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Research Paper

Pex13 and Pex14, the key components of the peroxisomal docking complex, are required for peroxisome formation, host infection and pathogenicity-related morphogenesis in Magnaporthe oryzae

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Pages 292-314 | Received 18 Dec 2018, Accepted 14 Mar 2019, Published online: 16 Apr 2019

References

  • Talbot NJ. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol. 2003;57:177–202.
  • Wilson RA, Talbot NJ. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol. 2009;7(3):185–195.
  • Hamer JE, Howard RJ, Chumley FG, et al. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science. 1988;239(4837):288–290.
  • De Jong JC, Mccormack BJ, Smirnoff N, et al. Glycerol generates turgor in rice blast. Nature. 1997;389(6648):244–245.
  • Chumley FG, Valent B. Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol Plant Microbe Interact. 1990;3(3):135–143.
  • Maciel JL, Ceresini PC, Castroagudin VL, et al. Population structure and pathotype diversity of the wheat blast pathogen Magnaporthe oryzae 25 years after its emergence in Brazil. Phytopathology. 2014;104(1):95–107.
  • Islam MT, Croll D, Gladieux P, et al. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 2016;14(1):84.
  • Kimura A, Takano Y, Furusawa I, et al. Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell. 2001;13(8):1945–1957.
  • Ramos-Pamplona M, Naqvi NI. Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA. Mol Microbiol. 2006;61(1):61–75.
  • Min K, Son H, Lee J, et al. Peroxisome function is required for virulence and survival of Fusarium graminearum. Mol Plant Microbe Interact. 2012;25(12):1617–1627.
  • Wang J, Zhang Z, Wang Y, et al. PTS1 peroxisomal import pathway plays shared and distinct roles to PTS2 pathway in development and pathogenicity of Magnaporthe oryzae. PLoS One. 2013;8(2):e55554.
  • Wang ZY, Soanes DM, Kershaw MJ, et al. Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid beta-oxidation during appressorium-mediated plant infection. Mol Plant Microbe Interact. 2007;20(5):475–491.
  • Li L, Wang JY, Zhang Z, et al. MoPex19, which is essential for maintenance of peroxisomal structure and woronin bodies, is required for metabolism and development in the rice blast fungus. PLoS One. 2014;9(1):e85252.
  • Li L, Wang JY, Chen HL, et al. Pex14/17, a filamentous fungus-specific peroxin, is required for the import of peroxisomal matrix proteins and full virulence of Magnaporthe oryzae. Mol Plant Pathol. 2016;18(9):1238.
  • Wang JY, Li L, Zhang Z, et al. One of three Pex11 family members is required for peroxisomal proliferation and full virulence of the rice blast fungus Magnaporthe oryzae. PLoS One. 2015;10(7):e0134249.
  • Fujihara N, Sakaguchi A, Tanaka S, et al. Peroxisome biogenesis factor PEX13 is required for appressorium-mediated plant infection by the anthracnose fungus Colletotrichum orbiculare. Mol Plant Microbe Interact. 2010;23(4):436–445.
  • Lazarow P, Fujiki Y. Biogenesis of peroxisomes. Ann Rev Cell Biol. 1985;1(1):489–530.
  • Faust PL, Banka D, Siriratsivawong R, et al. Peroxisome biogenesis disorders: the role of peroxisomes and metabolic dysfunction in developing brain. J Inherit Metab Dis. 2005;28(3):369–383.
  • Wanders RJA, Waterham HR. Peroxisomal disorders: the single peroxisomal enzyme deficiencies. BBA-Mol Cell Res. 2006;1763(12):1707–1720.
  • Meijer WH, Gidijala L, Fekken S, et al. Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum. Appl Environ Microbiol. 2010;76(17):5702–5709.
  • Markham P, Collinge AJ. Woronin bodies of filamentous fungi. FEMS Microbiol Rev. 1987;46:1–11.
  • Baker A, Sparkes IA. Peroxisome protein import: some answers, more questions. Curr Opin Plant Biol. 2005;8(6):640–647.
  • Kiel J, Van Den Berg M, Bovenberg RAL, et al. Penicillium chrysogenum Pex5p mediates differential sorting of PTS1 proteins to microbodies of the methylotrophic yeast Hansenula polymorpha. Fungal Genet Biol. 2004;41(7):708–720.
  • Bonnet C, Espagne E, Zickler D, et al. The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle. Mol Microbiol. 2006;62(1):157–169.
  • Deng SZ, Gu ZK, Yang N, et al. Identification and characterization of the peroxin 1 gene MoPEX1 required for infection-related morphogenesis and pathogenicity in Magnaporthe oryzae. Sci Rep-UK. 2016;6:36292.
  • Subramani S. Protein translocation into peroxisomes. J Biol Chem. 1996;271(51):32483–32486.
  • Kiel J, Veenhuis M, Van Der Klei IJ. PEX genes in fungal genomes: common, rare or redundant. Traffic. 2006;7(10):1291–1303.
  • Rayapuram N, Subramani S. The importomer - A peroxisomal membrane complex involved in protein translocation into the peroxisome matrix. BBA-Mol Cell Res. 2006;1763(12):1613–1619.
  • Urquhart AJ, Kennedy D, Gould SJ, et al. Interaction of Pex5p, the type 1 peroxisome targeting signal receptor, with the peroxisomal membrane proteins Pex14p and Pex13p. J Biol Chem. 2000;275(6):4127–4136.
