Role of the pathotype-specific ACRTS1 gene encoding a hydroxylase involved in the biosynthesis of host-selective ACR-toxin in the rough lemon pathotype of alternaria alternata

Phytopathology

Volumn 102, Issue 8, 2012, Pages 741-748

  Izumi, Yuriko ^a   Kamei, Eri ^a   Miyamoto, Yoko ^a   Ohtani, Kouhei ^a   Masunaka, Akira ^a   Fukumoto, Takeshi ^a   Gomi, Kenji ^a   Tada, Yasuomi ^a   Ichimura, Kazuya ^a   Peever, Tobin L ^b   Akimitsu, Kazuya ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MYCOTOXIN;

ALTERNARIA; ARTICLE; BIOSYNTHESIS; CITRUS; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; VIRULENCE;

ALTERNARIA; CITRUS; FUNGAL PROTEINS; MYCOTOXINS; PLANT DISEASES; VIRULENCE;

EID: 84865421009     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-02-12-0021-R     Document Type: Article

References (52)

1. Ajiro, N., Miyamoto, Y., Masunaka, A., Tsuge, T., Yamamoto, M., Ohtani, K., Fukumoto, T., Gomi, K., Peever, T. L., Izumi, Y., Tada, Y., and Akimitsu, K. 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., Akamatsu, H., Otani, H., and Kodama, M. 2009. Horizontal chromosome transfer: A mechanism for the evolution and differentiation of a plant pathogenic fungus. Eukaryot. Cell 8:1732-1738.
3. Akamatsu, H., Itoh, Y., Kodama, M., Otani, H., and Kohmoto, K. 1997. AAL-toxin-deficient mutants of Alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87:967-972.
4. Akamatsu, H., Otani, H., and Kodama, M. 2003. Characterization of a gene cluster for host-specific AAL-toxin biosynthesis in the tomato pathotype of Alternaria alternata. Fungal Genet. Newsl. 50:355.
5. Akamatsu, H., Taga, M., Kodama, M., Johnson, R., Otani, H., and Kohmoto, K. 1999. Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr. Genet. 35:647-656.
6. Akimitsu, K., Kohmoto, K., Otani, H., and Nishimura, S. 1989. Hostspecific effect of toxin from the rough lemon pathotype of Alternaria alternata on mitochondria. Plant Physiol. 89:952-931.
7. Akimitsu, K., Peever, T. L., and Timmer, L. W. 2003. Molecular, ecological and evolutionary approaches to understanding Alternaria diseases of citrus. Mol. Plant Pathol. 4:435-446.
8. Cogoni, C., Irelan, J., Schumacher, M., Schmidhauser, T. J., Selker, E. U., and Macino, G. 1996. Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J. 15:3153-3163.
9. Elbashir, S. M., Lendeckel, W., and Tuscchl, T. 2001. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15:188-200.
10. Fitzgerald, A., van Kan, J. A. L., and Plummer, K. M. 2004. Simultaneous silencing of multiple genes in the apple scab fungus, Venturia inaequalis, by expression of RNA with chimeric inverted repeats. Fungal Genet. Biol. 41:963-971.
11. Gardner, J. M., Kono, Y., Tatum, J. H., Suzuki, Y., and Takeuchi, S. 1985. Plant pathotoxins from Alternaria citri: The major toxin specific for rough lemon plants. Phytochemistry 24:2861-2867.
12. Gardner, J. M., Kono, Y., Tatum, J. H., Suzuki, Y., and Takeuchi, S. 1985. Structure of the major component of ACRL-toxins, host-specific pathotoxic compound produced by Alternaria citri. Agric. Biol. Chem. 49:1235-1238.
13. Hammond, T. M., and Keller, N. P. 2005. RNA silencing in Aspergillus nidulans is independent of RNA-dependent RNA polymerases. Genetics 169:607-617.
14. Harimoto, T., Hatta, R., Kodama, M., Yamamoto, M., Otani, H., and Tsuge, T. 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. 12:1463-1476.
