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At Death's Door: Alternaria Pathogenicity Mechanisms

  • Lawrence, Christopher B. (Virginia Bioinformatics Institute and Department of Biological Sciences) ;
  • Mitchell, Thomas K. (Department of Plant Pathology, Ohio State University) ;
  • Craven, Kelly D. (Plant Biology Division, Samuel Roberts Noble Foundation) ;
  • Cho, Yang-Rae (Department of Plant and Environmental Protection Sciences, University of Hawaii) ;
  • Cramer, Robert A. (Department of Veterinary Molecular Biology, Montana State University) ;
  • Kim, Kwang-Hyung (Virginia Bioinformatics Institute and Department of Biological Sciences)
  • 발행 : 2008.06.30

초록

The fungal genus Alternaria is comprised of many saprophytic and endophytic species, but is most well known as containing many notoriously destructive plant pathogens. There are over 4,000 Alternaria/host associations recorded in the USDA Fungal Host Index ranking the genus 10th among nearly 2,000 fungal genera based on the total number of host records. While few Alternaria species appear to have a sexual stage to their life cycles, the majority lack sexuality altogether. Many pathogenic species of Alternaria are prolific toxin producers, which facilitates their necrotrophic lifestyle. Necrotrophs must kill host cells prior to colonization, and thus these toxins are secreted to facilitate host cell death often by triggering genetically programmed apoptotic pathways or by directly causing cell damage resulting in necrosis. While many species of Alternaria produce toxins with rather broad host ranges, a closely-related group of agronomically important Alternaria species produce selective toxins with a very narrow range often to the cultivar level. Genes that code for and direct the biosynthesis of these host-specific toxins for the Alternaria alternata sensu lato lineages are often contained on small, mostly conditionally dispensable, chromosomes. Besides the role of toxins in Alternaria pathogenesis, relatively few genes and/or gene products have been identified that contribute to or are required for pathogenicity. Recently, the completion of the A. brassicicola genome sequencing project has facilitated the examination of a substantial subset of genes for their role in pathogenicity. In this review, we will highlight the role of toxins in Alternaria pathogenesis and the use of A. brassicicola as a model representative for basic virulence studies for the genus as a whole. The current status of these research efforts will be discussed.

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참고문헌

  1. 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. https://doi.org/10.1094/PHYTO.1997.87.9.967
  2. Arrese, J. E., PierardFranchimont, C. and Pierard, G. E. 1996. Onychomycosis and keratomycosis caused by Alternaria sp.: A bipolar opportunistic infection in a wood-pulp worker on chronic steroid therapy. Am. J. Dermatopathol. 18:611-613. https://doi.org/10.1097/00000372-199612000-00011
  3. Ballance, G. M., Lamari, L. and Bernier, C. C. 1989. Purification and characterization of a host-selective necrosis toxin from Pyrenophora tritici-repentis. Physiol. Mol. Plant Pathol. 35:203-213. https://doi.org/10.1016/0885-5765(89)90051-9
  4. Barbasso, E., Sforza, F., Stoppini, R. and Peruccio, C. 2005. Mycotic flora in the conjunctival fornix of horses in Northern Italy. Ippologia 16:21-29.
