Expression of ustR and the Golgi protease KexB are required for ustiloxin B biosynthesis in Aspergillus oryzae

AMB Express

Volumn 6, Issue 1, 2016, Pages 1-8

  Yoshimi, Akira ^a   Umemura, Myco ^b   Nagano, Nozomi ^c   Koike, Hideaki ^c   Machida, Masayuki ^b   Abe, Keietsu ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Aspergillus oryzae; Fungal C6 type transcription factor; RiPS pathway; Secondary metabolite; Ustiloxin B

Indexed keywords

GENOMIC DNA; KEXB PROTEASE; PROTEINASE; UNCLASSIFIED DRUG; USTILOXIN B;

ARTICLE; ASPERGILLUS ORYZAE; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL GENE; GENE CLUSTER; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; GENOTYPE; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; USTR GENE;

EID: 84957807109     PISSN: None     EISSN: 21910855     Source Type: Journal    
DOI: 10.1186/s13568-016-0181-4     Document Type: Article

References (48)

1. Abe K, Gomi K, Hasegawa F, Machida M. Impact of Aspergillus oryzae genomics on industrial production of metabolites. Mycopathologia. 2006;162:143–53.
2. Akao T, Sano M, Yamada O, Akeno T, Fujii K, Goto K, Ohashi-Kunihiro S, Takase K, Yasukawa-Watanabe M, Yamaguchi K, Kurihara Y, Maruyama J, Juvvadi PR, Tanaka A, Hata Y, Koyama Y, Yamaguchi S, Kitamoto N, Gomi K, Abe K, Takeuchi M, Kobayashi T, Horiuchi H, Kitamoto K, Kashiwagi Y, Machida M, Akita O. Analysis of expressed sequence tags from the fungus Aspergillus oryzae cultured under different conditions. DNA Res. 2007;14:47–57.
3. Amare MG, Keller NP. Molecular mechanisms of Aspergillus flavus secondary metabolism and development. Fung Genet Biol. 2014;66:11–8.
4. Barbesgaard P, Heldt-Hansen H, Diderichsen B. On the safety of Aspergillus oryzae. Appl Microbiol Biotechnol. 1992;36:569–72.
5. Bayram Ö, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Strimeyer S, Kwon N-J, Keller NP, Yu J-H, Braus GH. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science. 2008;320:1504–6.
6. Bok JW, Keller NP. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukariot Cell. 2004;3:527–35.
7. Brown DW, Yu JH, Kelkar HS, Fernandes M, Nesbitt TC, Keller NP, Adams TH, Leonard TJ. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc Natl Acad Sci USA. 1996;93:1418–22.
8. Chang P-K, Ehrlich KC, Yu J, Bhatnagar D, Cleveland TE. Increased expression of Aspergillus parasiticusaflR, encoding a sequence-specific DNA-binding protein, relieves nitrate inhibition of aflatoxin biosynthesis. Appl Environ Microbiol. 1995;61:2372–7.
9. FAO/WHO. Committee on food additives 31. Geneva: World Health Organization Technical Report Series; 1987.
10. Fujioka T, Mizutani O, Furukawa K, Sato N, Yoshimi A, Yamagata Y, Nakajima T, Abe K. MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukariot Cell. 2007;6:1497–510.
11. 2+-dependent serine protease. Proc Natl Acad Sci USA. 1989;86:1434–8.
12. Gomi K, Akeno T, Minetoki T, Ozeki K, Kumagai C, Okazaki N, Iimura Y. Molecular cloning and characterization of a transcriptional activator gene, amyR, involved in the amylolytic gene expression in Aspergillus oryzae. Biosci Biotechnol Biochem. 2000;64:816–27.
13. Johnson RD, Lane GA, Koulman A, Gao M, Fraser K, Fleetwood DJ, Voisey CR, Dyer JM, Pratt J, Christensen M, Simpson WR, Bryan GT, Johnson LJ. A novel family of cyclic oligopeptides derived from ribosomal peptide synthesis of an in planta-induced gene, gigA, in Epichloë endophytes of grasses. Fung Genet Biol. 2015;85:14–24. doi:10.1016/j.fgb.2015.10.005.
14. Kobayashi T, Abe K, Asai K, Gomi K, Juvvadi PR, Kato M, Kitamoto K, Takeuchi M, Machida M. Genomics of Aspergillus oryzae. Biosci Biotechnol Biochem. 2007;71:646–70.
