Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen alternaria alternata

Eukaryotic Cell

Volumn 9, Issue 5, 2010, Pages 682-694

  Imazaki, Ai ^a   Tanaka, Aiko ^a   Harimoto, Yoshiaki ^a   Yamamoto, Mikihiro ^b   Akimitsu, Kazuya ^c   Park, Pyoyun ^d   Tsuge, Takashi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c KAGAWA UNIVERSITY   (Japan)

^d KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MYCOTOXIN;

ALTERNARIA; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; FUNGUS HYPHAE; GENETIC TRANSFORMATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; INTRACELLULAR SPACE; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MORPHOGENESIS; MUTATION; PATHOGENICITY; PEAR; PEROXISOME; PHENOTYPE; PLANT DISEASE; PROTEIN TRANSPORT;

ALTERNARIA; FUNGAL PROTEINS; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; HYPHAE; IMMUNITY, INNATE; INTRACELLULAR SPACE; MORPHOGENESIS; MUTATION; MYCOTOXINS; PEROXISOMES; PHENOTYPE; PLANT DISEASES; PROTEIN TRANSPORT; PYRUS; RECOMBINANT FUSION PROTEINS; TRANSFORMATION, GENETIC;

ALTERNARIA ALTERNATA; FUNGI; PYRUS; PYRUS PYRIFOLIA VAR. CULTA;

EID: 77953486651     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00369-09     Document Type: Article

References (68)