  5. Barnes, S. D., Dohlman, C. H. and Durand, M. L. 2007. Fungal colonization and infection in Boston keratoprosthesis. Cornea 26:9-15. https://doi.org/10.1097/01.ico.0000224650.19837.25
  6. Berto, P., Commenil, P., Belingheri, L. and Dehorter, B. 1999. Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in the infection of cauliflower leaves. FEMS Microbiol. Lett. 180:183-189. https://doi.org/10.1111/j.1574-6968.1999.tb08794.x
  7. Black, P. N., Udy, A. A. and Brodie, S. M. 2000. Sensitivity to fungal allergens is a risk factor for life-threatening asthma. Allergy 55:501-504. https://doi.org/10.1034/j.1398-9995.2000.00293.x
  8. Brader, G., Djamei, A., Teige, M., Palva, E. T. and Hirt, H. 2007. The MAP kinase kinase MKK2 affects disease resistance in Arabidopsis. Mol. Plant-Microbe Interact. 20:589-596. https://doi.org/10.1094/MPMI-20-5-0589
  9. Brodersen, P., Petersen, M., Nielsen, H. B., Zhu, S. J., Newman, M. A., Shokat, K. M., Rietz, S., Parker, J. and Mundy, J. 2006. Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47:532-546. https://doi.org/10.1111/j.1365-313X.2006.02806.x
  10. Brugger, E. M., Wagner, J., Schumacher, D. M., Koch, K., Podlech, J., Metzler, M. and Lehmann, L. 2006. Mutagenicity of the mycotoxin alternariol in cultured mammalian cells. Toxicol. Lett. 164:221-230. https://doi.org/10.1016/j.toxlet.2006.01.001
  11. Bush, R. K. and Prochnau, J. J. 2004. Alternaria-induced asthma. J. Allergy Clin. Immunol. 113:227-234. https://doi.org/10.1016/j.jaci.2003.11.023
  12. Cho, Y., Cramer, R. A., Kim, K. H., Davis, J., Mitchell, T. K., Figuli, P., Pryor, B. M., Lemasters, E. and Lawrence, C. B. 2007. The Fus3/Kss1 MAP kinase homolog Amk1 regulates the expression of genes encoding hydrolytic enzymes in Alternaria brassicicola. Fungal Genet. Biol. 44:543-553. https://doi.org/10.1016/j.fgb.2006.11.015
  13. Cho, Y., Kim, K.-H., La Rota, C. M., Scott, D., Santopietro, G., Callihan, M., Mitchell, T. K. and Lawrence, C. B. 2008. Identification of novel virulence factors associated with signal transduction pathways in Alternaria brassicicola. Mol. Microbiol. (in press).
  14. Cho, Y., Davis, J. W., Kim, K. H., Wang, J., Sun, Q. H., Cramer, R. A. and Lawrence, C. B. 2006. A high throughput targeted gene disruption method for Alternaria brassicicola functional genomics using linear minimal element (LME) constructs. Mol. Plant-Microbe Interact. 19:7-15. https://doi.org/10.1094/MPMI-19-0007
  15. Conn, K. L., Tewari, J. P. and Dahiya, J. S. 1988. Resistance to Alternaria brassicae and phytoalexin elicitation in rapeseed and other crucifers. Plant Sci. 56:21-25. https://doi.org/10.1016/0168-9452(88)90180-X
  16. Cooke, D. E. L., Jenkins, P. D. and Lewis, D. M. 1997. Production of phytotoxic spore germination liquids by Alternaria brassicae and A. brassicicola and their effect on species of the family Brassicaceae. Ann. Appl. Biol. 131:413-426. https://doi.org/10.1111/j.1744-7348.1997.tb05169.x
  17. Cramer, R. A., La Rota, C. M., Cho, Y., Thon, M., Craven, K. D., Knudson, D. L., Mitchell, T. K. and Lawrence, C. B. 2006. Bioinformatic analysis of expressed sequence tags derived from a compatible Alternaria brassicicola-Brassica oleracea interaction. Mol. Plant Pathol. 7:113-124. https://doi.org/10.1111/j.1364-3703.2006.00324.x
  18. Cramer, R. A. and Lawrence, C. B. 2003. Cloning of a gene encoding an Alt a 1 isoallergen differentially expressed by the necrotrophic fungus Alternaria brassicicola during Arabidopsis infection. Appl. Environ. Microbiol. 69:2361-2364. https://doi.org/10.1128/AEM.69.4.2361-2364.2003
  19. Cramer, R. A. and Lawrence, C. B. 2004. Identification of Alternaria brassicicola genes expressed in planta during pathogenesis of Arabidopsis thaliana. Fungal Genet. Biol. 41:115-128. https://doi.org/10.1016/j.fgb.2003.10.009
  20. Craven, K. D., Velez, H., Cho, Y., Lawrence, C. B. and Mitchell, T. K. 2008. Anastomosis is required for virulence of the fungal necrotroph, Alternaria brassicicola. Eukaryot. Cell 7:675-683. https://doi.org/10.1128/EC.00423-07
  21. Dillard, H. R., Cobb, A. C. and Lamboy, J. S. 1998. Transmission of Alternaria brassicicola to cabbage by flea beetles (Phyllotreta cruciferae). Plant Dis. 82:153-157. https://doi.org/10.1094/PDIS.1998.82.2.153
  22. Feng, B. N., Nakatsuka, S., Goto, T., Tsuge, T. and Nishimura, S. 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. https://doi.org/10.1271/bbb1961.54.845
  23. Gilchrist, D. G. 1997. Mycotoxins reveal connections between plants and animals in apoptosis and ceramide signaling. Cell Death Differ. 4:689-698. https://doi.org/10.1038/sj.cdd.4400312
  24. Hatta, R., Ito, K., Hosaki, Y., Tanaka, T., Tanaka, A., Yamamoto, M., Akimitsu, K. and Tsuge, T. 2002. A conditionally dispens able chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59-70.
