Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Velvet Regulators in Aspergillus spp.

Aspergillus spp.에서의 Velvet 조절자

  • Park, Hee-Soo (School of Food Science and Biotechnology, Institute of Agricultural Science & Technology, Kyungpook National University) ;
  • Yu, Jae-Hyuk (Department of Bacteriology and Genetics, University of Wisconsin)
  • 박희수 (경북대학교 식품공학부, 농업과학기술연구소) ;
  • 유재혁 (위스콘신 주립대학교 미생물학과, 유전학과)
  • Received : 2016.07.21
  • Accepted : 2016.08.25
  • Published : 2016.12.28
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Abstract

Filamentous Aspergillus spp. are the most common fungi in our environment and can be beneficial and/or pathogenic to humans. Many Aspergillus spp. reproduce by forming asexual spores and can synthesize various secondary metabolites. A series of studies has revealed that Velvet regulators are fungus-specific transcription factors coordinating fungal growth, development, and secondary metabolism in the model fungus Aspergillus nidulans. Proteins of the Velvet family form various complexes that play diverse roles in the life cycle of A. nidulans. In other Aspergillus spp., proteins of this family are highly conserved and coordinate asexual development and secondary metabolism. This review summarizes the functions of Velvet proteins in Aspergillus spp.

사상성 진균인 Aspergillus spp.은 환경 속에서 흔히 찾을 수 있는 진균으로 인류에 유익한 역할을 주기도 하지만 병원성을 일으키기도 한다. 대부분의 Aspergillus spp.는 무성 포자를 생성하여 번식을 하며 다양한 이차 대사 산물을 합성한다. 여러 연구에 따르면 Velvet 조절자들은 진균 특이적 전사 인자로 모델 진균인 Aspergillus nidulans의 성장, 분화 및 이차 대사산물 생성 등 다양한 부분에서 중요한 역할을 한다고 보고되었다. 또한 Velvet 단백질들은 다양한 복합체를 형성하며, 이 복합체들은 Aspergillus nidulans에서 다양한 역할을 한다. 다른 Aspergillus spp.에서 Velvet 단백질들은 매우 유사한 구조를 가지며 진균의 무성 생식과 이차 대사를 조절한다. 이번 논문에는 Aspergillus spp.의 Velvet 단백질들의 기능에 대하여 요약하였다.

