⟩

Abstract

Metallothioneins are a class of small cysteine-rich proteins that have been associated with increased tolerance to metal and oxidative stresses in animals, plants, and fungi. We investigated a metallothionein-like (mt-like) gene shown previously to be upregulated in fruiting bodies of the fungus Agaricus bisporus in response to post-harvest storage. Analysis of an A. bisporus genomic DNA cosmid library identified two similar mt-like genes (met1 and met2) arranged as a bidirectional gene pair transcribed from the same promoter region. The promoter contained regulatory elements including 9 metal responsive elements and a CAAT box region 220 bp downstream of met1 that showed striking similarity to a feature in Coprinopsis cinerea mt-like gene promoters. Transcriptional analysis showed that both met genes are significantly and rapidly (within 3 hours) upregulated during post-harvest storage and expression is significantly greater in stipe and cap tissues compared with the gills. However, a strong directionality of the promoter was demonstrated, as transcript levels of met1 were at least two orders of magnitude greater than those of met2 in all samples tested.

Keywords

References

  1. Averbeck, N. B., C. Borghouts, A. Hamann, V. Specke, and H. D. Osiewacz. 2001. Molecular control of copper homeostasis in filamentous fungi: Increased expression of a metallothionein gene during aging of Podospora anserine. Mol. Gen. Genet. 264: 604-612. https://doi.org/10.1007/s004380000346
  2. Bellion, M., M. Courbot, C. Jacob, F. Guinet, D. Blaudez, and M. Chalot. 2007. Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum. New Phytol. 174: 151-158. https://doi.org/10.1111/j.1469-8137.2007.01973.x
  3. Bertini, A., H. Sigel, and I. Sigel (Eds.). 2001. Handbook on Metalloproteins. I. CRC Press.
  4. Burns, C., K. E. Gregory, M. Kirby, M. K. Cheung, M. Riquelme, T. J. Elliott, M. P. Challen, A. Bailey, and G. D. Foster. 2005. Efficient GFP expression in the mushrooms Agaricus bisporus and Coprinus cinereus requires introns. Fungal Genet. Biol. 42: 191-199. https://doi.org/10.1016/j.fgb.2004.11.005
  5. Burton, K. S., M. D. Partis, D. A. Wood, and C. F. Thurston. 1997. Accumulation of serine proteinase in senescent sporophores of the cultivated mushroom, Agaricus bisporus. Mycol. Res. 101: 146-152. https://doi.org/10.1017/S0953756296002316
  6. Butt, T. R., E. J. Sternberg, J. A. Gorman, P. Clark, D. Hamer, M. Rosenberg, and S. T. Crooke. 1984. Copper metallothionein of yeast, structure of gene, and regulation of expression. Proc. Natl. Acad. Sci. USA 81: 3332-3336 https://doi.org/10.1073/pnas.81.11.3332
  7. Choi, D., H. M. Kim, H. K. Yun, J. A. Park, W. T. Kim, and S. H. Bok. 1996. Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiol. 112: 353-359. https://doi.org/10.1104/pp.112.1.353
  8. Clemens, S. 2001. Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212: 475-486. https://doi.org/10.1007/s004250000458
  9. Cobbett, C. S. 2000. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123: 825-832. https://doi.org/10.1104/pp.123.3.825
  10. Cobbett, C. S. and P. Goldsbourgh. 2002. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53: 159-182. https://doi.org/10.1146/annurev.arplant.53.100301.135154
  11. De Groot, P. W. J., P. J. Schaap, L. J. L. D. van Griensven, and J. Visser. 1997. Isolation of developmentally regulated genes from the edible mushroom Agaricus bisporus. Microbiology. 143: 1993-2001. https://doi.org/10.1099/00221287-143-6-1993
  12. Eastwood, D. C., C. S. Kingsnorth, H. E. Jones, and K. S. Burton. 2001. Genes with increased transcript levels following harvest of the sporophore of Agaricus bisporus have multiple physiological roles. Mycol. Res. 105: 1223-1230. https://doi.org/10.1016/S0953-7562(08)61993-0
  13. Eastwood, D. C., A. Mead, M. J. Sergeant, and K. S. Burton. 2008. Statistical modelling of transcript profiles of differentially regulated genes. BMC Mol. Biol. 9: 66. https://doi.org/10.1186/1471-2199-9-66