  25. Hazouard, E., Doucet, O., Therizol-Ferly, M., Mayelo, V., Dequin, P. F., Legras, A. and Perrotin, D. 1999. Fatal septic shock to Alternaria alternata. Med. Mal. Infect. 29:136-138. https://doi.org/10.1016/S0399-077X(99)80025-0
  26. Hong, S. G., Cramer, R. A., Lawrence, C. B. and Pryor, B. M. 2005. Alt a 1 allergen homologs from Alternaria and related taxa: analysis of phylogenetic content and secondary structure. Fungal Genet. Biol. 42:119-129. https://doi.org/10.1016/j.fgb.2004.10.009
  27. Humpherson-Jones, F. M. 1983. The occurrence of Alternaria brassicicola, Alternaria brassicae and Leptosphaeria maculans in brassica seed crops in south-east England between 1976 and 1980. Plant Pathol. 32:33-39. https://doi.org/10.1111/j.1365-3059.1983.tb01298.x
  28. Humpherson-Jones, F. M. 1985. The incidence of Alternaria spp. and Leptosphaeria maculans in commercial brassica seed in the United Kingdom. Plant Pathol. 34:385-390. https://doi.org/10.1111/j.1365-3059.1985.tb01377.x
  29. Humpherson-Jones, F. M. 1989. Survival of Alternaria brassicae and Alternaria brassicicola on crop debris of oilseed rape and cabbage. Ann. Appl. Biol. 115:45-50. https://doi.org/10.1111/j.1744-7348.1989.tb06810.x
  30. Humpherson-Jones, F. M. and Maude, R. B. 1982a. Control of dark leaf spot (Alternaria brassicicola) of Brassica oleracea seed production crops with foliar sprays of iprodione. Ann. Appl. Biol. 100:99-104. https://doi.org/10.1111/j.1744-7348.1982.tb07196.x
  31. Humpherson-Jones, F. M. and Maude, R. B. 1982b. Studies on the epidemiology of Alternaria brassicicola in Brassica oleracea seed production crops. Ann. Appl. Biol. 100:61-71. https://doi.org/10.1111/j.1744-7348.1982.tb07192.x
  32. Humpherson-Jones, F. M. and Phelps, K. 1989. Climatic factors influencing spore production in Alternaria brassicae and Alternaria brassicicola. Ann. Appl. Biol. 114:449-458. https://doi.org/10.1111/j.1744-7348.1989.tb03360.x
  33. Johnson, R. D., Johnson, L., Itoh, Y., Kodama, M., Otani, H. and Kahmoto, 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. https://doi.org/10.1094/MPMI.2000.13.7.742
  34. Kagan, I. A. and Hammerschmidt, R. 2002. Arabidopsis ecotype variability in camalexin production and reaction to infection by Alternaria brassicicola. J. Chem. Ecol. 28:2121-2140. https://doi.org/10.1023/A:1021020512846
  35. Kim, K. H., Cho, Y., La Rota, M., Cramer, R. A. and Lawrence, C. B. 2007. Functional analysis of the Alternaria brassicicola non-ribosomal peptide synthetase gene AbNPS2 reveals a role in conidial cell wall construction. Mol. Plant Pathol. 8:23-39. https://doi.org/10.1111/j.1364-3703.2006.00366.x
  36. King, S. R. 1994. Screening, selection, and genetics of resistance to Alternaria diseases in Brassica oleracea. Ph.D. thesis, Cornell University, Ithaca, USA.