1. Ajiro, N., Y. Miyamoto, A. Masunaka, T. Tsuge, M. Yamamoto, K. Ohtani, T. Fukumoto, K. Gomi, T. L. Peever, Y. Izumi, Y. Tada, and K. Akimitsu. 2010. Role of the host-selective ACT-toxin synthesis gene ACTTS2 encoding an enoyl-reductase in pathogenicity of the tangerine pathotype of Alternaria alternata. Phytopathology 100:120-126.
2. Akagi, Y., H. Akamatsu, H. Otani, and M. Kodama. 2009. Horizontal chromosome transfer: a mechanism for the evolution and differentiation of a plant pathogenic fungus. Eukaryot. Cell 8:1732-1738.
3. Akagi, Y., M. Taga, M. Yamamoto, T. Tsuge, Y. Fukumasa-Nakai, H. Otani, and M. Kodama. 2009. Chromosome constitution of hybrid strains constructed by protoplast fusion between the tomato and strawberry pathotypes of Alternaria alternata. J. Gen. Plant Pathol. 75:101-109.
4. Altschul, S. F., T. L. Madden, A. A. Schäfer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
5. Asakura, M., S. Ninomiya, M. Sugimoto, M. Oku, S. Yamashita, T. Okuno, Y. Sakai, and Y. Takano. 2009. Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell 21:1291-1304.
6. Asakura, M., T. Okuno, and Y. Takano. 2006. Multiple contribution of peroxisomal metabolic function to fungal pathogenicity in Colletotrichum lagenarium. Appl. Environ. Microbiol. 72:6345-6354.
7. Beyer, A. 1997. Sequence analysis of the AAA protein family. Protein Sci. 6:2043-2058.
8. 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.
9. Brocard, C., and A. Harting. 2006. Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim. Biophys. Acta 1763:1565-1573.
10. Chida, T., and H. D. Sisler. 1987. Restoration of appressorial penetration ability by melanin precursors in Pyricularia oryzae treated with anti-penetrants and in melanin-deficient mutants. J. Pestic. Sci. 12:49-55.
11. Elgersma, Y., C. W. van Roermund, R. J. Wanders, and H. F. Tabak. 1995. Peroxisomal and mitochondrial carnitine acetyl-transferases of Saccharomyces cerevisiae are encoded by a single gene. EMBO J. 14:3472-3479.
12. Feng, B.-N., S. Nakatsuka, T. Goto, T. Tsuge, and S. Nishimura. 1990. Biosynthesis of host-selective toxins produced by Alternaria alternata pathogens. I. (8R,9S)-9,10-epoxy-8-hydroxy-9-methyl-deca-(2E,4Z,6E)-trienoic acid as a biological precursor of AK-toxins. Agric. Biol. Chem. 54:845-848.
13. Harimoto, Y., R. Hatta, M. Kodama, M. Yamamoto, H. Otani, and T. Tsuge. 2007. Expression profiles of genes encoded by the supernumerary chromosome controlling AM-toxin biosynthesis and pathogenicity in the apple pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 20:1463-1476.
14. Harimoto, Y., T. Tanaka, M. Kodama, M. Yamamoto, H. Otani, and T. Tsuge. 2008. Multiple copies of AMT2 are prerequisite for the apple pathotype of Alternaria alternata to produce enough AM-toxin for expressing pathogenicity. J. Gen. Plant Pathol. 74:222-229.
15. Hatta, R., K. Ito, Y. Hosaki, T. Tanaka, A. Tanaka, M. Yamamoto, K. Akimitsu, and T. Tsuge. 2002. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59-70.
16. Hayashi, N., K. Tanabe, T. Tsuge, S. Nishimura, K. Kohmoto, and H. Otani. 1990. Determination of host-selective toxin production during spore germination of Alternaria alternata by high-performance liquid chromatography. Phytopathology 80:1088-1091.
17. Howlett, B. J. 2006. Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr. Opin. Plant Biol. 9:371-375.
18. Idnurm, A., and B. J. Howlett. 2002. Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryot. Cell 1:719-724.
19. Inoue, I., F. Namiki, and T. Tsuge. 2002. Plant colonization by the vascular wilt fungus Fusarium oxysporum requires FOW1, a gene encoding a mitochondrial protein. Plant Cell 14:1869-1883.
20. Ito, K., T. Tanaka, R. Hatta, M. Yamamoto, K. Akimitsu, and T. Tsuge. 2004. Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol. Microbiol. 52:399-411.
21. Johnson, L., R. D. Johnson, H. Akamatsu, A. Salamiah, H. Otani, K. Kohmoto, and M. Kodama. 2001. Spontaneous loss of a conditionally dispensable chromosome from Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr. Genet. 40:65-72.
22. Kawamura, C., T. Tsujimoto, and T. Tsuge. 1999. Targeted disruption of a melanin biosynthesis gene affects conidial development and UV tolerance in the Japanese pear pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 12:59-63.
23. Keller, N. P., G. Turner, and J. W. Bennett. 2005. Fungal secondary metabolism-biochemistry to genomics. Nat. Rev. Microbiol. 3:937-947.