Keywords

References

  1. Adams TH, Wieser JK, Yu J-H. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62: 35-54.
  2. Ahmed YL, Gerke J, Park H-S, Bayram O, Neumann P, Ni M, et al. 2013. The velvet family of fungal regulators contains a DNA-binding domain structurally similar to NF-kappaB. PLoS Biol. 11: e1001750. https://doi.org/10.1371/journal.pbio.1001750
  3. Amaike S, Keller NP. 2009. Distinct roles for VeA and LaeA in development and pathogenesis of Aspergillus flavus. Eukaryot. Cell 8: 1051-1060. https://doi.org/10.1128/EC.00088-09
  4. Atoui A, Kastner C, Larey CM, Thokala R, Etxebeste O, Espeso EA, et al. 2010. Cross-talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet. Biol. 47: 962-972. https://doi.org/10.1016/j.fgb.2010.08.007
  5. Baidya S, Duran RM, Lohmar JM, Harris-Coward PY, Cary JW, Hong SY, et al. 2014. VeA is associated with the response to oxidative stress in the aflatoxin producer Aspergillus flavus. Eukaryot. Cell 13: 1095-1103. https://doi.org/10.1128/EC.00099-14
  6. Bayram O, Bayram OS, Ahmed YL, Maruyama J, Valerius O, Rizzoli SO, et al. 2012. The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet. 8: e1002816. https://doi.org/10.1371/journal.pgen.1002816
  7. Bayram O, Braus GH. 2012. Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36: 1-24. https://doi.org/10.1111/j.1574-6976.2011.00285.x
  8. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, et al. 2008. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506. https://doi.org/10.1126/science.1155888
  9. Bennett JW. 2010. An Overview of the Genus Aspergillus. Aspergillus: Molecular Biology and Genomics 1-17.
  10. Beyhan S, Gutierrez M, Voorhies M, Sil A. 2013. A temperature-responsive network links cell shape and virulence traits in a primary fungal pathogen. PLoS Biol. 11: e1001614. https://doi.org/10.1371/journal.pbio.1001614
  11. Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, et al. 2005. The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 15: 1833-1838. https://doi.org/10.1016/j.cub.2005.08.061
  12. Bok JW, Keller NP. 2004. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot. Cell 3: 527-535. https://doi.org/10.1128/EC.3.2.527-535.2004
  13. Bok JW, Soukup AA, Chadwick E, Chiang YM, Wang CC, Keller NP. 2013. VeA and MvlA repression of the cryptic orsellinic acid gene cluster in Aspergillus nidulans involves histone 3 acetylation. Molecul. Microbiol. 89: 963-974. https://doi.org/10.1111/mmi.12326
  14. Calvo AM. 2008. The VeA regulatory system and its role in morphological and chemical development in fungi. Fungal Genet. Biol. 45: 1053-1061. https://doi.org/10.1016/j.fgb.2008.03.014
  15. Calvo AM, Bok J, Brooks W, Keller NP. 2004. veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl. Environ. Microbiol. 70: 4733-4739. https://doi.org/10.1128/AEM.70.8.4733-4739.2004
  16. Calvo AM, Wilson RA, Bok JW, Keller NP. 2002. Relationship between secondary metabolism and fungal development. Microbiol. Mol. Biol. Rev. 66: 447-459. https://doi.org/10.1128/MMBR.66.3.447-459.2002
  17. Cary JW, Harris-Coward PY, Ehrlich KC, Di Mavungu JD, Malysheva SV, De Saeger S, et al. 2014. Functional characterization of a veA-dependent polyketide synthase gene in Aspergillus flavus necessary for the synthesis of asparasone, a sclerotium-specific pigment. Fungal Genet. Biol. 64: 25-35. https://doi.org/10.1016/j.fgb.2014.01.001
  18. Casselton L, Zolan M. 2002. The art and design of genetic screens: filamentous fungi. Nat. Rev. Genet. 3: 683-697. https://doi.org/10.1038/nrg889
  19. Chang PK, Scharfenstein LL, Li P, Ehrlich KC. 2013. Aspergillus flavus VelB acts distinctly from VeA in conidiation and may coordinate with FluG to modulate sclerotial production. Fungal Genet. Biol. 58-59: 71-79. https://doi.org/10.1016/j.fgb.2013.08.009
  20. Crespo-Sempere A, Marin S, Sanchis V, Ramos AJ. 2013. VeA and LaeA transcriptional factors regulate ochratoxin A biosynthesis in Aspergillus carbonarius. Int. J. Food Microbiol. 166: 479-486. https://doi.org/10.1016/j.ijfoodmicro.2013.07.027
  21. Dhingra S, Andes D, Calvo AM. 2012. VeA regulates conidiation, gliotoxin production, and protease activity in the opportunistic human pathogen Aspergillus fumigatus. Eukaryot. Cell 11: 1531-1543. https://doi.org/10.1128/EC.00222-12
  22. Duran RM, Cary JW, Calvo AM. 2007. Production of cyclopiazonic acid, aflatrem, and aflatoxin by Aspergillus flavus is regulated by veA, a gene necessary for sclerotial formation. Appl. Microbiol. Biotechnol. 73: 1158-1168.