  37. Kohmoto, K., Itoh, Y., Shimomura, N., Kondoh, Y., Otani, H., Kodama, M., et al. 1993. Isolation and biological activities of 2 host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495-502. https://doi.org/10.1094/Phyto-83-495
  38. Li, J., Brader, G., Kariola, T. and Palva, E. T. 2006. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 46:477-491. https://doi.org/10.1111/j.1365-313X.2006.02712.x
  39. Liu, G. T., Qian, Y. Z., Zhang, P., Dong, W. H., Qi, Y. M. and Guo, H.T. 1992. Etiologic role of Alternaria alternata in human esophageal cancer. Chin. Med. J. 105:394-400.
  40. Machet, M. C., Stephanov, E., Esteve, E., Declosets, F., Barrabes, A., Therizolferly, M., et al. 1994. Cutaneous alternariosis occurring in the course of pemphigus: report on 2 cases. Ann. Pathol. 14:186-191.
  41. MacKinnon, S. L., Keifer, P. and Ayer, W. A. 1999. Components from the phytotoxic extract of Alternaria brassicicola, a black spot pathogen of canola. Phytochemistry 51:215-221. https://doi.org/10.1016/S0031-9422(98)00732-8
  42. Maiero, M., Bean, G. A. and Ng, T. J. 1991. Toxin production by Alternaria solani and its related phytotoxicity to tomato breeding lines. Phytopathology 81:1030-1033. https://doi.org/10.1094/Phyto-81-1030
  43. Masunaka, A., Ohtani, K., Peever, T.L., Timmer, L. W., Tsuge, T., Yamamoto, M., et al. 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. https://doi.org/10.1094/PHYTO-95-0241
  44. Maude, R. B. and Humpherson-Jones, F. M. 1980. Studies on the seed-borne phases of dark leaf spot (Alternaria brassicicola) and grey leaf spot (Alternaria brassicae) of brassicas. Ann. Appl. Biol. 95:311-319. https://doi.org/10.1111/j.1744-7348.1980.tb04752.x
  45. Mckenzie, K. J., Robb, J. and Lennard, J. H. 1988. Toxin production by Alternaria pathogens of oilseed rape (Brassica napus). Crop Res. 28:67-81.
  46. Mengiste, T., Chen, X., Salmeron, J. and Dietrich, R. 2003. The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551-2565. https://doi.org/10.1105/tpc.014167
  47. Mirkin, L. D. 1994. Alternaria alternata infection of skin in a 6-year-old boy with aplastic anemia. Pediatr. Pathol. 14:757-761. https://doi.org/10.3109/15513819409037672
  48. Morrison, V. A. and Weisdorf, D. J. 1993. Alternaria: a sinonasal pathogen of immunocompromised hosts. Clin. Infect. Dis. 16:265-270. https://doi.org/10.1093/clind/16.2.265
  49. Nakashima, T., Ueno, T., Fukami, H., Taga, T., Masuda, H., Osaki, K., et al. 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. https://doi.org/10.1271/bbb1961.49.807
  50. Nakatsuka, S., Feng, B. N., Goto, T., Tsuge, T. and Nishimura, S. 1990. Biosynthesis of host-selective toxins produced by Alternaria alternata pathogens, 2: 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. Phytochemistry 29:1529-1531. https://doi.org/10.1016/0031-9422(90)80114-V
  51. Nakatsuka, S., Ueda, K., Goto, T., Yamamoto, M., Nishimura, S. and Kohmoto, K. 1986. Structure of AF-toxin II, one of the host-specific toxins produced by Alternaria alternata strawberry pathotype. Tetrahedron Lett. 27:2753-2756. https://doi.org/10.1016/S0040-4039(00)84635-3