15. Harimoto, T., Tanaka, T., Kodama, M., Yamamoto, M., Otani, H., and Tsuge, T. 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.
16. Hatta, R., Ito, K., Hosaki, Y., Tanaka, T., Tanaka, A., Yamamoto, M., Akimitsu, K., and Tsuge, K. 2002. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59-70.
17. Isshiki, A., Akimitsu, K., Yamamoto, M., and Yamamoto, H. 2001. Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol. Plant- Microbe Interact. 14:749-757.
18. Ito, K., Tanaka, A., Hatta, R., Yamamoto, M., Akimitsu, K., and Tsuge, T. 2004. Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol. Microbiol. 52:399-411.
19. Johnson, L. J., Johnson, R. D., Akamatsu, H., Salamiah, A., Otani, H., Kohmoto, K., and Kodama, M. 2001. Spontaneous loss of a conditionally dispensable chromosome from the Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr. Genet. 40:65-72.
20. Johnson, R. D., Johnson, L., Itoh, Y., Kodama, M., Otani, H., and Kohmoto, K. 2000. Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol. Plant-Microbe Interact. 13:742-753.
21. Kadotani, N., Nakayashiki, H., Tosa, Y., and Mayama, S. 2003. RNA silencing in the phytopathogenic fungus Magnaporthe oryzae. Mol. Plant- Microbe Interact. 16:769-776.
22. Kohmoto, K., Akimitsu, K., and Otani, H. 1991. Correlation of resistance and susceptibility of citrus to Alternaria alternata with sensitivity to hostspecific toxins. Phytopathology 81:719-722.
23. Kohmoto, K., Kondoh, Y., Kohguchi, T., Otani, H., Nishimura, S., and Sheffer, R. P. 1984. Ultrastructural changes in host leaf cells caused by host-selective toxin of Alternaria alternata from rough lemon. Can. J. Bot. 62:2485-2492.
24. Kohmoto, K., and Otani, H. 1991. Host recognition by toxigenic plant pathogens. Experientia 47:755-764.
25. Kohmoto, K., Otani, H., and Tsuge, T., (1995) Alternaria alternata pathogens. Pages 51-63 in: Pathogenesis and Host-Specificity in Plant Diseases: Histopathological, Biochemical Genetic and Molecule Bases, Vol. II, Eukaryotes. K. Kohmoto, U. S. Singh, and R. P. Singh, eds. Pergamon, Oxford.
26. Kohmoto, K., Sheffer, R. P., and Whiteside, J. O. 1979. Host-selective toxins from Alternaria citri. Phytopathology 69:667-671.
27. Kusaba, M., and Tsuge, T. 1995. Phylogeny of Alternaria fungi known to produce host-specific toxins on the basis of variation in internal transcribed spacers of ribosomal DNA. Curr. Genet. 28:491-498.
28. Liu, H., Cottrell, T. R., Pierini, L. M., Goldman, W. E., and Doering T. L. 2002. RNA interference in the pathogenic fungus Cryptococcus neoformans. Genetics 160:463-470.
29. Masunaka, A., Ohtani, K., Peever, T. L., Timmer, L. W., Tsuge, T., Yamamoto, M., Yamamoto, H., and Akimitsu, K. 2005. An isolate that is pathogenic to both tangerines and rough lemon and produces two hostselective toxins, ACT- and ACR-toxins. Phytopathology 95:241-247.
30. Masunaka, A., Tanaka, A., Tsuge, T., Peever, T. L., Timmer, L. W., Yamamoto, M., Yamamoto, H., and Akimitsu, K. 2000. Distribution and characterization of AKT homologs in the tangerine pathotype of Alternaria alternata. Phytopathology 90:762-768.
31. McDonald, T., Brown, D., Keller, N. P., and Hammond, T. M. 2005. RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol. Plant-Microbe Interact. 18:539-545.
32. Miyamoto, Y., Ishii, Y., Honda, A., Masunaka, A., Tsuge, T., Yamamoto, M., Ohtani, K., Fukumoto, T., Gomi, K., Peever, T. L., and Akimitsu, K. 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.
