The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Histone Acetylation in Fungal Pathogens of Plants

  • Jeon, Junhyun (Department of Agricultural Biotechnology, College of Agriculture and Life science, Seoul National University) ;
  • Kwon, Seomun (Department of Agricultural Biotechnology, College of Agriculture and Life science, Seoul National University) ;
  • Lee, Yong-Hwan (Department of Agricultural Biotechnology, College of Agriculture and Life science, Seoul National University)
  • Received : 2014.01.16
  • Accepted : 2014.02.07
  • Published : 2014.03.01
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Abstract

Acetylation of histone lysine residues occurs in different organisms ranging from yeast to plants and mammals for the regulation of diverse cellular processes. With the identification of enzymes that create or reverse this modification, our understanding on histone acetylation has expanded at an amazing pace during the last two decades. In fungal pathogens of plants, however, the importance of such modification has only just begun to be appreciated in the recent years and there is a dearth of information on how histone acetylation is implicated in fungal pathogenesis. This review covers the current status of research related to histone acetylation in plant pathogenic fungi and considers relevant findings in the interaction between fungal pathogens and host plants. We first describe the families of histone acetyltransferases and deacetylases. Then we provide the cases where histone acetylation was investigated in the context of fungal pathogenesis. Finally, future directions and perspectives in epigenetics of fungal pathogenesis are discussed.

Keywords

References

  1. Allard, S., Utley, R. T., Savard, J., Clarke, A., Grant, P., Brandl, C. J., Pillus, L., Workman, J. L. and Cote, J. 1999. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 18:5108-5119. https://doi.org/10.1093/emboj/18.18.5108
  2. Allfrey, V. G., Faulkner, R. and Mirsky, A. E. 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 51:786-794. https://doi.org/10.1073/pnas.51.5.786
  3. Allis, C. D., Berger, S. L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R., Shilatifard, A., Workman, J. and Zhang, Y. 2007. New nomenclature for chromatin-modifying enzymes. Cell 131: 633-636. https://doi.org/10.1016/j.cell.2007.10.039
  4. Babiarz, J. E., Halley, J. E. and Rine, J. 2006. Telomeric heterochromatin boundaries require NuA4-dependent acetylation of histone variant H2A.Z in Saccharomyces cerevisiae. Genes Dev. 20:700-710. https://doi.org/10.1101/gad.1386306
  5. Bannister, A. J. and Kouzarides, T. 2011. Regulation of chromatin by histone modifications. Cell Res. 21:381-395. https://doi.org/10.1038/cr.2011.22
  6. Brosch, G., Ransom, R., Lechner, T., Walton, J. D. and Loidl, P. 1995. Inhibition of maize histone deacetylases by HC toxin, the host-selective toxin of Cochliobolus carbonum. Plant Cell 7:1941-1950. https://doi.org/10.1105/tpc.7.11.1941
  7. Chen, C. C., Carson, J. J., Feser, J., Tamburini, B., Zabaronick, S., Linger, J. and Tyler, J. K. 2008. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134:231-243. https://doi.org/10.1016/j.cell.2008.06.035
  8. Chookajorn, T., Dzikowski, R., Frank, M., Li, F., Jiwani, A. Z., Hartl, D. L. and Deitsch, K. W. 2007. Epigenetic memory at malaria virulence genes. Proc. Natl. Acad. Sci. USA 104:899-902. https://doi.org/10.1073/pnas.0609084103
  9. Clarke, A. S., Lowell, J. E., Jacobson, S. J. and Pillus, L. 1999. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell. Biol. 19:2515-2526. https://doi.org/10.1128/MCB.19.4.2515
  10. Croken, M. M., Nardelli, S. C. and Kim, K. 2012. Chromatin modifications, epigenetics, and how protozoan parasites regulate their lives. Trends Parasitol. 28:202-213. https://doi.org/10.1016/j.pt.2012.02.009