  14. Esser, J. and H. Brunnert. 1986. Isolation and partial purification of cadmium-binding components from fruiting bodies of Agaricus bisporus. Environ. Pollut. A 41: 263-275. https://doi.org/10.1016/0143-1471(86)90074-7
  15. Faraco, V., P. Giardina, and G. Sannia. 2003. Metal-responsive elements in Pleurotus ostreatus laccase gene promoters. Microbiology 149: 2155-2162. https://doi.org/10.1099/mic.0.26360-0
  16. Goidin, D., A. Mamessier, M.-J. Statquet, D. Schmitt, and O. Berthier-Vergnes. 2000. Ribosomal 18S RNA prevails over glyceraldehyde-3-phosphate dehydrogenase and $\beta$-actin genes as internal standards for quantitative comparison of mRNA levels in invasive and noninvasive human melanoma cell subpopulations. Anal. Biochem. 295: 17-21.
  17. Hammond, J. B. W. 1979. Changes in composition of harvested mushrooms (Agaricus bisporus). Phytochemistry 18: 415-418. https://doi.org/10.1016/S0031-9422(00)81878-6
  18. Hammond, J. B. W. and R. Nichols. 1975. Changes in respiration and soluble carbohydrates during the post-harvest storage of mushrooms (Agaricus bisporus). J. Sci. Food Agric. 26: 835-842. https://doi.org/10.1002/jsfa.2740260615
  19. Hammond, J. B. W. and R. Nichols. 1976. Carbohydrate metabolism in Agaricus bisporus (Lange) Sign.: Changes in soluble carbohydrates during growth of mycelium and fruiting body. J. Gen. Microbiol. 93: 309-320. https://doi.org/10.1099/00221287-93-2-309
  20. Humphrey, T. and N. J. Proudfoot. 1988. A beginning to the biochemistry of polyadenylation. Trends Genet. 4: 243-245. https://doi.org/10.1016/0168-9525(88)90028-5
  21. Kalitsis, P. and R. Saffery. 2009. Inherent promoter bidirectionality facilitates maintenance of sequence integrity and transcription of parasitic DNA in mammalian genomes. BMC Genomics 10: 498. https://doi.org/10.1186/1471-2164-10-498
  22. Kensche, P. R., M. Oti, B. E. Dutilh, and M. A. Huynen. 2008. Conservation of divergent transcription in fungi. Trends Genet. 24: 207-211. https://doi.org/10.1016/j.tig.2008.02.003
  23. Kingsnorth, C. S., D. C. Eastwood, and K. S. Burton. 2001. Cloning and postharvest expression in serine proteinase transcripts in the cultivated mushroom Agaricus bisporus. Fungal Genet. Biol. 32: 135-144. https://doi.org/10.1006/fgbi.2001.1257
  24. Lanfranco, L., A. Bolchi, E. Cesale Ros, S. Ottonello, and P. Bonfontane. 2002. Differential expression of a metallothionein gene during presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol. 130: 58-67. https://doi.org/10.1104/pp.003525
  25. Lin, J. M., P. J. Collins, N. D. Trinklein, Y. Fu, H. Xi, R. M. Myers, and Z. Weng. 2008. Transcription factor binding and modified histones in human bidirectional promoters. Genome Res. 17: 818-827.
  26. Liu, X.-D. and D. J. Thiele. 1997. Yeast metallothionein gene expression in response to metals and oxidative stress. Methods 11: 289-299. https://doi.org/10.1006/meth.1996.0423
  27. Lorang, J. M., R. P. Tuori, J. P. Martinez, T. L. Sawyer, R. S. Redman, J. A. Rollins, et al. 2001. Green fluorescent protein is lighting up fungal biology. Appl. Environ. Microbiol. 67: 1987- 1994. https://doi.org/10.1128/AEM.67.5.1987-1994.2001
  28. Mehra, R. K., J. R. Garey, and D. R. Winge. 1990. Selective and tandem amplification of a member of the metallothionein gene family in Candida glabrata. J. Biol. Chem. 265: 6369-6375.
  29. Mehra, R. K., E. B. Tarbet, W. R. Garey, and D. R. Winge. 1998. Metal-specific synthesis of two metallothioneins and $\gamma$ glutamyl peptides in Candida glabrata. Proc. Natl. Acad. Sci. USA 85: 8815-8819.
  30. Munger, K., U. A. Germann, and K. Lerch. 1987. The Neurospora crassa metallothionein gene: Regulation of expression and chromosomal location. J. Biol. Chem. 262: 7363-7367.
  31. Munger, K. and K. Lerch. 1985. Copper metallothionein from the fungus Agaricus bisporus: Chemical and spectroscopic properties. Biochemistry 24: 6751-6756. https://doi.org/10.1021/bi00345a004
  32. Nordberg, M. 1998. Metallothioneins: Historical review and state of knowledge. Talanta 46: 243-254. https://doi.org/10.1016/S0039-9140(97)00345-7
  33. Osiewacz, H. D. 2002. Mitochondrial functions and aging. Gene 286: 65-71. https://doi.org/10.1016/S0378-1119(01)00804-6