15. Koiso K, Natori M, Iwasaki S, Sato S, Sonoda R, Fujita Y, Yaegashi H, Sato Z. Ustiloxin: a phytotoxin and a mycotoxin from false smut balls on rice panicles. Tetrahedron Lett. 1992;33:4157–60.
16. Koiso K, Li Y, Iwasaki S, Hanaoka K, Kobayashi T, Sonoda R, Fujita Y, Yaegashi H, Sato Z. Ustiloxins, antimitotic cyclic peptides from false smut balls on rice panicles caused by Ustilaginoidea virens. J Antibiot. 1994;47:765–73.
17. Koiso K, Morisaki N, Yamashita Y, Mitsui Y, Shirai R, Hashimoto Y, Iwasaki S. Isolation and structure of an antimitotic cyclic peptide, Ustiloxin F: chemical interrelation with a homologous peptide, Ustiloxin B. J Antibiot. 1998;51:418–22.
18. Kusumoto K, Yabe K, Nogata T, Ohta H. Transcript of a homolog of aflR, a regulatory gene for aflatoxin synthesis in Aspergillus parasiticus, was not detected in Aspergillus oryzae strains. FEMS Microbiol Lett. 1998;169:303–7.
19. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H. Genome sequencing and analysis of Aspergillus oryzae. Nature. 2005;438:1157–61. doi:10.1038/nature04300.
20. Machida M, Yamada O, Gomi K. Genomics of Aspergillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res. 2008;15:173–83.
21. Marui J, Ohashi-Kunihiro S, Ando T, Nishimura M, Koike H, Machida M. Penicillin biosynthesis in Aspergillus oryzae and its overproduction by genetic engineering. J Biosci Bioeng. 2010;110:8–11. doi:10.1016/j.jbiosc.2010.01.001.
22. 6 transcriptional activator and induced by kojic acid at the transcriptional level. J Biosci Bioeng. 2011;112:40–3.
23. Matsushima K, Chang PK, Yu J, Abe K, Bhatnagar D, Cleveland TE. Pre-termination in aflR of Aspergillus sojae inhibits aflatoxin biosynthesis. Appl Microbiol Biotechnol. 2001a;55:585–9.
24. Matsushima K, Yashiro K, Hanya Y, Abe K, Yabe K, Hamasaki T. Absence of aflatoxin biosynthesis in koji mold (Aspergillus sojae). Appl Microbiol Biotechnol. 2001b;55:771–6.
25. Minetoki T, Nunokawa Y, Gomi K, Kitamoto K, Kumagai C, Tamura G. Deletion analysis of promoter elements of the Aspergillus oryzaeagdA gene encoding α-glucosidase. Curr Genet. 1996;30:432–8.
26. Minetoki T, Kumagai C, Gomi K, Kitamoto K, Takahashi K. Improvement of promoter activity by the introduction of multiple copies of the conserved region III sequence, involved in the efficient expression of Aspergillus oryzae amylase-encoding genes. Appl Microbiol Biotechnol. 1998;50:459–67.
27. Minetoki T, Tsuboi H, Koda A, Ozeki K. Development of high expression system with the improved promoter using the cis-acting element in Aspergillus species. J Biol Macromol. 2003;3:89–96.
28. Mizuno K, Nakamura T, Oshima T, Tanaka S, Matsuo H. Yeast KEX2 gene encodes an endopeptidase homologous to subtilisin-like serine proteases. Biochem Biophys Res Commun. 1988;156:246–54.
29. Mizutani O, Nojima A, Yamamoto M, Furukawa K, Fujioka T, Yamagata Y, Abe K, Nakajima T. Disordered cell integrity signaling caused by disruption of the kexB gene in Aspergillus oryzae. Eukariot Cell. 2004;3:1036–48.
30. Mizutani O, Kudo Y, Saito A, Matsuura T, Inoue H, Abe K, Gomi K. A defect of LigD (human Lig4 homolog) for nonhomologous end joining significantly improves efficiency of gene-targeting in Aspergillus oryzae. Fung Genet Biol. 2008;45:878–89.
31. Noguchi Y, Sano M, Kanamaru K, Ko T, Takeuchi M, Kato M, Kobayashi T. Genes regulated by AoXlnR, the xylanolytic and cellulolytic transcriptional regulator, in Aspergillus oryzae. Appl Microbiol Biotechnol. 2009;85:141–54.
32. 6 transcriptional activator, controls the β-mannan utilization system in Aspergillus oryzae. Fungal Genet Biol. 2012;49:987–95.
33. Payne GA, Nystrom GJ, Bhatnagar D, Cleveland TE, Woloshuk CP. Cloning of the afl-2 gene involved in aflatoxin biosynthesis from Aspergillus flavus. Appl Environ Microbiol. 1993;59:156–62.