  11. Ding, S., Mehrabi, R., Koten, C., Kang, Z., Wei, Y., Seong, K., Kistler, H. C. and Xu, J. R. 2009. Transducin beta-like gene FTL1 is essential for pathogenesis in Fusarium graminearum. Eukaryot. Cell 8:867-876. https://doi.org/10.1128/EC.00048-09
  12. Ding, S. L., Liu, W., Iliuk, A., Ribot, C., Vallet, J., Tao, A., Wang, Y., Lebrun, M. H. and Xu, J. R. 2010. The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22:2495-2508. https://doi.org/10.1105/tpc.110.074302
  13. Driscoll, R., Hudson, A. and Jackson, S. P. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315:649-652. https://doi.org/10.1126/science.1135862
  14. Gartenberg, M. R. 2000. The Sir proteins of Saccharomyces cerevisiae:mediators of transcriptional silencing and much more. Curr. Opin. Microbiol. 3:132-137. https://doi.org/10.1016/S1369-5274(00)00064-3
  15. Gomez-Diaz, E., Jorda, M., Peinado, M. A. and Rivero, A. 2012. Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog. 8:e1003007. https://doi.org/10.1371/journal.ppat.1003007
  16. Grant, P. A., Duggan, L., Cote, J., Roberts, S. M., Brownell, J. E., Candau, R., Ohba, R., Owen-Hughes, T., Allis, C. D., Winston, F., Berger, S. L. and Workman, J. L. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11:1640-1650. https://doi.org/10.1101/gad.11.13.1640
  17. Gregoretti, I. V., Lee, Y. M. and Goodson, H. V. 2004. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338:17-31. https://doi.org/10.1016/j.jmb.2004.02.006
  18. Grimaldi, B., Coiro, P., Filetici, P., Berge, E., Dobosy, J. R., Freitag, M., Selker, E. U. and Ballario, P. 2006. The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol. Biol. Cell. 17:4576-4583. https://doi.org/10.1091/mbc.E06-03-0232
  19. Grozinger, C. M. and Schreiber, S. L. 2002. Deacetylase enzymes: biological functions and the use of small-molecule inhibitors. Chem. Biol. 9:3-16. https://doi.org/10.1016/S1074-5521(02)00092-3
  20. Guarente, L. 2013. Calorie restriction and sirtuins revisited. Genes Dev. 27:2072-2085. https://doi.org/10.1101/gad.227439.113
  21. Hamon, M. A. and Cossart, P. 2008. Histone modifications and chromatin remodeling during bacterial infections. Cell Host Microbe 4:100-109. https://doi.org/10.1016/j.chom.2008.07.009
  22. Han, J., Zhou, H., Horazdovsky, B., Zhang, K., Xu, R. M. and Zhang, Z. 2007. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315:653-655. https://doi.org/10.1126/science.1133234
  23. Howe, L., Auston, D., Grant, P., John, S., Cook, R. G., Workman, J. L. and Pillus, L. 2001. Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 15:3144-3154. https://doi.org/10.1101/gad.931401
  24. Kimura, A., Umehara, T. and Horikoshi, M. 2002. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32:370-377. https://doi.org/10.1038/ng993
  25. Kornberg, R. D. and Lorch, Y. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285-294. https://doi.org/10.1016/S0092-8674(00)81958-3
  26. Kouzarides, T. 2000. Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 19:1176-1179. https://doi.org/10.1093/emboj/19.6.1176
  27. Kwon, H. J., Owa, T., Hassig, C. A., Shimada, J. and Schreiber, S. L. 1998. Depudecin induces morphological reversion of transformed fibroblasts via the inhibition of histone deacetylase. Proc. Natl. Acad. Sci. USA 95:3356-3361. https://doi.org/10.1073/pnas.95.7.3356
  28. Lee, K. K. and Workman, J. L. 2007. Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell. Biol. 8:284-295. https://doi.org/10.1038/nrm2145
  29. Li, B., Carey, M. and Workman, J. L. 2007. The role of chromatin during transcription. Cell 128:707-719. https://doi.org/10.1016/j.cell.2007.01.015
  30. Li, Y., Wang, C., Liu, W., Wang, G., Kang, Z., Kistler, H. C. and Xu, J. R. 2011. The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Mol. Plant- Microbe Interact. 24:487-496. https://doi.org/10.1094/MPMI-10-10-0233
  31. Lopes da Rosa, J., Boyartchuk, V. L., Zhu, L. J. and Kaufman, P. D. 2010. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. USA 107:1594-1599. https://doi.org/10.1073/pnas.0912427107