  23. Duran RM, Gregersen S, Smith TD, Bhetariya PJ, Cary JW, Harris-Coward PY, et al. 2014. The role of Aspergillus flavus veA in the production of extracellular proteins during growth on starch substrates. Appl. Microbiol. Biotechnol. 98: 5081-5094. https://doi.org/10.1007/s00253-014-5598-6
  24. Ebbole DJ. 2010. The Conidium. Cellular and Molecular Biology of Filamentous Fungi. 577-590.
  25. Geiser DM, Klich MA, Frisvad JC, Peterson SW, Varga J, Samson RA. 2007. The current status of species recognition and identification in Aspergillus. Stud. Mycol. 59: 1-10. https://doi.org/10.3114/sim.2007.59.01
  26. Han KH, Kim JH, Moon H, Kim S, Lee SS, Han DM, et al. 2008. The Aspergillus nidulans esdC (early sexual development) gene is necessary for sexual development and is controlled by veA and a heterotrimeric G protein. Fungal Genet. Biol. 45: 310-318. https://doi.org/10.1016/j.fgb.2007.09.008
  27. Hedtke M, Rauscher S, Rohrig J, Rodriguez-Romero J, Yu Z, Fischer R. 2015. Light-dependent gene activation in Aspergillus nidulans is strictly dependent on phytochrome and involves the interplay of phytochrome and white collar-regulated histone H3 acetylation. Mol. Microbiol. 97: 733-745. https://doi.org/10.1111/mmi.13062
  28. Jeong HY, Han DM, Jahng KY, Chae KS. 2000. The rpl16a gene for ribosomal protein L16A identified from expressed sequence tags is differentially expressed during sexual development of Aspergillus nidulans. Fungal Genet. Biol. 31: 69-78. https://doi.org/10.1006/fgbi.2000.1233
  29. Kafer E. 1965. Origins of translocations in Aspergillus nidulans. Genetics 52: 217-232.
  30. Kamei K, Watanabe A. 2005. Aspergillus mycotoxins and their effect on the host. Med. Mycol. 43: S95-S99. https://doi.org/10.1080/13693780500051547
  31. Kato N, Brooks W, Calvo AM. 2003. The expression of sterigmatocystin and penicillin genes in Aspergillus nidulans is controlled by veA, a gene required for sexual development. Eukaryot. Cell 2: 1178-1186. https://doi.org/10.1128/EC.2.6.1178-1186.2003
  32. Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism - from biochemistry to genomics. Nat. Rev. Microbiol. 3: 937-947. https://doi.org/10.1038/nrmicro1286
  33. Kensler TW, Roebuck BD, Wogan GN, Groopman JD. 2011. Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol. Sci. 120: S28-48. https://doi.org/10.1093/toxsci/kfq283
  34. Kim H, Han K, Kim K, Han D, Jahng K, Chae K. 2002. The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet. Biol. 37: 72-80. https://doi.org/10.1016/S1087-1845(02)00029-4
  35. Krappmann S, Bayram O, Braus GH. 2005. Deletion and allelic exchange of the Aspergillus fumigatus veA locus via a novel recyclable marker module. Eukaryot. Cell 4: 1298-1307. https://doi.org/10.1128/EC.4.7.1298-1307.2005
  36. Krijgsheld P, Bleichrodt R, van Veluw GJ, Wang F, Muller WH, Dijksterhuis J, et al. 2013. Development in Aspergillus. Stud. Mycol. 74: 1-29. https://doi.org/10.3114/sim0006
  37. Marui J, Ohashi-Kunihiro S, Ando T, Nishimura M, Koike H, Machida M. 2010. Penicillin biosynthesis in Aspergillus oryzae and its overproduction by genetic engineering. J. Biosci. Bioeng. 110: 8-11. https://doi.org/10.1016/j.jbiosc.2010.01.001
  38. Mooney JL, Hassett DE, Yager LN. 1990. Genetic analysis of suppressors of the veA1 mutation in Aspergillus nidulans. Genetics 126: 869-874.
  39. Mooney JL, Yager LN. 1990. Light is required for conidiation in Aspergillus nidulans. Genes Dev. 4: 1473-1482. https://doi.org/10.1101/gad.4.9.1473
  40. Ni M, Yu J-H. 2007. A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. PLoS One 2: e970. https://doi.org/10.1371/journal.pone.0000970
  41. Palmer JM, Theisen JM, Duran RM, Grayburn WS, Calvo AM, Keller NP. 2013. Secondary metabolism and development is mediated by LlmF control of VeA subcellular localization in Aspergillus nidulans. PLoS Genet. 9: e1003193. https://doi.org/10.1371/journal.pgen.1003193
  42. Park H-S, Bayram O, Braus GH, Kim SC, Yu J-H. 2012. Characterization of the velvet regulators in Aspergillus fumigatus. Molecul. Microbiol. 86: 937-953. https://doi.org/10.1111/mmi.12032
  43. Park H-S, Nam TY, Han KH, Kim SC, Yu J-H. 2014. VelC positively controls sexual development in Aspergillus nidulans. PLoS One 9: e89883. https://doi.org/10.1371/journal.pone.0089883
  44. Park H-S, Ni M, Jeong K-C, Kim YH, Yu J-H. 2012. The role, interaction and regulation of the velvet regulator VelB in Aspergillus nidulans. PLoS One 7: e45935. https://doi.org/10.1371/journal.pone.0045935
  45. Park H-S, Yu J-H. 2012. Genetic control of asexual sporulation in filamentous fungi. Curr. Opin. Microbiol. 15: 669-677. https://doi.org/10.1016/j.mib.2012.09.006
