Disruption of the Aopex11-1 gene involved in peroxisome proliferation leads to impaired woronin body formation in Aspergillus oryzae

Eukaryotic Cell

Volumn 8, Issue 3, 2009, Pages 296-305

  Escaño, Cristopher Salazar ^a   Juvvadi, Praveen Rao ^a,c   Feng, Jie Jin ^b   Takahashi, Tadashi ^b   Koyama, Yasuji ^b   Yamashita, Shuichi ^a   Maruyama, Jun Ichi ^a   Kitamoto, Katsuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b Noda Institute for Scientific Research   (Japan)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

ARTICLE; ASPERGILLUS ORYZAE; CELL ORGANELLE; CLASSIFICATION; GENE SILENCING; GENETICS; METABOLISM; PEROXISOME; PHYLOGENY; ULTRASTRUCTURE;

ASPERGILLUS ORYZAE; FUNGAL PROTEINS; GENE SILENCING; ORGANELLES; PEROXISOMES; PHYLOGENY;

ASPERGILLUS ORYZAE; PEZIZOMYCOTINA;

EID: 61949336473     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00197-08     Document Type: Article

References (49)

1. Asiegbu, F. O., W. Choi, J. S. Jeong, and R. A. Dean. 2004. Cloning, sequencing and functional analysis of Magnaporthe grisea MVP1 gene, a hex-1 homolog encoding a putative "Woronin body" protein. FEMS Microbiol. Lett. 230:85-90.
2. Bhambra, G. K., Z. Y. Wang, D. M. Soanes, G. E. Wakley, and N. J. Talbot. 2006. Peroxisomal carnitine acetyl transferase is required for elaboration of penetration hyphae during plant infection by Magnaporthe grisea. Mol. Microbiol. 61:46-60.
3. Bonnet, C., E. Espagne, D. Zickler, S. Boisnard, A. Bourdais, and V. Berteaux-Lecellier. 2006. The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle. Mol. Microbiol. 62:157-169.
4. Chandrasekar, P. H., and J. D. Sobel. 2006. Micafungin: a new echinocandin. Clin. Infect. Dis. 42:1171-1178.
5. Charlton, W., and E. Lopez-Huertas. 2002. PEX genes in plants and other organisms, p. 385-426. In A. Baker and I. A. Graham (ed.), Plant peroxisomes. Kluwer Academic Publishers, Dordrecht, The Netherlands.
6. Curach, N. C., V. S. Te'o, M. D. Gibbs, P. L. Bergquist, and K. M. Nevalainen. 2004. Isolation, characterization and expression of the hex1 gene from Trichoderma reesei. Gene 331:133-140.
7. Distel, B., R. Erdmann, S. J. Gould, G. Blobel, D. I. Crane, J. M. Cregg, G. Dodt, Y. Fujiki, J. M. Goodman, W. W. Just, J. A. Kiel, W. H. Kunau, P. B. Lazarow, G. P. Mannaerts, H. W. Moser, T. Osumi, R. A. Rachubinski, A. Roscher, S. Subramani, H. F. Tabak, T. Tsukamoto, D. Valle, I. van der Klei, P. P. van Veldhoven, and M. Veenhuis. 1996. A unified nomenclature for peroxisome biogenesis factors. J. Cell Biol. 135:1-3.
8. Erdmann, R., and G. Blobel. 1995. Giant peroxisomes in oleic acid induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol. 128:509-523.
9. Gould, S. J., and D. Valle. 2000. Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet. 16:340-345.
10. Heiland, I., and R. Erdmann. 2005. Biogenesis of peroxisomes. Topogenesis of the peroxisomal membrane and matrix proteins. FEBS J. 272:2362-2372.
11. Hynes, M. J., S. L. Murray, G. S. Khew, and M. A. Davis. 2008. Genetic analysis of the role of peroxisomes in the utilisation of acetate and fatty acids in Aspergillus nidulans. Genetics 178:1355-1369.
12. Jedd, G., and N. H. Chua. 2000. A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat. Cell Biol. 2:226-231.
13. Jin, F. J., J. Maruyama, P. R. Juvvadi, M. Arioka, and K. Kitamoto. 2004. Development of a novel quadruple auxotrophic host transformation system by argB gene disruption using adeA gene and exploiting adenine auxotrophy in Aspergillus oryzae. FEMS Microbiol. Lett. 239:79-85.
14. Jin, F. J., T. Watanabe, P. R. Juvvadi, J. Maruyama, M. Arioka, and K. Kitamoto. 2007. Double disruption of the proteinase genes, tppA and pepE, increases the production level of human lysozyme by Aspergillus oryzae. Appl. Microbiol. Biotechnol. 76:1059-1068.
15. Juvvadi, P. R., J. Maruyama, and K. Kitamoto. 2007. Phosphorylation of the Aspergillus oryzae Woronin body protein, AoHex1, by protein kinase C: evidence for its role in the multimerization and proper localization of the Woronin body protein. Biochem. J. 405:533-540.
16. Kiel, J. A., I. J. van der Klei, M. A. van den Berg, R. A. Bovenberg, and M. Veenhuis. 2005. Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet. Biol. 42:154-164.
17. Kiel, J. A., M. Veenhuis, and I. J. van der Klei. 2006. PEX genes in fungal genomes: common, rare or redundant. Traffic 7:1291-1303.
18. Kimura, A., Y. Takano, I. Furusawa, and T. Okuno. 2001. Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell 13:1945-1958.
19. Kitamoto, K. 2002. Molecular biology of the Koji molds. Adv. Appl. Microbiol. 51:129-153.
20. Koch, A., G. Schneider, G. H. Luers, and M. Schrader. 2004. Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J. Cell Sci. 117:3995-4006.
21. Koch, A., M. Thiemann, M. Grabenbauer, Y. Yoon, M. A. McNiven, and M. Schrader. 2003. Dynamin-like protein 1 is involved in peroxisomal fission. J. Biol. Chem. 278:8597-8605.
