Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016, Article ID 9343417, 10 pages
http://dx.doi.org/10.1155/2016/9343417
Review Article

Roles of Peroxisomes in the Rice Blast Fungus

State Key Laboratory of Agricultural Microbiology, The Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China

Received 3 June 2016; Accepted 25 July 2016

Academic Editor: Frederick D. Quinn

Copyright © 2016 Xiao-Lin Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. J. Smith and J. D. Aitchison, “Peroxisomes take shape,” Nature Reviews Molecular Cell Biology, vol. 14, no. 12, pp. 803–817, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. I. J. van der Klei and M. Veenhuis, “Yeast and filamentous fungi as model organisms in microbody research,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 1763, no. 12, pp. 1364–1373, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. H. W. Platta and R. Erdmann, “Peroxisomal dynamics,” Trends in Cell Biology, vol. 17, no. 10, pp. 474–484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. I. J. van der Klei and M. Veenhuis, “Yeast peroxisomes: function and biogenesis of a versatile cell organelle,” Trends in Microbiology, vol. 5, no. 12, pp. 502–509, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Hu, A. Baker, B. Bartel et al., “Plant peroxisomes: biogenesis and function,” Plant Cell, vol. 24, no. 6, pp. 2279–2303, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. J. A. Wanders and H. R. Waterham, “Biochemistry of mammalian peroxisomes revisited,” Annual Review of Biochemistry, vol. 75, pp. 295–332, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Pieuchot and G. Jedd, “Peroxisome assembly and functional diversity in eukaryotic microorganisms,” Annual Review of Microbiology, vol. 66, pp. 237–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. M. J. Hynes, S. L. Murray, G. S. Khew, and M. A. Davis, “Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans,” Genetics, vol. 178, no. 3, pp. 1355–1369, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. M. J. Hynes, S. L. Murray, A. Duncan, G. S. Khew, and M. A. Davis, “Regulatory genes controlling fatty acid catabolism and peroxisomal functions in the filamentous fungus Aspergillus nidulans,” Eukaryotic Cell, vol. 5, no. 5, pp. 794–805, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Managadze, C. Würtz, S. Wiese et al., “Identification of PEX33, a novel component of the peroxisomal docking complex in the filamentous fungus Neurospora crassa,” European Journal of Cell Biology, vol. 89, no. 12, pp. 955–964, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Sichting, A. Schell-Steven, H. Prokisch, R. Erdmann, and H. Rottensteiner, “Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes,” Molecular Biology of the Cell, vol. 14, no. 2, pp. 810–821, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Managadze, C. Würtz, M. Sichting, G. Niehaus, M. Veenhuis, and H. Rottensteiner, “The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and woronin bodies,” Traffic, vol. 8, no. 6, pp. 687–701, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Asakura, S. Ninomiya, M. Sugimoto et al., “Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare,” The Plant Cell, vol. 21, no. 4, pp. 1291–1304, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. N. Fujihara, A. Sakaguchi, S. Tanaka et al., “Peroxisome biogenesis factor PEX13 is required for appressorium-mediated plant infection by the anthracnose fungus Colletotrichum orbiculare,” Molecular Plant-Microbe Interactions, vol. 23, no. 4, pp. 436–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Kubo, N. Fujihara, K. Harata, U. Neumann, G. P. Robin, and R. O'Connell, “Colletotrichum orbiculare FAM1 encodes a novel Woronin body-associated Pex22 peroxin required for appressorium-mediated plant infection,” Mbio, vol. 6, no. 5, pp. e01305–e01315, 2015. View at Publisher · View at Google Scholar
  16. L. Li, J. Y. Wang, Z. Zhang 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, vol. 9, no. 1, Article ID e85252, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Goh, J. Jeon, K. S. Kim, J. Park, S.-Y. Park, and Y.-H. Lee, “The PEX7-mediated peroxisomal import system is required for fungal development and pathogenicity in Magnaporthe oryzae,” PLoS ONE, vol. 6, no. 12, Article ID e28220, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Y. Wang, Z. Zhang, Y. L. Wang et al., “PTS1 peroxisomal import pathway plays shared and distinct roles to PTS2 pathway in development and pathogenicity of Magnaporthe oryzae,” PLoS ONE, vol. 8, no. 2, Article ID e55554, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Deng, Z. Qu, and N. I. Naqvi, “The role of Snx41-based pexophagy in Magnaporthe development,” PLoS ONE, vol. 8, no. 11, article e79128, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Y. Wang, L. Li, Z. Zhang 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, vol. 10, no. 7, Article ID 0134249, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Piekarska, G. Hardy, E. Mol et al., “The activity of the glyoxylate cycle in peroxisomes of Candida albicans depends on a functional β-oxidation pathway: evidence for reduced metabolite transport across the peroxisomal membrane,” Microbiology, vol. 154, no. 10, pp. 3061–3072, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Gabriel, I. Accoceberry, J. J. Bessoule et al., “A Fox2-dependent fatty acid beta-oxidation pathway coexists both in peroxisomes and mitochondria of the ascomycete Yeast Candida lusitaniae,” PLoS ONE, vol. 9, no. 12, 27 pages, 2014. View at Google Scholar