  52. Neumeister, B., Hartmann, W., Oethinger, M., Heymer, B. and Marre, R. 1994. A fatal infection with Alternaria alternata and Aspergillus terreus in a child with agranulocytosis of unknown origin. Mycoses 37:181-185. https://doi.org/10.1111/j.1439-0507.1994.tb00297.x
  53. Oh, I. S., Park, A. R., Bae, M. S., Kwon, S. J., Kim, Y. S., Lee, J. E., Kang, N. Y., Lee, S., Cheong, H. and Park, O. K. 2005. Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17:2832-2847. https://doi.org/10.1105/tpc.105.034819
  54. Ohollaren, M. T., Yunginger, J. W., Offord, K. P., Somers, M. J., Oconnell, E. J., Ballard, D. J. and Sachs, M. I. 1991. Exposure to an aeroallergen as a possible precipitating factor in respiratory arrest in young-patients with asthma. N. Engl. J. Med. 324:359-363. https://doi.org/10.1056/NEJM199102073240602
  55. Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K. and Turgeon, B. G. 2006. NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836-2853. https://doi.org/10.1105/tpc.106.045633
  56. Ospina-Giraldo, M. D., Mullins, E. and Kang, S. 2003. Loss of function of the Fusarium oxysporum SNF1 gene reduces virulence on cabbage and Arabidopsis. Curr. Genet. 44:49-57. https://doi.org/10.1007/s00294-003-0419-y
  57. Otani, H., Kohmoto, K. and Kodama, M. 1995. Alternaria toxins and their effects on host plants. Can. J. Bot. 73:S453-S458. https://doi.org/10.1139/b95-282
  58. Otani, H., Kohnobe, A., Kodama, M. and Kohmoto, K. 1998. Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiol. Mol. Plant Pathol. 52:285-295. https://doi.org/10.1006/pmpp.1998.0147
  59. Palecek, S. P., Parikh, A. S., Huh, J. H. and Kron, S. J. 2002. Depression of Saccharomyces cerevisiae invasive growth on non-glucose carbon sources requires the Snf1 kinase. Mol. Microbiol. 45:453-469. https://doi.org/10.1046/j.1365-2958.2002.03024.x
  60. Pattanamahakul, P. and Strange, R. N. 1999. Identification and toxicity of Alternaria brassicicola, the causal agent of dark leaf spot disease of Brassica species grown in Thailand. Plant Pathol. 48:749-755. https://doi.org/10.1046/j.1365-3059.1999.00406.x
  61. Plaza, V., Serrano, J., Picado, C., Cosano, J., Ancochea, J., de Diego, A., Martin, J. J. and Sanchis, J. 2003. Clinical characteristics of the fatal and near-fatal asthma in Alternaria alternata sensitized patients. Med. Clin. 121:721-724. https://doi.org/10.1016/S0025-7753(03)74076-7
  62. Rimmer, S. R. and Buchwaldt, H. 1995. Diseases. In: Brassica oilseeds-production and utilization, ed. by D. Kimber and D.I. Mcgregor, pp. 111-140. CAB International, Wallingford, UK.
  63. Romano, C., Paccagnini, E. and Difonzo, E. M. 2001. Onychomycosis caused by Alternaria spp. in Tuscany, Italy from 1985 to 1999. Mycoses 44:73-76. https://doi.org/10.1046/j.1439-0507.2001.00622.x
  64. Rotem, J. 1994. The Genus Alternaria. biology, epidemiology, and pathogenicity. APS Press, St. Paul.
  65. Saenz-de-Santamaria, M., Guisantes, J. A. and Martinez, J. 2006. Enzymatic activities of Alternaria alternata allergenic extracts and its major allergen (Alt a 1). Mycoses 49:88-292.
