Function of peroxisomes in plant-pathogen interactions

Subcellular Biochemistry

Volumn 69, Issue , 2014, Pages 329-345

  Kubo, Yasuyuki ^a  

^a Graduate School of Life and Environmental Sciences   (Japan)

Author keywords

Appressoria; Fungal pathogenesis; Glyoxylate cycle; Lipolysis; Melanin biosynthesis; Pexophagy; Woronin body; oxidation

Indexed keywords

ALTERNARIA ALTERNATA; COLLETOTRICHUM ORBICULARE; EUKARYOTA; FUNGI; MAGNAPORTHE ORYZAE;

EID: 84930211216     PISSN: 03060225     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-6889-5_18     Document Type: Article

References (77)

1. Asakura M, Ninomiya S, Sugimoto M, Oku M, Yamashita S, Okuno T, Sakai Y, Takano Y (2009) Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell 21:1291-1304
2. Asakura M, Okuno T, Takano Y (2006) Multiple contributions of peroxisomal metabolic function to fungal pathogenicity in Colletotrichum lagenarium. Appl Environ Microbiol 72:6345-6354
3. Asakura M, Yoshino K, Hill AM, Kubo Y, Sakai Y, Takano Y (2012) Primary and secondary metabolism regulates lipolysis in appressoria of Colletotrichum orbiculare. Fungal Genet Biol 49:967-975
4. Bertoni G (2009) Pexophagy in fungal pathogenesis. Plant Cell 21:1030
5. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G,Wei Y (2012) Peroxisomal alanine: glyoxylate aminotransferase AGT1 is indispensable for appressorium function of the rice blast pathogen, Magnaporthe oryzae. PLoS One 7:e36266
6. Bhambra GK, Wang ZY, Soanes DM, Wakley GE, Talbot NJ (2006) Peroxisomal carnitine acetyl transferase is required for elaboration of penetration hyphae during plant infection by Magnaporthe grisea. Mol Microbiol 61:46-60
7. Bonnet C, Espagne E, Zickler D, Boisnard S, Bourdais A, Berteaux-Lecellier V (2006) The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle. Mol Microbiol 62:157-169
8. Brown LA, Baker A (2008) Shuttles and cycles: transport of proteins into the peroxisome matrix. Mol Membr Biol 25:363-375
9. Chumley FG, Valent B (1990) Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Mol Plant Microbe Interact 3:135-143
10. Choi J, Kim Y, Kim S, Park J, Lee YH (2009) MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet Biol 46:243-254
11. de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ (1997) Glycerol generates turgor in rice blast. Nature 389:244-245
12. Eastmond PJ, Germain V, Lange PR, Bryce JH, Smith SM, Graham IA (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc Natl Acad Sci USA 97:5669-5674
13. Erdmann R, Blobel G (1996) Identification of Pex13p a peroxisomal membrane receptor for the PTS1 recognition factor. J Cell Biol 135:111-121
14. Farré JC, Subramani S (2004) Peroxisome turnover by micropexography: an autophagy-related process. Trends Cell Biol 14:515-523
15. Fujihara N, Sakaguchi A, Tanaka S, Fujii S, Tsuji G, Shiraishi T, O'Connell R, Kubo Y (2010) Peroxisome biogenesis factor PEX13 is required for appressorium-mediated plant infection by the anthracnose fungus Colletotrichum orbiculare. Mol Plant Microbe Interact 23:436-445
16. Fujii I, Mori Y, Watanabe A, Kubo Y, Tsuji G, Ebizuka Y (2000) Enzymatic synthesis of 1,3,6,8-tetrahydoxynaphthalene solely from malonyl coenzyme A by a fungal iterative type I polyketide synthase PKS1. Biochemistry 39:8853-8858
17. Goh J, Jeon J, Kim KS, Park J, Park SY, Lee YH (2011) The PEX7-mediated peroxisomal import system is required for fungal development and pathogenicity in Magnaporthe oryzae. PLoS One 6:e28220
18. Gould SJ, Kalish JE, Morrell JC, Bjorkman J, Urquhart AJ, Crane DI (1996) Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J Cell Biol 135:85-95
19. Heiland I, Erdmann R (2005) Biogenesis of peroxisomes: topogenesis of the peroxisomeal membrane and matrix proteins. FEBS J 272:2362-2372
20. Howard RJ, Ferrari MA, Roach DH, Money NP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci USA 88:11281-11284
21. Idnurm A, Howlett BJ (2002) Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryot Cell 1:719-724
22. Idnurm A, Giles SS, Perfect JR, Heitman J (2007) Peroxisome function regulates growth on glucose in the Basidiomycete fungus Cryptococcus neoformans. Eukaryot Cell 6:60-72
23. Imazaki A, Tanaka A, Harimoto Y, YamamotoM, Akimitsu K, Park P, Tsuge T (2010) Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen Alternaria alternata. Eukaryot Cell 9:682-694
24. Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226-231
25. Jeon J, Goh J, Yoo S, Chi MH, Choi J, Rho HS, Park J, Han SS, Kim BR, Park SY, Kim S, Lee YH (2008) A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol Plant Microbe Interact 21:525-534
26. Kershaw MJ, Talbot NJ (2009) Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci USA 106:15967-15972
27. Kiel JA, van den Berg M, Bovenberg RA, van der Klei IJ, Veenhuis M (2004) Penicillium chrysogenum Pex5p mediates differential sorting of PTS1 proteins to microbodies of the methylotrophic yeast Hansenula polymorpha. Fungal Genet Biol 41:708-720
28. Kiel JA, van der Klei IJ, van den Berg MA, Bovenberg RA, Veenhuis M (2005) Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol 42:154-164
29. Kiel JA, Veenhuis M, van der Klei IJ (2006) PEX genes in fungal genomes: common, rare or redundant. Traffic 7:1291-1303
30. Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl N, Cho Y, Mukhopadhyay B, Cramer RA Jr, Lawrence CB (2009) TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen. PLoS Pathog 5:e1000653
31. Kimura A, Takano Y, Furusawa I, Okuno T (2001) Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell 13: 1945-1957
32. Kionka C, Kunau WH (1985) Inducible ß-oxidation pathway in Neurospora crassa. J Bacteriol 161:153-157
33. Klose J, Kronstad JW (2006) The multifunctional beta-oxidation enzyme is required for full symptom development by the biotrophic maize pathogen Ustilago maydis. Eukaryot Cell 5:2047-2061
34. Kondrashov FA, Koonin EV, Morgunov IG, Finogenova TV, Kondrashova MN (2006) Evolution of glyoxylate cycle enzymes in Metazoa: evidence of multiple horizontal transfer events and pseudogene formation. Biol Direct 1:31
35. Kretschmer M, Klose J, Kronstad JW (2012) Defects in mitochondrial and peroxisomal ß- oxidation influence virulence in the maize pathogen Ustilago maydis. Eukaryot Cell 11: 1055-1066
36. Kubo Y (2012) Appressorium function in Colletotrichum orbiculare and prospect for genome based analysis. In: Pérez-Martín J, Di Pietro A (eds) Morphogenesis and pathogenicity in fungi, vol 22, Topics in Current Genetics, pp 115-131
37. Kubo Y, Furusawa I (1991) Melanin biosynthesis: prerequisite for successful invasion of the plant host by appressoria of Colletotrichum and Pyricularia. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Publishing, New York
38. Kubo Y, Nakamura H, Kobayashi K, Okuno T, Furusawa I (1991) Cloning of a melanin biosynthetic gene essential for appressorial penetration of Colletotrichum lagenarium. Mol Plant Microbe Interact 4:440-445
39. Kubo Y, Suzuki K, Furusawa I, Ishida N, Yamamoto M (1982) Relation of appressorium pigmentation and penetration of nitrocellulose membranes by Colletotrichum lagenarium. Phytopathology 72:498-501
40. Kubo Y, Takano Y, Endo N, Yasuda N, Tajima S, Furusawa I (1996) Cloning and structural analysis of the melanin biosynthesis gene SCD1 encoding scytalone dehydratase in Colletotrichum lagenarium. Appl Environ Microbiol 62:4340-4344
41. Kubo Y, Tanaka S (2010) Pathogenesis and plant basal resistance in Colletotrichum orbiculare and Magnaporthe oryzae infection. In: Wolpert T, Shiraishi T, Allen C, Glazebrook J, Akimitsu K (eds) Genome-enabled integration of research in plant pathogen systems. APS Press, St. Paul Minnesota
42. Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G (2008) Making two organelles from one: woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180:325-339
43. Lorenz MC, Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86
44. Maggio-Hall LA, Keller NP (2004) Mitochondrial beta-oxidation in Aspergillus nidulans. Mol Microbiol 54:1173-1185
45. Markham P, Collinge AJ (1987) Woronin bodies in filamentous fungi. FEMS Microbiol Rev 46:1-11
46. Mizushima N, Klionsky DJ (2007) Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr 27:19-40
47. Momany M, Richardson E, Van Sickle C, Jedd G (2002) Mapping Woronin body function in Aspergillus nidulans. Mycologia 94:260-266
48. Nakashima T, Ueno T, Fukami H, Taga T, Masuda H, Osaki K, Otani H, Kohmoto K, Nishimura S (1985) Isolation and structures of AK-toxin I and II, host-specific phytotoxic metabolites produced by Alternaria alternata Japanese pear pathotype. Agric Biol Chem 49:807-815