33. Miyamoto, Y., Masunaka, A., Tsuge, T., Yamamoto, M., Ohtani, K., Fukumoto, T., Gomi, K., Peever, T. L., and Akimitsu, K. 2008. Functional analysis of a multicopy host-selective ACT-toxin biosynthesis gene in the tangerine pathotype of Alternaria alternata using RNA silencing. Mol. Plant-Microbe Interact. 21:1591-1599.
34. Miyamoto, Y., Masunaka, A., Tsuge, T., Yamamoto, M., Ohtani, K., Fukumoto, T., Gomi, K., Peever, T. L., Tada, Y., Ichimura, K., and Akimitsu, K. 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.
35. Moriwaki, A., Ueno, M., Arase, S., and Kihara, J. 2007. RNA-mediated gene silencing in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol. Lett. 269:85-89.
36. Mouyna, I., Henry, C., Doering, T. L., and Latge, J. P. 2004. Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigates. FEMS Microbiol. Lett. 237:317-324.
37. Nakatsuka, S., Goto, T., Kohmoto, K., and Nishimura, S. 1986. Hostspecific phytotoxins. Pages 11-18 in: Natural Products and Biological Activities. H. Imura, T. Goto, T. Murachi, and T. Nakajima, eds. University of Tokyo Press, Tokyo.
38. Nakayashiki, H., Hanada, S., Quoc, N. B., Kadotani, N., Tosa, Y., and Mayama, S. 2005. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42:275-283.
39. Nishimura, S., and Kohmoto, K. 1983. Host-specific toxins and chemical structures from Alternaria species. Annu. Rev. Phytopathol. 21:87-116.
40. Ohtani, K., Yamamoto, H., and Akimitsu, K. 2002. Sensitivity to Alternaria alternata toxin in citrus because of altered mitochondrial RNA processing. Proc. Natl. Acad. Sci. USA 99:2439-2444.
41. Peever, T. L., Canihos, Y., Olsen, L., Ibanez, A., Liu, Y. C., and Timmer, L. W. 1999. Population genetic structure and host specificity of Alternaria spp. causing brown spot of Minneola tangelo and rough lemon in Florida. Phytopathology 89:851-860.
42. Peever, T. L., Su, G., Carpenter-Boggs, L., and Timmer, L. W. 2004. Molecular systematics of citrus-associated Alternaria species. Mycologia 96:119-134.
43. Rotem, J. 1994. The genus Alternaria. Pages 1-10 in: Biology, Epidemiology, and Pathogenicity. The American Phytopathological Society, St. Paul, MN
44. Ruswandi, S., Kitani, K., Akimitsu, K., Tsuge, T., Shiraishi, T., and Yamamoto, M. 2005. Structural analysis of cosmid clone pcAFT-2 carrying AFT10-1 encoding an acyl-CoA dehydrogenase involved in AFtoxin production in the strawberry pathotype of Alternaria alternata. J. Gen. Plant Pathol. 71:107-116.
45. Sanger, F., Nicklen, S., and Coulson, A. R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
46. Scheffer, R. P., and Livingston, R. S. 1984. Host-selective toxins and their role in plant diseases. Science 223:17-21.
47. Tanaka, A., Shiotani, H., Yamamoto, M., and Tsuge, T. 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.
48. Tanaka, A., and 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.
49. Thomma, B. P. H. J. 2003. Alternaria spp.: From general saprophyte to specific parasite. Mol. Plant-Microbe Interact. 4:225-236.
50. Walton, J. D. 1996. Host-selective toxins: Agents of compatibility. Plant Cell 8:1723-1733.
51. Wolpert, T. J., Dunkle, L. D., and Ciuffetti, L. M. 2002. Host-selective toxins and avirulence determinants: What's in a name? Annu. Rev. Phytopathol. 40:251-285.
52. Yoder, O. C. 1980. Toxins in pathogenesis. Annu. Rev. Phytopathol. 18:103-129.