  34. Pointkivska, H., M. Q. Yang, D. M. Larkin, H. A. Lewin, J. Reecy, and L. Elnitsky. 2009. Cross-species mapping of bidirectional promoters enables prediction of unannotated 5' UTR's and identification of species-specific transcripts. BMC Genomics 10: 189. https://doi.org/10.1186/1471-2164-10-189
  35. Ramesh, G., G. K. Podila, G. Gay, R. Marmeisse, and M. S. Reddy. 2009. Different patterns of regulation for copper and cadmium metallothioneins of the ectomycorrhiza fungus Hebeloma clyndrosporum. Appl. Environ. Microbiol. 75: 2266-2274. https://doi.org/10.1128/AEM.02142-08
  36. Reddy Dhadi, S., N. Krom, and W. Ramakrishna. 2009. Genomewide comparative analysis of putative bidirectional promoters from rice Arabidopsis and Populus. Gene 429: 65-73. https://doi.org/10.1016/j.gene.2008.09.034
  37. Reid, S. J. and G. S. Ross. 1997. Up-regulation of two cDNA clones encoding metallothionein-like proteins in apple fruit during cool storage. Physiol. Plant. 100: 183-189. https://doi.org/10.1111/j.1399-3054.1997.tb03471.x
  38. Rosen, K. M. and L. Villa-Kormaroff. 1993. An alternative method for the visualisation of RNA in formaldehyde agarose gels. Focus 12: 23-24.
  39. Sambrook, J. and D. W. Russell. 2001. Molecular Cloning: A Laboratory Manual. 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  40. Scholtmiejer, K., H. A. B. Wösten, J. Springer, and J. G. Wessels. 2001. Effect of introns and AT-rich sequences on expression of the bacterial hygromycin B resistance gene in the basidiomycete Schizophyllum commune. Appl. Environ. Microbiol. 67: 481-483 https://doi.org/10.1128/AEM.67.1.481-483.2001
  41. Stillman, M. J. 1995. Metallothioneins. Coord. Chem. Rev. 144: 461-511.
  42. Stijve, T. and R. Besson. 1976. Mercury, cadmium, lead and selenium content of mushroom species belonging to the genus Agaricus. Chemosphere 2: 151-158.
  43. Thiele, D. J. 1992. Metal regulated transcription in eukaryotes. Nucleic Acids Res. 20: 1183-1191. https://doi.org/10.1093/nar/20.6.1183
  44. Trinklein, N. D., S. Force Aldred, S. J. Hartman, D. I. Schroeder, R. P. Otillar, and R. M. Myers. 2004. An abundance of bidirectional promoters in the human genome. Genome Res. 14: 62-66.
  45. Unkles, S. E. 1992. Gene organization in industrial filamentous fungi, pp. 28-53. In J. R. Kinghorn and G. Turner (eds.). Applied Molecular Genetics of Filamentous Fungi. University Press, Cambridge.
  46. Voth, H., A. Oberthuer, T. Simon, Y. Kahlert, F. Berthold, and M. Fischer. 2009. Co-regulated expression of HAND2 and DEIN by a bidirectional promoter with asymmetrical activity in neuroblastoma. BMC Molec. Biol. 10: 28. https://doi.org/10.1186/1471-2199-10-28
  47. Wagemaker, M. J. M., D. C. Eastwood, C. van der Drift, M. S. M Jetten, K. S. Burton, L. J. L. D Van Griensven, and H. J. M. Op den Camp. 2006. Expression of the urease gene of Agaricus bisporus: A tool for studying fruiting body formation and postharvest development. Appl. Microbiol. Biotechnol. 71: 486-492. https://doi.org/10.1007/s00253-005-0185-5
  48. Wagemaker, M. J. M., D.C. Eastwood, C. van der Drift, M. S. M. Jetten, K. S. Burton, L. J. L. D van Griensven, and H. J. M. Op den Camp. 2007. Argininosuccinate synthetase and argininosuccinate lyase: Two ornithine cycle enzymes from Agaricus bisporus. Mycol. Res. 111: 493-502. https://doi.org/10.1016/j.mycres.2007.01.016
  49. Yagüe, E., M. Mehak-Zunic, L. Morgan, D. A. Wood, and C. F. Thurston. 1997. Expression of CEL2 and CEL4, two proteins from Agaricus bisporus with similarity to fungal cellobiohydrolase I and $\beta$-mannanase, respectively, is regulated by the carbon source. Microbiology 143: 239-244. https://doi.org/10.1099/00221287-143-1-239
  50. Zhou, P., M. S. Szczypka, T. Sosinowski, and D. J. Thiele. 1992. Expression of a yeast metallothionein gene family is activated by a single metalloregulatory transcription factor. Mol. Cell. Biol. 12: 3766-3775.

Cited by

  1. Gene expression and metabolite changes during Tuber magnatum fruiting body storage vol.60, pp.4, 2011, https://doi.org/10.1007/s00294-014-0434-1