  • Huhse B, Rehling P, Albertini M, et al. Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal protein translocation machinery. J Cell Biol. 1998;140(1):49–60.
  • Managadze D, Wurtz C, Wiese S, et al. Identification of PEX33, a novel component of the peroxisomal docking complex in the filamentous fungus Neurospora crassa. Eur J Cell Biol. 2010;89(12):955–964.
  • Opalinski L, Kiel J, Homan TG, et al. Penicillium chrysogenum Pex14/17p-a novel component of the peroxisomal membrane that is important for penicillin production. FEBS J. 2010;277(15):3203–3218.
  • Notteghem JL, Silue D. Distribution of the mating type alleles in Magnaporthe grisea populations pathogenic on rice. Phytopathology. 1992;82(4):421–424.
  • Crawford MS, Chumley FG, Weaver CG, et al. Characterization of the heterokaryotic and vegetative diploid phases of Magnaporthe grisae. Genetics. 1986;114(4):1111–1129.
  • Talbot NJ, Ebbole DJ, Hamer JE. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell. 1993;5(11):1575–1590.
  • Rho HS, Kang S, Lee YH. Agrobacterium tumefaciens-mediated transformation of the plant pathogenic fungus, Magnaporthe grisea. Mol Cells. 2001;12(3):407–411.
  • Wang JY, Wu XY, Zhang Z, et al. Fluorescent co-localization of PTS1 and PTS2 and its application in analysis of the gene function and the peroxisomal dynamic in Magnaporthe oryzae. J Zhejiang Univ-Sc B. 2008;9(10):802–810.
  • Liu XH, Lu JP, Zhang L, et al. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell. 2007;6(6):997–1005.
  • Gould SJ, Kalish JE, Morrell JC, et al. Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J Cell Biol. 1996;135(1):85–95.
  • Itoh R, Fujiki Y. Functional domains and dynamic assembly of the peroxin Pex14p, the entry site of matrix proteins. J Biol Chem. 2006;281(15):10196–10205.
  • Soundararajan S, Jedd G, Li XL, et al. Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell. 2004;16(6):1564–1574.
  • Liu F, Ng SK, Lu Y, et al. Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol. 2008;180(2):325–339.
  • Albertini M, Rehling P, Erdmann R, et al. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell. 1997;89(1):83–92.
  • Erdmann R, Blobel G. Identification of Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J Cell Biol. 1996;135(1):111–121.
  • Managadze D, Wurtz C, Sichting M, et al. The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. Traffic. 2007;8(6):687–701.
  • Barnett P, Bottger G, Klein ATJ, et al. The peroxisomal membrane protein Pex13p shows a novel mode of SH3 interaction. Embo J. 2000;19(23):6382–6391.
  • Peraza-Reyes L, Arnaise S, Zickler D, et al. The importomer peroxins are differentially required for peroxisome assembly and meiotic development in Podospora anserina: insights into a new peroxisome import pathway. Mol Microbiol. 2011;82(2):365–377.
  • Hynes MJ, Murray SL, Khew GS, et al. Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics. 2008;178(3):1355–1369.
  • Mano S, Nakamori C, Nito K, et al. The Arabidopsis pex12 and pex13 mutants are defective in both PTS1- and PTS2-dependent protein transport to peroxisomes. Plant J. 2006;47(4):604–618.
  • Williams C, Van Den Berg M, Distel B. Saccharomyces cerevisiae Pex14p contains two independent Pex5p binding sites, which are both essential for PTS1 protein import. FEBS Lett. 2005;579(16):3416–3420.
  • Will GK, Soukupova M, Hong X, et al. Identification and characterization of the human orthologue of yeast pex14p. Mol Cell Biol. 1999;19(3):2265–2277.
  • Monroe-Augustus M, Ramon NM, Ratzel SE, et al. Matrix proteins are inefficiently imported into Arabidopsis peroxisomes lacking the receptor-docking peroxin PEX14. Plant Mol Biol. 2011;77(1–2):1–15.
  • Johnson MA, Snyder WB, Cereghino JL, et al. Pichia pastoris Pex14p, a phosphorylated peroxisomal membrane protein, is part of a PTS-receptor docking complex and interacts with many peroxins. Yeast. 2001;18(7):621–641.
  • Girzalsky W, Rehling P, Stein K, et al. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J Cell Biol. 1999;144(6):1151–1162.
  • Beck J, Ebel F. Characterization of the major Woronin body protein HexA of the human pathogenic mold Aspergillus fumigatus. Int J Med Microbiol. 2013;303(2):90–97.
  • Escano CS, Juvvadi PR, Jin FJ, et al. Disruption of the Aopex11-1 gene involved in peroxisome proliferation leads to impaired Woronin body formation in Aspergillus oryzae. Eukaryot Cell. 2009;8(3):296–305.
  • Kubo Y, Fujihara N, Harata K, et al. Colletotrichum orbiculare FAM1 encodes a novel woronin body-associated Pex22 peroxin required for appressorium-mediated plant infection. MBio. 2015;6(5):e01305–e01315.
  • Peraza-Reyes L, Zickler D, Berteaux-Lecellier V. The peroxisome RING-finger complex is required for meiocyte formation in the fungus Podospora anserina. Traffic. 2008;9(11):1998–2009.