49. Perpetua NS, Kubo Y, Yasuda N, Takano Y, Furusawa I (1996) Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium. Mol Plant Microbe Interact 9:323-329
50. Pollack JK, Harris SD, Marten MR (2009) Autophagy in filamentous fungi. Fungal Genet Biol 46:1-8
51. Ramsay RR, Naismith JH (2003) A snapshot of carnitine acetyltransferase. Trends Biochem Sci 28:343-346
52. Ramos-Pamplona M, Naqvi NI (2006) Host invasion during rice-blast disease requires carnitinedependent transport of peroxisomal acetyl-CoA. Mol Microbiol 61:61-75
53. Rauyaree P, Choi W, Fang E, Blackmon B, Dean RA (2001) Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Mol Plant Pathol 2:347-354
54. Schadeck RJ, Leite B, de Freitas BD (1998) Lipid mobilization and acid phosphatase activity in lytic compartments during conidium dormancy and appressorium formation of Colletotrichum lagenarium. Cell Struct Func 23:333-340
55. Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol 41:641-667
56. Solomon PS, Lee RC, Wilson TJ, Oliver RP (2004) Pathogenicity of Stagonospora nodorum requires malate synthase. Mol Microbiol 53:1065-1073
57. Soundararajan S, Jedd G, Li X, Ramos-Pamploña M, Chua NH, Naqvi NI (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 16:1564-1574
58. Sweigard JA, Carroll AM, Farrall L, Chumley FG, Valent B (1998) Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol Plant Microbe Interact 11:404-412
59. Takano Y, Asakura M, Sakai Y (2009) Atg26-mediated pexophagy and fungal phytopathogenicity. Autophagy 5:1041-1042
60. Takano Y, Kubo Y, Shimizu K,Mise K, Okuno T, Furusawa I (1995) Structural analysis of PKS1, a polyketide synthase gene involved in melanin biosynthesis of Colletotrichum lagenarium. Mol Gen Genet 249:162-167
61. Talbot NJ (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57:177-202
62. Tanaka A, Tsuge T (2000) Structural and functional complexity of the genomic region controlling AK-toxin biosynthesis and pathogenicity in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 13:975-986
63. Taylor KM, Kaplan CP, Gao X, Baker A (1996) Localization and targeting of isocitrate lyases in Saccharomyces cerevisiae. Biochem J 319:255-262
64. Tey WK, North AJ, Reyes JL, Lu YF, Jedd G (2005) Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol Biol Cell 16:2651-2659
65. Thines E, Weber RW, Talbot NJ (2000) MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703-1718
66. Titorenko VI, Rachubinski RA (2001) The life cycle of the peroxisome. Nat Rev Mol Cell Biol 2:357-368
67. Titorenko VI, Rachubinski RA (2000) Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p. J Cell Biol 150:881-886
68. Titorenko VI, Smith JJ, Szilard RK, Rachubinski RA (1998) Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolse in the cytosol and for its targeting to the peroxisome. J Cell Biol 142:403-420
69. Trinci AP, Collinge AJ (1974) Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals. Protoplasma 80:57-67
70. Valenciano SJ, De Lucas R, Pedregosa A,Monistrol IF, Laborda F (1996) Induction of b-oxidation enzymes and microbody proliferation in Aspergillus nidulans. Arch Microbiol 166:336-341
71. Wanders RJA, Waterman HR (2004) Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorder. Clin Genet 67:107-133
72. Wang ZY, Jenkinson JM, Holcombe LJ, Soanes DM, Veneault-Fourrey C, Bhambra GK, Talbot NJ (2005) The molecular biology of appressorium turgor generation by the rice blast fungus Magnaporthe grisea. Biochem Soc Trans 33:384-388
73. Wang ZY, Soanes DM, Kershaw MJ, Talbot NJ (2007) Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid ß-oxidation during appressorium-mediated plant infection. Mol Plant Microbe Interact 20:475-491
74. Wang ZY, Thornton CR, Kershaw MJ, Debao L, Talbot NJ (2003) The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol 47:1601-1612
75. Weber RW, Wakley GE, Thines E, Talbot NJ (2001) The vacuole as central element of the lytic system and sink for lipid droplets in maturing appressoria of Magnaporthe grisea. Protoplasma 216:101-112
76. Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185-195
77. Yang J, Kong L, Chen X, Wang D, Qi L, Zhao W, Zhang Y, Liu X, Peng YL (2012) A carnitineacylcarnitine carrier protein, MoCrc1, is essential for pathogenicity in Magnaporthe oryzae. Curr Genet 58:139-148