22. Kubodera, T., N. Yamashita, and A. Nishimura. 2000. Pyrithiamine resistance gene (ptrA) of Aspergillus oryzae: cloning, characterization and application as a dominant selectable marker for transformation. Biosci. Biotechnol. Biochem. 64:1416-1421.
23. Kunze, M., I. Pracharoenwattana, S. M. Smith, and A. Hartig. 2006. A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim. Biophys. Acta 1763:1441-1452.
24. Liu, F., S. K. Ng, Y. Lu, W. Low, J. Lai, and G. Jedd. 2008. Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J. Cell Biol. 180:325-339.
25. Mabashi, Y., T. Kikuma, J. Maruyama, M. Arioka, and K. Kitamoto. 2006. Development of a versatile expression plasmid construction system for Aspergillus oryzae and its application to visualization of mitochondria. Biosci. Biotechnol. Biochem. 70:1882-1889.
26. Managadze, D., C. Würtz, M. Sichting, G. Niehaus, M. Veenhuis, and H. Rottensteiner. 2007. The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. Traffic 8:687-701.
27. Markham, P., and A. J. Collinge. 1987. Woronin bodies of filamentous fungi. FEMS Microbiol. Rev. 46:1-11.
28. Marshall, P. A., Y. I. Krimkevich, R. H. Lark, J. M. Dyer, M. Veenhuis, and J. M. Goodman. 1995. Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129:345-355.
29. Maruyama, J., P. R. Juvvadi, K. Ishi, and K. Kitamoto. 2005. Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem. Biophys. Res. Commun. 331:1081-1088.
30. Orth, T., S. Reumann, X. Zhang, J. Fan, D. Wenzel, S. Quan, and J. Hu. 2007. The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19:333-350.
31. Purdue, P. E., and P. B. Lazarow. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701-752.
32. Ramos-Pamplona, M., and N. I. Naqvi. 2006. Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA. Mol. Microbiol. 61:61-75.
33. Roncero, C., and A. Durán. 1985. Effect of calcofluor white and Congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J. Bacteriol. 163:1180-1185.
34. Rottensteiner, H., K. Stein, E. Sonnenhol, and R. Erdmann. 2003. Conserved function of pex11p and the novel pex25p and pex27p in peroxisome biogenesis. Mol. Biol. Cell 14:4316-4328.
35. Schrader, M. 2006. Shared components of mitochondrial and peroxisomal division. Biochim. Biophys. Acta 1763:531-541.
36. Schrader, M., B. E. Reuber, J. C. Morrell, G. Jimenez-Sanchez, C. Obie, T. A. Stroh, D. Valle, T. A. Schroer, and S. J. Gould. 1998. Expression of PEX11beta mediates peroxisome proliferation in the absence of extracellular stimuli. J. Biol. Chem. 273:29607-29614.
37. Smith, J. J., M. Marelli, R. H. Christmas, F. J. Vizeacoumar, D. J. Dilworth, T. Ideker, T. Galitski, K. Dimitrov, R. A. Rachubinski, and J. D. Aitchison. 2002. Transcriptome profiling to identify genes involved in peroxisome assembly and function. J. Cell Biol. 158:259-271.
38. Soundararajan, S., G. Jedd, X. Li, M. Ramos-Pamploña, N. H. Chua, and N. I. Naqvi. 2004. Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 6:1564-1574.
39. Takahashi, T., T. Masuda, and Y. Koyama. 2006. Enhanced gene targeting frequency in ku70 and ku80 disruption mutants of Aspergillus sojae and Aspergillus oryzae. Mol. Genet. Genomics 275:460-470.
40. Tam, Y. Y., J. C. Torres-Guzman, F. J. Vizeacoumar, J. J. Smith, M. Marelli, J. D. Aitchison, and R. A. Rachubinski. 2003. Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae. Mol. Biol. Cell 14:4089-4102.
41. Tenney, K., I. Hunt, J. Sweigard, J. I. Pounder, C. McClain, E. J. Bowman, and B. J. Bowman. 2000. Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores. Fungal Genet. Biol. 31:205-217.
42. Tey, W. K., A. J. North, J. L. Reyes, Y. F. Lu, and G. Jedd. 2005. Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol. Biol. Cell 16:2651-2659.
43. Thoms, S., and R. Erdmann. 2005. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation. FEBS J. 272:5169-5181.
44. Thoms, S., and R. Erdmann. 2005. Import of proteins into peroxisomes, p. 125-134. In J. Eichler (ed.), Protein movement across membranes Landes Bioscience, Georgetown, TX.
45. van den Bosch, H., R. B. Schutgens, R. J. Wanders, and J. M. Tager. 1992. Biochemistry of peroxisomes. Annu. Rev. Biochem. 61:157-197.
46. Veenhuis, M. 1992. Peroxisome biogenesis and function in Hansenula polymorpha. Cell Biochem. Funct. 10:175-184.
47. Würtz, C., W. Schliebs, R. Erdmann, and H. Rottensteiner. 2008. Dynamin-like protein-dependent formation of Woronin bodies in Saccharomyces cerevisiae upon heterologous expression of a single protein. FEBS J. 275:2932-2941.
48. Yan, M., N. Rayapuram, and S. Subramani. 2005. The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17:376-383.
49. Yuan, P., G. Jedd, D. Kumaran, S. Swaminathan, H. Shio, D. Hewitt, N. H. Chua, and K. Swaminathan. 2003. A HEX-1 crystal lattice required for Woronin body function in Neurospora crassa. Nat. Struct. Biol. 4:264-270.