  66. Schenk, P. M., Kazan, K., Manners, J. M., Anderson, J. P., Simpson, R. S., Wilson, I. W., Somerville, S. C. and Maclean, D. J. 2003. Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol. 132:999-1010. https://doi.org/10.1104/pp.103.021683
  67. Schenk, P. M., Kazan, K., Wilson, I., Anderson, J. P., Richmond, T., Somerville, S. C., et al. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97:11655-11660. https://doi.org/10.1073/pnas.97.21.11655
  68. Shin, S. H., Lee, Y. H. and Jeon, C. H. 2006. Protease-dependent activation of nasal polyp epithelial cells by airborne fungi leads to migration of eosinophils and neutrophils. Acta Otolaryngol. 126:1286-1294. https://doi.org/10.1080/00016480500395179
  69. Shin, S. H., Ponikau, J. U., Sherris, D. A., Congdon, D., Frigas, E., Homburger, H. A., Swanson, M., Gleich, G. and Kita, H. 2004. Chronic rhinosinusitis: An enhanced immune response to ubiquitous airborne fungi. J. Allergy Clin. Immunol. 114:1369-1375. https://doi.org/10.1016/j.jaci.2004.08.012
  70. Sigareva, M.A. and Earle, E. D. 1999a. Camalexin induction in intertribal somatic hybrids between Camelina sativa and rapid cycling Brassica oleracea. Theor. Appl. Genet. 98:164-170. https://doi.org/10.1007/s001220051053
  71. Sigareva, M. A. and Earle, E. D. 1999b. Regeneration of plants from protoplasts of Capsella bursapastoris and somatic hybridization with rapid cycling Brassica oleracea. Plant Cell Rep. 18:412-417. https://doi.org/10.1007/s002990050595
  72. Staswick, P. E., Yuen, G. Y. and Lehman, C. C. 1998. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. Plant J. 15:747-754. https://doi.org/10.1046/j.1365-313X.1998.00265.x
  73. Thaker, A. J., Devouge, M. W., Zhang, L., Muradia, G., Rode, H. and Vijay, H. M. 1995. Molecular cloning of Ige-binding allergens from Alternaria alternata. J. Allergy Clin. Immunol. 95:348-348.
  74. Thomma, B. P. H. J. 2003. Alternaria spp.: from general saprophyte to specific parasite. Mol. Plant Pathol. 4:225-236. https://doi.org/10.1046/j.1364-3703.2003.00173.x
  75. Thomma, B. P. H. J., Eggermont, K., Broekaert, W. F. and Cammue, B. P. A. 2000. Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38:421-427. https://doi.org/10.1016/S0981-9428(00)00756-7
  76. Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A. and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95:15107-15111. https://doi.org/10.1073/pnas.95.25.15107
  77. Thomma, B. P. H. J., Eggermont, K., Tierens, K. F. M. J. and Broekaert, W. F. 1999a. Requirement of functional ethyleneinsensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 121:1093-1101. https://doi.org/10.1104/pp.121.4.1093
  78. Thomma, B. P. H. J., Nelissen, I., Eggermont, K. and Broekaert, W. F. 1999b. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J. 19:163-171. https://doi.org/10.1046/j.1365-313X.1999.00513.x
  79. Thomma, B. P. H. J., Tadesse, Y. S. H., Cammue, B. P. A. and Broekaert, W. F. 1997. Susceptibility of an ethylene response mutant of Arabidopsis thaliana to Botrytis cinerea and Alternaria brassicicola. Plant Physiol. 114:1177-1177. https://doi.org/10.1104/pp.114.4.1177