  32. Luna, E., Bruce, T. J., Roberts, M. R., Flors, V. and Ton, J. 2012. Next-generation systemic acquired resistance. Plant Physiol. 158:844-853. https://doi.org/10.1104/pp.111.187468
  33. Marazzi, I., Ho, J. S. Y., Kim, J., Manicassamy, B., Dewell, S., Albrecht, R. A., Seibert, C. W., Schaefer, U., Jeffrey, K. L., Prinjha, R. K., Lee, K., Garcia-Sastre, A., Roeder, R. G. and Tarakhovsky, A. 2012. Suppression of the antiviral response by an influenza histone mimic. Nature 483:428-433. https://doi.org/10.1038/nature10892
  34. Matsumoto, M., Matsutani, S., Sugita, K., Yoshida, H., Hayashi, F., Terui, Y., Nakai, H., Uotani, N., Kawamura, Y., Matsumoto, K. and et al. 1992. Depudecin: a novel compound inducing the flat phenotype of NIH3T3 cells doubly transformed by ras- and src-oncogene, produced by Alternaria brassicicola. J. Antibiot. 45:879-885. https://doi.org/10.7164/antibiotics.45.879
  35. Meeley, R. B. and Walton, J. D. 1991. Enzymatic Detoxification of HC-toxin, the Host-Selective Cyclic Peptide from Cochliobolus carbonum. Plant Physiol. 97:1080-1086. https://doi.org/10.1104/pp.97.3.1080
  36. Mersfelder, E. L. and Parthun, M. R. 2006. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res. 34:2653-2662. https://doi.org/10.1093/nar/gkl338
  37. Nutzmann, H. W., Reyes-Dominguez, Y., Scherlach, K., Schroeckh, V., Horn, F., Gacek, A., Schumann, J., Hertweck, C., Strauss, J. and Brakhage, A. A. 2011. Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc. Natl. Acad. Sci. USA 108:14282-14287. https://doi.org/10.1073/pnas.1103523108
  38. O'Meara, T. R., Hay, C., Price, M. S., Giles, S. and Alspaugh, J. A. 2010. Cryptococcus neoformans histone acetyltransferase Gcn5 regulates fungal adaptation to the host. Eukaryot. Cell 9:1193-1202.
  39. Park, S., Mori, R. and Shimokawa, I. 2013. Do sirtuins promote mammalian longevity? A critical review on its relevance to the longevity effect induced by calorie restriction. Mol. Cells 35:474-480. https://doi.org/10.1007/s10059-013-0130-x
  40. Pennini, M. E., Pai, R. K., Schultz, D. C., Boom, W. H. and Harding, C. V. 2006. Mycobacterium tuberculosis 19- kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J. Immunol. 176:4323-4330. https://doi.org/10.4049/jimmunol.176.7.4323
  41. Pijnappel, W. W., Schaft, D., Roguev, A., Shevchenko, A., Tekotte, H., Wilm, M., Rigaut, G., Seraphin, B., Aasland, R. and Stewart, A. F. 2001. The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev. 15:2991-3004. https://doi.org/10.1101/gad.207401
  42. Pray-Grant, M. G., Schieltz, D., McMahon, S. J., Wood, J. M., Kennedy, E. L., Cook, R. G., Workman, J. L., Yates, J. R. and Grant, P. A. 2002. The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Mol. Cell. Biol. 22:8774-8786. https://doi.org/10.1128/MCB.22.24.8774-8786.2002
  43. Qutob, D., Chapman, B. P. and Gijzen, M. 2013. Transgenerational gene silencing causes gain of virulence in a plant pathogen. Nat. Commun. 4:1349. https://doi.org/10.1038/ncomms2354
  44. Roze, L. V., Arthur, A. E., Hong, S. Y., Chanda, A. and Linz, J. E. 2007. The initiation and pattern of spread of histone H4 acetylation parallel the order of transcriptional activation of genes in the aflatoxin cluster. Mol. Microbiol. 66:713-726. https://doi.org/10.1111/j.1365-2958.2007.05952.x
  45. Schneider, J., Bajwa, P., Johnson, F. C., Bhaumik, S. R. and Shilatifard, A. 2006. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 281:37270-37274. https://doi.org/10.1074/jbc.C600265200
  46. Sengupta, N. and Seto, E. 2004. Regulation of histone deacetylase activities. J. Cell Biochem. 93:57-67. https://doi.org/10.1002/jcb.20179
  47. Shwab, E. K., Bok, J. W., Tribus, M., Galehr, J., Graessle, S. and Keller, N. P. 2007. Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot. Cell 6:1656-1664.