24. Kiel, J. A., R. E. Hilbrands, R. A. Bovenberg, and M. Veenhuis. 2000. Isolation of Penicillium chrysogenum PEX1 and PEX6 encoding AAA proteins involved in peroxisome biogenesis. Appl. Microbiol. Biotechnol. 54: 238-242.
25. 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 13:1945-1957.
26. Kimura, N., and T. Tsuge. 1993. Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J. Bacteriol. 175:4427-4435.
27. Kohmoto, K., Y. Itoh, N. Shimomura, Y. Kondoh, H. Otani, H. M. Kodama, S. Nishimura, and S. Nakatsuka. 1993. Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495-502.
28. Kohmoto, K., H. Otani, and T. Tsuge. 1995. Alternaria alternata pathogens, p. 51-63. In K. Kohmoto, U. S. Singh, and R. P. Singh (ed.), Pathogenesis and host specificity in plant diseases: histopathological biochemical, genetic and molecular bases, vol. II. Eukaryotes. Pergamon, Oxford, United Kingdom.
29. Lazarow, P. B. 2006. The import receptor Pex7p and the PTS2 targeting sequence. Biochim. Biophys. Acta 1763:1599-1604.
30. Lee, L. W., C. H. Chiou, K. L. Klomparens, J. W. Cray, and J. E. Linz. 2004. Subcellular localization of aflatoxin biosynthetic enzyme Nor-1, Ver-1, and OmtA in time-dependent fractionated colonies of Aspergillus parasiticus. Arch. Microbiol. 181:204-214.
31. Maekawa, N., M. Yamamoto, S. Nishimura, K. Kohmoto, M. Kuwata, and Y. Watanabe. 1984. Studies on host-specific AF-toxins produced by Alternaria alternata strawberry pathotype causing Alternaria black spot of strawberry. (1) Production of host-specific toxins and their biological activity. Ann. Phytopathol. Soc. Jpn. 50:600-609.
32. Maggio-Hall, L. A., R. A. Wilson, and N. P. Keller. 2005. Fundamental contribution of-oxidation to polyketide mycotoxin production in planta. Mol. Plant Microbe Interact. 18:783-793.
33. Masunaka, A., K. Ohtani, T. L. Peever, L. W. Timmer, T. Tsuge, M. Yamamoto, H. Yamamoto, and K. Akimitsu. 2005. An isolate of Alternaria alternata that is pathogenic to both tangerines and rough lemon and produces two host-selective toxins, ACT-and ACR-toxins. Phytopathology 95: 241-247.
34. Miyamoto, Y., Y. Isshiki, Y. A. Honda, A. Masunaka, T. Tsuge, M. Yamamoto, K. Ohtani, T. Fukumoto, K. Gomi, T. L. Peever, and K. Akimitsu. 2009. Function of genes encoding acyl-CoA synthetase and enoyl-CoA hydratase for host-selective ACT-toxin biosynthesis in the tangerine pathotype of Alternaria alternata. Phytopathology 99:369-377.
35. Miyamoto, Y., A. Masunaka, T. Tsuge, M. Yamamoto, K. Ohtani, T. Fukumoto, K. Gomi, T. L. Peever, and K. Akimitsu. 2008. Functional analysis of a multi-copy host-selective ACT-toxin biosynthesis gene in the tangerine pathotype of Alternaria alternata using RNA silencing. Mol. Plant Microbe Interact. 21:1591-1599.
36. Miyamoto, Y., A. Masunaka, T. Tsuge, M. Yamamoto, K. Ohtani, T. Fukumoto, K. Gomi, T. L. Peever, Y. Tada, K. Ichimura, and K. Akimitsu. 2010. ACTTS3 encoding a polyketide synthase is essential for the biosynthesis of ACT-toxin and pathogenicity in the tangerine pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 23:406-414.
37. Mullaney, E. J., J. E. Hamer, K. A. Roberti, M. M. Yelton, and W. E. Timberlake. 1985. Primary structure of the trpC gene from Aspergillus nidulans. Mol. Gen. Genet. 199:37-45.
38. Müller, W. H., R. A. Bovenberg, M. H. Groothuis, F. Kattevilder, E. B. Smaal, L. H. van der Voort, and A. J. Verkleij. 1992. Involvement of microbodies in penicillin biosynthesis. Biochim. Biophys. Acta 1116:210-213.
39. Müller, W. H., T. P. van der Krift, A. J. J. Krouwer, H. A. B. Wösten, L. H. M. van der Voort, E. B. Smaal, and A. J. Verkleij. 1991. Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J. 10:489-495.
40. Nakai, K., and P. Horton. 1999. PSORT: a program for detecting sorting signals in proteins and determining their subcellular localization. Trends Biochem. Sci. 24:34-35.
41. Nakashima, T., T. Ueno, H. Fukami, T. Taga, H. Masuda, K. Osaki, H. Otani, K. Kohmoto, and S. Nishimura. 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.
42. Nakatsuka, S., B.-N. Feng, T. Goto, T. Tsuge, and S. Nishimura. 1990. Biosynthetic origin of (8R,9S)-9,10-epoxy-8-hydroxy-9-methyl-deca-(2E,4Z,6E)-trienoic acid, a precursor of AK-toxins produced by Alternaria alternata Japanese pear pathotype. Phytochemistry 29:1529-1531.
43. Nakatsuka, S., K. Ueda, T. Goto, M. Yamamoto, S. Nishimura, and K. Kohmoto. 1986. Structure of AF-toxin II, one of the host-specific toxins produced by Alternaria alternata strawberry pathotype. Tetrahedron Lett. 27:2753-2756.