  80. Tierens, K. F. M. J., Thomma, B. P. H. J., Bari, R. P., Garmier, M., Eggermont, K., Brouwer, M., Penninckx, I. A. M. A., Broekaert, W. F. and Cammue, B. P. A. 2002. Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defense responses by reactive oxygen generating compounds. Plant J. 29:131-140. https://doi.org/10.1046/j.1365-313x.2002.01199.x
  81. Tomas, A., Feng, G. H., Reeck, G. R., Bockus, W. W. and Leach, J. E. 1990. Purification of a cultivar-specific toxin from Pyrenophora tritici-repentis, causal agent of tan spot of wheat. Mol. Plant-Microbe Interact. 3:221-224. https://doi.org/10.1094/MPMI-3-221
  82. Tonukari, N. J., Scott-Craig, J. S. and Walton, J. D. 2000. The Cochliobolus carbonum SNF1 gene is required for cell walldegrading enzyme expression and virulence on maize. Plant Cell 12:237-248. https://doi.org/10.1105/tpc.12.2.237
  83. Tuori, R. P., Wolpert, T. J. and Ciuffetti, L. M. 1995. Purification and immunological characterization of toxic components from cultures of Pyrenophora tritici-repentis. Mol. Plant-Microbe Interact. 8:41-48. https://doi.org/10.1094/MPMI-8-0041
  84. van Wees, S. C. M., Chang, H. S., Zhu, T. and Glazebrook, J. 2003. Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol. 132:606-617. https://doi.org/10.1104/pp.103.022186
  85. Vartivarian, S. E., Anaissie, E. J. and Bodey, G. P. 1993. Emerging fungal pathogens in immunocompromised patients: classification, diagnosis, and management. Clin. Infect. Dis. 17:S487-S491. https://doi.org/10.1093/clinids/17.Supplement_2.S487
  86. Vijayan, P., Shockey, J., Levesque, C. A., Cook, R. J. and Browse, J. 1998. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. USA 95:7209-7214. https://doi.org/10.1073/pnas.95.12.7209
  87. Wang, H., Jones, C., CiacciZanella, J., Holt, T., Gilchrist, D. G. and Dickman, M. B. 1996. Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc. Natl. Acad. Sci. USA 93:3461-3465. https://doi.org/10.1073/pnas.93.8.3461
  88. Westman, A. L., Kresovich, S. and Dickson, M. H. 1999. Regional variation in Brassica nigra and other weedy crucifers for disease reaction to Alternaria brassicicola and Xanthomonas campestris pv. campestris. Euphytica 106:253-259. https://doi.org/10.1023/A:1003544025146
  89. Xu, J. R. 2000. MAP kinases in fungal pathogens. Fungal Genet. Biol. 31:137-152. https://doi.org/10.1006/fgbi.2000.1237
  90. Yao, C. and Koller, W. 1994. Diversity of cutinases from plant pathogenic fungi: Cloning and characterization of a cutinase gene from Alternaria brassicicola. Physiol. Mol. Plant Pathol. 44:81-92. https://doi.org/10.1016/S0885-5765(05)80103-1
  91. Yao, C. L. and Koller, W. 1995. Diversity of cutinases from plant pathogenic fungi: Different cutinases are expressed during saprophytic and pathogenic stages of Alternaria brassicicola. Mol. Plant-Microbe Interact. 8:122-130. https://doi.org/10.1094/MPMI-8-0122
  92. Yekeler, H., Bitmis, K., Ozcelik, N., Doymaz, M. Z. and Calta, M. 2001. Analysis of toxic effects of Alternaria toxins on esophagus of mice by light and electron microscopy. Toxicol. Pathol. 29:492-497. https://doi.org/10.1080/01926230152499980