  48. Slaughter, A., Daniel, X., Flors, V., Luna, E., Hohn, B. and Mauch-Mani, B. 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158:835-843. https://doi.org/10.1104/pp.111.191593
  49. Smith, D. L., Jr., McClure, J. M., Matecic, M. and Smith, J. S. 2007. Calorie restriction extends the chronological lifespan of Saccharomyces cerevisiae independently of the Sirtuins. Aging Cell 6:649-662. https://doi.org/10.1111/j.1474-9726.2007.00326.x
  50. Smith, K. T. and Workman, J. L. 2009. Introducing the acetylome. Nat. Biotechnol. 27:917-919. https://doi.org/10.1038/nbt1009-917
  51. Soukup, A. A., Chiang, Y. M., Bok, J. W., Reyes-Dominguez, Y., Oakley, B. R., Wang, C. C., Strauss, J. and Keller, N. P. 2012. Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production. Mol. Microbiol. 86:314-330. https://doi.org/10.1111/j.1365-2958.2012.08195.x
  52. Suvarna, B. S. 2012. Sirtuins: the future insight. Kathmandu Univ Med. J. (KUMJ) 10:77-82.
  53. Tang, Y., Holbert, M. A., Wurtele, H., Meeth, K., Rocha, W., Gharib, M., Jiang, E., Thibault, P., Verreault, A., Cole, P. A. and Marmorstein, R. 2008. Fungal Rtt109 histone acetyltransferase is an unexpected structural homolog of metazoan p300/CBP. Nat. Struct. Mol. Biol. 15:738-745. https://doi.org/10.1038/nsmb.1448
  54. Taunton, J., Hassig, C. A. and Schreiber, S. L. 1996. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272:408-411. https://doi.org/10.1126/science.272.5260.408
  55. Torres, M. A., Jones, J. D. and Dangl, J. L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141:373-378. https://doi.org/10.1104/pp.106.079467
  56. Tudzynski, P., Heller, J. and Siegmund, U. 2012. Reactive oxygen species generation in fungal development and pathogenesis. Curr. Opin. Microbiol. 15:653-659. https://doi.org/10.1016/j.mib.2012.10.002
  57. Turner, B. M. 2007. Defining an epigenetic code. Nat. Cell. Biol. 9:2-6. https://doi.org/10.1038/ncb0107-2
  58. Verdin, E., Dequiedt, F. and Kasler, H. G. 2003. Class II histone deacetylases: versatile regulators. Trends Genet. 19:286-293. https://doi.org/10.1016/S0168-9525(03)00073-8
  59. Vidal, M. and Gaber, R. F. 1991. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:6317-6327. https://doi.org/10.1128/MCB.11.12.6317
  60. Voss, A. K. and Thomas, T. 2009. MYST family histone acetyltransferases take center stage in stem cells and development. Bioessays 31:1050-1061. https://doi.org/10.1002/bies.200900051
  61. Wang, L., Tang, Y., Cole, P. A. and Marmorstein, R. 2008. Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: implications for histone acetyltransferase evolution and function. Curr. Opin. Struct. Biol. 18:741-747. https://doi.org/10.1016/j.sbi.2008.09.004
  62. Wight, W. D., Kim, K. H., Lawrence, C. B. and Walton, J. D. 2009. Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol. Plant- Microbe Interact. 22:1258-1267. https://doi.org/10.1094/MPMI-22-10-1258
  63. Xin, Q., Gong, Y., Lv, X., Chen, G. and Liu, W. 2013. Trichoderma reesei histone acetyltransferase Gcn5 regulates fungal growth, conidiation, and cellulase gene expression. Curr. Microbiol. 67:580-589. https://doi.org/10.1007/s00284-013-0396-4
  64. Xu, W. T., Edmondson, D. G. and Roth, S. Y. 1998. Mammalian GCN5 and P/CAF acetyltransferases have homologous amino-terminal domains important for recognition of nucleosomal substrates. Mol. Cell. Biol. 18:5659-5669. https://doi.org/10.1128/MCB.18.10.5659
  65. Xue-Franzen, Y., Henriksson, J., Burglin, T. R. and Wright, A. P. 2013. Distinct roles of the Gcn5 histone acetyltransferase revealed during transient stress-induced reprogramming of the genome. BMC Genomics 14:479. https://doi.org/10.1186/1471-2164-14-479
  66. Yang, X. J. and Seto, E. 2008. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell. Biol. 9:206-218. https://doi.org/10.1038/nrm2346
  67. Zhou, C., Zhang, L., Duan, J., Miki, B. and Wu, K. 2005. HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17:1196-1204. https://doi.org/10.1105/tpc.104.028514

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