44. Namiki, F., M. Matsunaga, M. Okuda, I. Inoue, K. Nishi, Y. Fujita, and T. Tsuge. 2001. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant Microbe Interact. 14:580-584.
45. Otani, H., K. Kohmoto, S. Nishimura, T. Nakashima, T. Ueno, and H. Fukami. 1985. Biological activities of AK-toxins I and II, host-specific toxins from Alternaria alternata Japanese pear pathotype. Ann. Phytopathol. Soc. Jpn. 51:285-293.
46. Otani, H., S. Nishimura, and K. Kohmoto. 1983. Different responses of heat-shocked pear leaves to Alternaria alternata Japanese pear pathotype and AK-toxin. J. Fac. Agric. Tottori Univ. 18:1-8.
47. Otani, H., S. Nishimura, K. Kohmoto, K. Yano, and T. Seno. 1975. Nature of specific susceptibility to Alternaria kikuchiana in Nijisseiki cultivar among Japanese pears (V). Role of host-specific toxin in early step of infection. Ann. Phytopathol. Soc. Jpn. 41:467-476.
48. Platta, H. W., and R. Erdmann. 2007. Peroxisomal dynamics. Trends Cell Biol. 17:474-484.
49. Ramos-Pamplona, M., and N. I. Naqvi. 2006. Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acyl-CoA. Mol. Microbiol. 61:61-75.
50. Rotem, J. 1994. The genus Alternaria: biology, epidemiology, and pathogenicity. The American Phytopathological Society Press, St. Paul, MN.
51. Ruswandi, S. R., K. Kitani, K. Akimitsu, T. Tsuge, T. Shiraishi, and M. Yamamoto. 2005. Structural analysis of cosmid clone pcAFT-2 carrying AFT10-1 encoding an acyl-CoA dehydrogenase involved in AF-toxin production in the strawberry pathotype of Alternaria alternata. J. Gen. Plant Pathol. 71:107-116.
52. Sanderson, K. E., and A. M. Srb. 1965. Heterokaryosis and parasexuality in the fungus Ascochyta imperfecta. Am. J. Bot. 42:72-81.
53. Solomon, P. S., R. C. Lee, T. C. J. Wilson, and R. P. Oliver. 2004. Pathogenicity of Stagonospora nodorum requires malate synthase. Mol. Microbiol. 53:1065-1073.
54. Tanabe, K., P. Park, T. Tsuge, K. Kohmoto, and S. Nishimura. 1995. Characterization of the mutants of Alternaria alternata Japanese pear pathotype deficient in melanin production and their pathogenicity. Ann. Phytopathol. Soc. Jpn. 61:27-33.
55. Tanaka, A., H. Shiotani, M. Yamamoto, and T. Tsuge. 1999. Insertional mutagenesis and cloning of the genes required for biosynthesis of the host-specific AK-toxin in the Japanese pear pathotype of Alternaria alternata. Mol. Plant Microbe Interact. 12:691-702.
56. Tanaka, A., and T. Tsuge. 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.
57. Tanaka, S., K. Yamada, K. Yabumoto, S. Fujii, A. Huser, G. Tsuji, H. Koga, K. Dohi, M. Mori, T. Shiraishi, R. O'Connel, and Y. Kubo. 2007. Saccharomyces cerevisiae SSD1 orthologues are essential for host infection by the ascomycete plant pathogens Colletotrichum lagenarium and Magnaporthe grisea. Mol. Microbiol. 64:1332-1349.
58. Thomma, B. P. H. J. 2003. Alternaria spp.: from general saprophyte to specific parasite. Mol. Plant Pathol. 4:225-236.
59. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
60. Titorenko, V. I., and R. A. Rachubinski. 2001. The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2:357-368.
61. Tucker, S. L., and N. J. Talbot. 2001. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu. Rev. Phytopathol. 39:385-417.
62. van den Bosch, H., R. B. H. Schutgens, R. J. A. Wanders, and J. M. Tager. 1992. Biochemistry of peroxisomes. Annu. Rev. Biochem. 61:157-197.
63. van Roermund, C. W. T., H. R. Waterham, L. Ijlst, and R. J. A. Wanders. 2003. Fatty acid metabolism in Saccharomyces cerevisiae. Cell. Mol. Life Sci. 60:1838-1851.
64. Voorn-Brouwer, T., I. van der Leij, W. Hemrika, B. Distel, and H. F. Tabak. 1993. Sequence of the PAS8 gene, the product of which is essential for biogenesis of peroxisomes in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1216:325-328.
65. Wang, Z.-Y., D. M. Soanes, M. J. Kershaw, and N. J. Talbot. 2007. Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid -oxidation during appressorium-mediated plant infection. Mol. Plant Microbe Interact. 20:475-491.
66. Wang, Z.-Y., C. R. Thornton, M. J. Kershaw, L. Debao, and N. J. Talbot. 2003. The glyoxylate cycle is required for correct temporal regulation of virulence by the rice blast fungus Magnaporthe grisea. Mol. Microbiol. 47: 1601-1612.
67. Watanabe, C. M. H., and C. A. Townsend. 2002. Initial characterization of a type I fatty acid synthase and polyketide synthase multienzyme complex NorS in the biosynthesis of aflatoxin B1. Chem. Biol. 9:981-988.
68. Wolpert, T. J., L. D. Dunkle, and L. M. Ciuffetti. 2002. Host-selective toxins and avirulence determinants: what's in a name? Annu. Rev. Phytopathol. 40:251-285.