  93. Yunginger, J. W. and Jones, R. T. 1978. Isolation of Alternaria allergens. Fed. Proc. 37:1553-1553.
  94. Zheng, Z. Y., Abu Qamar, S., Chen, Z. X. and Mengiste, T. 2006. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48:592-605. https://doi.org/10.1111/j.1365-313X.2006.02901.x
  95. Zhou, N., Tootle, T. L. and Glazebrook, J. 1999. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419-2428. https://doi.org/10.1105/tpc.11.12.2419

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  1. Metabolism of the phytoalexins camalexins, their bioisosteres and analogues in the plant pathogenic fungus Alternaria brassicicola vol.21, pp.15, 2013, https://doi.org/10.1016/j.bmc.2013.05.026
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  3. Arabidopsis cell death in compatible and incompatible interactions with Alternaria brassicicola vol.31, pp.6, 2011, https://doi.org/10.1007/s10059-011-2203-z
  4. Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer vol.13, pp.1, 2012, https://doi.org/10.1186/1471-2164-13-171
  5. Comparative pathobiology of Heterobasidion annosum during challenge on Pinus sylvestris and Arabidopsis roots: an analysis of defensin gene expression in two pathosystems vol.239, pp.3, 2014, https://doi.org/10.1007/s00425-013-2012-z
  6. Serine protease identification (in vitro) and molecular structure predictions (in silico) from a phytopathogenic fungus,Alternaria solani vol.54, pp.S1, 2014, https://doi.org/10.1002/jobm.201300433
  7. A Pectate Lyase-Coding Gene Abundantly Expressed during Early Stages of Infection Is Required for Full Virulence in Alternaria brassicicola vol.10, pp.5, 2015, https://doi.org/10.1371/journal.pone.0127140
  8. Phenotypic and phylogenetic segregation ofAlternaria infectoriafrom small-sporedAlternariaspecies isolated from wheat in Germany and Russia vol.119, pp.6, 2015, https://doi.org/10.1111/jam.12951
  9. All Mold Is Not Alike: The Importance of Intraspecific Diversity in Necrotrophic Plant Pathogens vol.6, pp.3, 2010, https://doi.org/10.1371/journal.ppat.1000759
  10. Functional genomics tools to decipher the pathogenicity mechanisms of the necrotrophic fungusPlectosphaerella cucumerinainArabidopsis thaliana vol.14, pp.1, 2013, https://doi.org/10.1111/j.1364-3703.2012.00826.x
  11. Beneficial endophytic microorganisms of Brassica – A review vol.90, 2015, https://doi.org/10.1016/j.biocontrol.2015.06.001
  12. A novel role of ammonia in appressorium formation of Alternaria alternata (Fries) Keissler, a tobacco pathogenic fungus vol.117, pp.3, 2010, https://doi.org/10.1007/BF03356345
  13. Mycotoxins as antagonistic or supporting agents in the interaction between phytopathogenicFusariumandAlternariafungi vol.8, pp.3, 2015, https://doi.org/10.3920/WMJ2014.1747
  14. The Pepper Calmodulin GeneCaCaM1Is Involved in Reactive Oxygen Species and Nitric Oxide Generation Required for Cell Death and the Defense Response vol.22, pp.11, 2009, https://doi.org/10.1094/MPMI-22-11-1389
  15. Overexpression of Withania somnifera SGTL1 gene resists the interaction of fungus Alternaria brassicicola in Arabidopsis thaliana vol.97, 2017, https://doi.org/10.1016/j.pmpp.2016.11.003
  16. Jasmonic acid signalling mediates resistance of the wild tobaccoNicotiana attenuatato its nativeFusarium, but notAlternaria, fungal pathogens vol.38, pp.3, 2015, https://doi.org/10.1111/pce.12416
  17. Proteomics of Plant Pathogenic Fungi vol.2010, 2010, https://doi.org/10.1155/2010/932527
  18. Impact of the UPR on the virulence of the plant fungal pathogenA. brassicicola vol.5, pp.2, 2014, https://doi.org/10.4161/viru.26772
  19. Biodiversity and taxonomy of the pleomorphic genus Alternaria vol.15, pp.1, 2016, https://doi.org/10.1007/s11557-015-1144-x
  20. The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi vol.8, pp.1, 2012, https://doi.org/10.1186/1746-4811-8-16
  21. ArabidopsisABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin vol.114, pp.28, 2017, https://doi.org/10.1073/pnas.1702259114
  22. The phytoalexin camalexin induces fundamental changes in the proteome of Alternaria brassicicola different from those caused by brassinin vol.118, pp.1, 2014, https://doi.org/10.1016/j.funbio.2013.11.005
  23. How the Necrotrophic Fungus Alternaria brassicicola Kills Plant Cells Remains an Enigma vol.14, pp.4, 2015, https://doi.org/10.1128/EC.00226-14
  24. plant latex is inhabited by diverse microbial communities vol.102, pp.12, 2015, https://doi.org/10.3732/ajb.1500223
  25. Abra43 vol.6, pp.6, 2018, https://doi.org/10.1128/genomeA.01559-17
  26. leaves under growth room conditions vol.67, pp.5, 2018, https://doi.org/10.1111/ppa.12828