34. Redding K, Holcomb C, Fuller RS. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. J Cell Biol. 1991;113:527–38.
35. Sakai K, Kinoshita H, Shimizu T, Nihira T. Construction of a citrinin gene cluster expression system in heterologous Aspergillus oryzae. J Biosci Bioeng. 2008;106:466–72.
36. Takahashi T, Chang P-K, Matsushima K, Yu J, Abe K, Bhatnagar D, Cleveland TE, Koyama Y. Nonfunctionality of Aspergillus sojae aflR in a strain of Aspergillus parasiticus with a disrupted aflR gene. Appl Environ Microbiol. 2002;68:3737–43.
37. Tamano K, Sano M, Yamane N, Terabayashi Y, Toda T, Sunagawa M, Koike H, Hatamoto O, Umitsuki G, Takahashi T, Koyama Y, Asai R, Abe K, Machida M. Transcriptional regulation of genes on the non-syntenic blocks of Aspergillus oryzae and its functional relationship to solid-state cultivation. Fung Genet Biol. 2008;45:139–51.
38. Tokuoka M, Seshime Y, Fujii I, Kitamoto K, Takahashi T, Koyama Y. Identification of a novel polyketide synthase-nonribosomal peptide synthetase (PKS-NRPS) gene required for the biosynthesis of cyclopiazonic acid in Aspergillusoryzae. Fungal Genet Biol. 2008;45:1608–15.
39. Tsukui T, Nagano N, Umemura M, Kumagai T, Terai G, Machida M, Asai K. Ustiloxins, fungal cyclic peptides, are ribosomally synthesized in Ustilaginoidea virens. Bioinformatics. 2015;31:981–5. doi:10.1093/bioinformatics/btu753.
40. Umemura M, Koike H, Nagano N, Ishii T, Kawano J, Yamane N, Kozone I, Horimoto K, Shin-ya K, Asai K, Yu J, Bennett JW, Machida M. MIDDAS-M: motif-independent de novo detection of secondary metabolite gene clusters through the integration of genome sequencing and transcriptome data. PLoS One. 2013;8:e84028. doi:10.1371/journal.pone.0084028.
41. Umemura M, Nagano N, Koike H, Kawano J, Ishii T, Miyamura Y, Kikuchi M, Yu J, Shin-ya K, Machida M. Characterization of the biosynthetic gene cluster for the ribosomally synthesized cyclic peptide ustiloxin B in Aspergillus flavus. Fungal Genet Biol. 2014;68:23–30. doi:10.1016/j.fgb.2014.04.011.
42. Watson AJ, Fuller LJ, Jeenes DJ, Archer DB. Homologs of aflatoxin biosynthesis genes and sequence of aflR in Aspergillus oryzae and Aspergillus sojae. Appl Environ Microbiol. 1999;65:307–10.
43. Woloshuk CP, Foutz KR, Brewer JF, Bhatnagar D, Cleveland TE, Payne GA. Molecular characterization of aflR, a regulatory locus for aflatoxin biosynthesis. Appl Environ Microbiol. 1994;60:2408–14.
44. Yamada O, Lee BR, Gomi K. Transformation system for Aspergillus oryzae with double auxotrophic mutants, niaD and sC. Biosci Biotech Biochem. 1997;61:1367–9.
45. Yoon J, Maruyama J-I, Kitamoto K. Disruption of ten protease genes in the filamentous fungus Aspergillus oryzae highly improves production of heterologous proteins. Appl Microbiol Biotechnol. 2011;89:747–59.
46. Yoshimi A, Sano M, Inaba A, Kokubun Y, Fujioka T, Mizutani O, Hagiwara D, Fujikawa T, Nishimura M, Yano S, Kasahara S, Shimizu K, Yamaguchi M, Kawakami K, Abe K. Functional analysis of the α-1,3-glucan synthase genes agsA and agsB in Aspergillus nidulans: AgsB is the major α-1,3-glucan synthase in this fungus. PLoS One. 2013;8:e54893. doi:10.1371/journal.pone.0054893.
47. Yoshimi A, Fujioka T, Mizutani O, Marui J, Hagiwara D, Abe K. Mitogen-activated protein kinases MpkA and MpkB independently affect micafungin sensitivity in Aspergillus nidulans. Biosci Biotechnol Biochem. 2015;79:836–44. doi:10.1080/09168451.2014.998619.
48. Zhang Y-Q, Wilkinson H, Keller NP, Tsitsigiannis D. Secondary metabolite gene clusters. In: An Z, editor. Handbook of industrial microbiology. New York: Marcel Dekker; 2005. p. 355–86.