  46. Park H-S, Yu YM, Lee MK, Maeng PJ, Kim SC, Yu J-H. 2015. Velvetmediated repression of beta-glucan synthesis in Aspergillus nidulans spores. Sci. Rep. 5: 10199. https://doi.org/10.1038/srep10199
  47. Park HS, Yu JH. 2016. Developmental regulators in Aspergillus fumigatus. J. Microbiol. 54: 223-231. https://doi.org/10.1007/s12275-016-5619-5
  48. Purschwitz J, Muller S, Fischer R. 2009. Mapping the interaction sites of Aspergillus nidulans phytochrome FphA with the global regulator VeA and the White Collar protein LreB. Mol. Genet. Genomics 281: 35-42. https://doi.org/10.1007/s00438-008-0390-x
  49. Purschwitz J, Muller S, Kastner C, Schoser M, Haas H, Espeso EA, et al. 2008. Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr. Biol. 18: 255-259. https://doi.org/10.1016/j.cub.2008.01.061
  50. Reverberi M, Ricelli A, Zjalic S, Fabbri AA, Fanelli C. 2010. Natural functions of mycotoxins and control of their biosynthesis in fungi. Appl. Microbiol. Biotechnol. 87: 899-911. https://doi.org/10.1007/s00253-010-2657-5
  51. Reyes-Dominguez Y, Bok JW, Berger H, Shwab EK, Basheer A, Gallmetzer A, et al. 2010. Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans. Mol. Microbiol. 76: 1376-1386. https://doi.org/10.1111/j.1365-2958.2010.07051.x
  52. Roberts RG. 2013. The velvet underground emerges. PLoS Biol. 11: e1001751. https://doi.org/10.1371/journal.pbio.1001751
  53. Rogers S, Wells R, Rechsteiner M. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234: 364-368. https://doi.org/10.1126/science.2876518
  54. Roze LV, Chanda A, Laivenieks M, Beaudry RM, Artymovich KA, Koptina AV, et al. 2010. Volatile profiling reveals intracellular metabolic changes in Aspergillus parasiticus: veA regulates branched chain amino acid and ethanol metabolism. BMC Biochem. 11: 33. https://doi.org/10.1186/1471-2091-11-33
  55. Sarikaya-Bayram O, Bayram O, Feussner K, Kim JH, Kim HS, Kaever A, et al. 2014. Membrane-bound methyltransferase complex VapA-VipC-VapB guides epigenetic control of fungal development. Dev. Cell 29: 406-420. https://doi.org/10.1016/j.devcel.2014.03.020
  56. Sarikaya-Bayram O, Palmer JM, Keller N, Braus GH, Bayram O. 2015. One Juliet and four Romeos: VeA and its methyltransferases. Front. Microbiol. 6: 1.
  57. Sarikaya Bayram O, Bayram O, Valerius O, Park H-S, Irniger S, Gerke J, et al. 2010. LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet. 6: e1001226. https://doi.org/10.1371/journal.pgen.1001226
  58. Sprote P, Brakhage AA. 2007. The light-dependent regulator velvet A of Aspergillus nidulans acts as a repressor of the penicillin biosynthesis. Arch. Microbiol. 188: 69-79. https://doi.org/10.1007/s00203-007-0224-y
  59. Stinnett SM, Espeso EA, Cobeno L, Araujo-Bazan L, Calvo AM. 2007. Aspergillus nidulans VeA subcellular localization is dependent on the importin alpha carrier and on light. Mol. Microbiol. 63: 242-255. https://doi.org/10.1111/j.1365-2958.2006.05506.x
  60. Timberlake WE. 1990. Molecular genetics of Aspergillus development. Ann. Rev. Genet. 24: 5-36. https://doi.org/10.1146/annurev.ge.24.120190.000253
  61. Todd RB, Hynes MJ, Andrianopoulos A. 2006. The Aspergillus nidulans rcoA gene is required for veA-dependent sexual development. Genetics 174: 1685-1688. https://doi.org/10.1534/genetics.106.062893
  62. Tsitsigiannis DI, Zarnowski R, Keller NP. 2004. The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. J. Biol. Chem. 279: 11344-11353. https://doi.org/10.1074/jbc.M310840200
  63. Vienken K, Scherer M, Fischer R. 2005. The Zn(II)2Cys6 putative Aspergillus nidulans transcription factor repressor of sexual development inhibits sexual development under low-carbon conditions and in submersed culture. Genetics 169: 619-630. https://doi.org/10.1534/genetics.104.030767
  64. Wang F, Dijksterhuis J, Wyatt T, Wosten HA, Bleichrodt RJ. 2015. VeA of Aspergillus niger increases spore dispersing capacity by impacting conidiophore architecture. Antonie van Leeuwenhoek. 107: 187-199. https://doi.org/10.1007/s10482-014-0316-z
  65. Yager LN. 1992. Early developmental events during asexual and sexual sporulation in Aspergillus nidulans. Biotechnology 23: 19-41.
  66. Yu J-H. 2006. Heterotrimeric G protein signaling and RGSs in Aspergillus nidulans. J. Microbiol. 44: 145-154.
  67. Yu J-H, Keller N. 2005. Regulation of secondary metabolism in filamentous fungi. Ann. Rev. Phytopathol. 43: 437-458. https://doi.org/10.1146/annurev.phyto.43.040204.140214

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