  23. M. Gründlinger, S. Yasmin, B. E. Lechner et al., “Fungal siderophore biosynthesis is partially localized in peroxisomes,” Molecular Microbiology, vol. 88, no. 5, pp. 862–875, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Beck and F. Ebel, “Characterization of the major Woronin body protein HexA of the human pathogenic mold Aspergillus fumigatus,” International Journal of Medical Microbiology, vol. 303, no. 2, pp. 90–97, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Kretschmer, J. Wang, and J. W. Kronstad, “Peroxisomal and mitochondrial β-oxidation pathways influence the virulence of the pathogenic fungus Cryptococcus neoformans,” Eukaryotic Cell, vol. 11, no. 8, pp. 1042–1054, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Idnurm, S. S. Giles, J. R. Perfect, and J. Heitman, “Peroxisome function regulates growth on glucose in the basidiomycete fungus Cryptococcus neoformans,” Eukaryotic Cell, vol. 6, no. 1, pp. 60–72, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. V. I. Titorenko and R. A. Rachubinski, “The life cycle of the peroxisome,” Nature Reviews Molecular Cell Biology, vol. 2, no. 5, pp. 357–368, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Ramos-Pamplona and N. I. Naqvi, “Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA,” Molecular Microbiology, vol. 61, no. 1, pp. 61–75, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. E. H. Hettema, W. Girzalsky, M. Van Den Berg, R. Erdmann, and B. Distel, “Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins,” The EMBO Journal, vol. 19, no. 2, pp. 223–233, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. K. A. Sacksteder, J. M. Jones, S. T. South, X. Li, Y. Liu, and S. J. Gould, “PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis,” The Journal of Cell Biology, vol. 148, no. 5, pp. 931–944, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Ghaedi, S. Tamura, K. Okumoto, Y. Matsuzono, and Y. Fujiki, “The peroxin Pex3p initiates membrane assembly in peroxisome biogenesis,” Molecular Biology of the Cell, vol. 11, no. 6, pp. 2085–2102, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Fang, J. C. Morrell, J. M. Jones, and S. J. Gould, “PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins,” Journal of Cell Biology, vol. 164, no. 6, pp. 863–875, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. X.-L. Chen, M. Shen, J. Yang et al., “Peroxisomal fission is induced during appressorium formation and is required for full virulence of the rice blast fungus,” Molecular Plant Pathology, 2016. View at Publisher · View at Google Scholar
  34. A. M. Motley, G. P. Ward, and E. H. Hettema, “Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p,” Journal of Cell Science, vol. 121, no. 10, pp. 1633–1640, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Schrader, N. A. Bonekamp, and M. Islinger, “Fission and proliferation of peroxisomes,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1822, no. 9, pp. 1343–1357, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. I. A. Khan, G. Ning, X. Liu, X. Feng, F. Lin, and J. Lu, “Mitochondrial fission protein MoFis1 mediates conidiation and is required for full virulence of the rice blast fungus Magnaporthe oryzae,” Microbiological Research, vol. 178, pp. 51–58, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Reidick and H. Platta, “Regulation of the selective autophagic degradation of peroxisomes by PtdIns3P and Rab-GTPases,” Yeast, vol. 30, p. 125, 2013. View at Google Scholar
  38. J.-C. Farré, R. Manjithaya, R. D. Mathewson, and S. Subramani, “PpAtg30 tags peroxisomes for turnover by selective autophagy,” Developmental cell, vol. 14, no. 3, pp. 365–376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Y. Nazarko, A. S. Polupanov, R. R. Manjithaya, S. Subramani, and A. A. Sibirny, “The requirement of sterol glucoside for pexophagy in yeast is dependent on the species and nature of peroxisome inducers,” Molecular Biology of the Cell, vol. 18, no. 1, pp. 106–118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. W. H. Meijer, I. J. van der Klei, M. Veenhuis, and J. A. K. W. Kiel, “ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes,” Autophagy, vol. 3, no. 2, pp. 106–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Komori, S. W. Rasmussen, J. A. K. W. Kiel et al., “The Hansenula polymorpha PEX14 gene encodes a novel peroxisomal membrane protein essential for peroxisome biogenesis,” The EMBO Journal, vol. 16, no. 1, pp. 44–53, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. F. F. Liu, S. K. Ng, Y. F. Lu, W. Low, J. Lai, and G. Jedd, “Making two organelles from one: woronin body biogenesis by peroxisomal protein sorting,” The Journal of Cell Biology, vol. 180, no. 2, pp. 325–339, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. A. P. J. Trinci and A. J. Collinge, “Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals,” Protoplasma, vol. 80, no. 1–3, pp. 57–67, 1974. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Markham and A. J. Collinge, “Woronin bodies of filamentous fungi,” FEMS Microbiology Letters, vol. 46, no. 1, pp. 1–11, 1987. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Soundararajan, G. Jedd, X. Li, M. Ramos-Pamploña, N. H. Chua, and N. I. Naqvi, “Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress,” Plant Cell, vol. 16, no. 6, pp. 1564–1574, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. X.-Q. Zeng, G.-Q. Chen, X.-H. Liu et al., “Crosstalk between SNF1 pathway and the peroxisome-mediated lipid metabolism in Magnaporthe oryzae,” PLoS ONE, vol. 9, no. 8, Article ID e103124, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. Z.-Y. Wang, D. M. Soanes, M. J. Kershaw, and N. J. Talbot, “Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid β-oxidation during appressorium-mediated plant infection,” Molecular Plant-Microbe Interactions, vol. 20, no. 5, pp. 475–491, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. G. K. Bhambra, Z.-Y. Wang, D. M. Soanes, G. E. Wakley, and N. J. Talbot, “Peroxisomal carnitine acetyl transferase is required for elaboration of penetration hyphae during plant infection by Magnaporthe grisea,” Molecular Microbiology, vol. 61, no. 1, pp. 46–60, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Yang, L. Kong, X. Chen et al., “A carnitine-acylcarnitine carrier protein, MoCrc1, is essential for pathogenicity in Magnaporthe oryzae,” Current Genetics, vol. 58, no. 3, pp. 139–148, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. Z.-Y. Wang, C. R. Thornton, M. J. Kershaw, L. Debao, and N. J. Talbot, “The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea,” Molecular Microbiology, vol. 47, no. 6, pp. 1601–1612, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. V. Bhadauria, S. Banniza, A. Vandenberg, G. Selvaraj, and Y. Wei, “Peroxisomal alanine: glyoxylate aminotransferase AGT1 is indispensable for appressorium function of the rice blast pathogen, magnaporthe oryzae,” PLoS ONE, vol. 7, no. 4, Article ID e36266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Kunze, I. Pracharoenwattana, S. M. Smith, and A. Hartig, “A central role for the peroxisomal membrane in glyoxylate cycle function,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1763, no. 12, pp. 1441–1452, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Opaliński, M. Bartoszewska, S. Fekken et al., “De novo peroxisome biogenesis in Penicillium chrysogenum is not dependent on the Pex11 family members or Pex16,” PLoS ONE, vol. 7, no. 4, Article ID e35490, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Langfelder, M. Streibel, B. Jahn, G. Haase, and A. A. Brakhage, “Biosynthesis of fungal melanins and their importance for human pathogenic fungi,” Fungal Genetics and Biology, vol. 38, no. 2, pp. 143–158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Poirier, V. D. Antonenkov, T. Glumoff, and J. K. Hiltunen, “Peroxisomal β-oxidation—a metabolic pathway with multiple functions,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1763, no. 12, pp. 1413–1426, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. R. N. Patkar, M. Ramos-Pamplona, A. P. Gupta, Y. Fan, and N. I. Naqvi, “Mitochondrial β-oxidation regulates organellar integrity and is necessary for conidial germination and invasive growth in Magnaporthe oryzae,” Molecular Microbiology, vol. 86, no. 6, pp. 1345–1363, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. J. H. Swiegers, N. Dippenaar, I. S. Pretorius, and F. F. Bauer, “Carnitine-dependent metabolic activities in Saccharomyces cerevisiae: three carnitine acetyltransferases are essential in a carnitine-dependent strain,” Yeast, vol. 18, no. 7, pp. 585–595, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. V. I. Titorenko and S. R. Terlecky, “Peroxisome metabolism and cellular aging,” Traffic, vol. 12, no. 3, pp. 252–259, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. P. Skamnioti, C. Henderson, Z. Zhang, Z. Robinson, and S. J. Gurr, “A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea,” Molecular Plant-Microbe Interactions, vol. 20, no. 5, pp. 568–580, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Tanabe, N. Ishii-Minami, K.-I. Saitoh et al., “The role of catalase-peroxidase secreted by Magnaporthe oryzae during early infection of rice cells,” Molecular Plant-Microbe Interactions, vol. 24, no. 2, pp. 163–171, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Schrader and H. D. Fahimi, “Peroxisomes and oxidative stress,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1763, no. 12, pp. 1755–1766, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. K.-H. Kim, S. D. Willger, S.-W. Park et al., “TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen,” PLoS Pathogens, vol. 5, no. 11, article e1000653, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. A. J. Hamilton and B. L. Gomez, “Melanins in fungal pathogens,” Journal of Medical Microbiology, vol. 51, no. 3, pp. 189–191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. S. M. Bowman and S. J. Free, “The structure and synthesis of the fungal cell wall,” BioEssays, vol. 28, no. 8, pp. 799–808, 2006. View at Publisher · View at Google Scholar · View at Scopus