Skip to main content

Alternaria host-selective toxins: determinant factors of plant disease

Abstract

Seven diseases caused by pathotypes of Alternaria alternata, which produced host-selective toxins (HSTs), a diverse group of low-molecular-weight secondary metabolites, are known, and each HST has an essential role as a determinant of pathogenicity in all interactions between the plant host and A. alternata. Although these HST-producing pathotypes are morphologically indistinguishable, each has a distinct host range and can be distinguished by its specificity on the respective host plant, hence their designation as pathotypes of A. alternata. In 1933, Tanaka made the first discovery of a HST; fungus-free culture filtrates of A. kikuchiana (now called A. alternata Japanese pear pathotype) were toxic to susceptible cultivar Nijisseiki, but not to resistant cultivars. Over the 80 years since then, the structure of HST molecules, target sites and mode of actions of HSTs, and the molecular genetics of HST production regulating by supernumerary chromosomes encoding HST gene clusters have been studied extensively. We focus this review on studies of low-molecular-weight HSTs produced by A. alternata and give an overview of various types of HST studies.

This is a preview of subscription content, access via your institution.

References

  1. Adachi Y, Watanabe H, Tanabe K, Doke N, Nishimura S, Tsuge T (1993) Nuclear ribosomal DNA as a probe for genetic variability in the Japanese pear pathotype of Alternaria alternata. Appl Environ Microbiol 59:3197–3205

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Ajiro N, Miyamoto Y, Masunaka A, Tsuge T, Yamamoto M, Ohtani K, Fukumoto T, Gomi K, Peever TL, Izumi Y, Tada Y, 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

    CAS  PubMed  Google Scholar 

  3. Akagi Y, Akamatsu H, Otani H, Kodama M (2009a) Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Akagi Y, Taga M, Yamamoto M, Tsuge T, Fukumasa-Nakai Y, Otani H, Kodama M (2009b) 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

    Google Scholar 

  5. Akamatsu H, Itoh Y, Kodama M, Otani H, Kohmoto K (1997) AAL-toxin-deficient mutants of Alternaria alternata tomato pathotype by restriction enzyme-mediated integration. Phytopathology 87:967–972

    CAS  PubMed  Google Scholar 

  6. Akamatsu H, Taga M, Kodama M, Johnson R, Otani H, Kohmoto K (1999) Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr Genet 35:647–656

    CAS  PubMed  Google Scholar 

  7. Akamatsu H, Otani H, 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 (Suppl.):355

    Google Scholar 

  8. Akimitsu K, Kohmoto K, Otani H, Nishimura S (1989) Host-specific effect of toxin from the rough lemon pathotype of Alternaria alternata on mitochondria. Plant Physiol 89:925–931

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Akimitsu K, Hart LP, Walton JD, Hollingsworth R (1992) Covalent binding sites of victorin in oat leaf tissues detected by anti-victorin polyclonal antibodies. Plant Physiol 98:121–126

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Akimitsu K, Peever TL, Timmer LW (2003) Molecular, ecological and evolutionary approaches to understanding Alternaria diseases of citrus. Mol Plant Pathol 4:435–446

    CAS  PubMed  Google Scholar 

  11. Andrew M, Peever TL, Pryor BM (2009) An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex. Mycologia 101:95–109

    CAS  PubMed  Google Scholar 

  12. Bezuidenhout SC, Gelderblom WCA, Gorst-Allman CP, Horak RM, Marasas WFO, Spiteller G, Vleggaar R (1988) Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J Chem Soc Chem Commun 11:743–745

    Google Scholar 

  13. Bottini AT, Gilchrist DG (1981) Phytotoxins. I. A 1-aminodimethylheptadecapentol from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22:2719–2722

    CAS  Google Scholar 

  14. Bottini AT, Bowen JR, Gilchrist DG (1981) Phytotoxins. II. Characterization of a phytotoxic fraction from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22:2723–2726

    CAS  Google Scholar 

  15. Brandwagt BF, Mesbah LA, Takken FLW, Laurent PL, Kneppers TJA, Hille J, Nijkamp HJJ (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97:4961–4966

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Braun CJ, Siedow JN, Levings CS III (1990) Fungal toxins bind to the URF13 protein in maize mitochondria and Escherichia coli. Plant Cell 2:153–161

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Covert SF (1998) Supernumerary chromosomes in filamentous fungi. Curr Genet 33:311–319

    CAS  PubMed  Google Scholar 

  18. de Zélicourt A, Montiel G, Pouvreau J-B, Thoiron S, Delgrange S, Simier P, Delavault P (2009) Susceptibility of Phelipanche and Orobanche species to AAL-toxin. Planta 230:1047–1055

    PubMed  Google Scholar 

  19. Dewey RE, Levings CS III, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the texas male-sterile cytoplasm. Cell 44:439–449

    CAS  PubMed  Google Scholar 

  20. Dewey RE, Siedow JN, Timothy DH, Levings CS III (1988) A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science 239:293–295

    CAS  PubMed  Google Scholar 

  21. Doidge EM (1929) A study of some Alternarias infecting citrus in South Africa. Union S Afr Dept Agric Sci Bull 69:1–29

    Google Scholar 

  22. Ellis MB (1971) Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew

    Google Scholar 

  23. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956

    CAS  PubMed  Google Scholar 

  24. Friesen TL, Faris JD, Solomon PS, Oliver RP (2008) Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 10:1421–1428

    CAS  PubMed  Google Scholar 

  25. Gardner JM, Kono Y, Tatum JH, Suzuki Y, Takeuchi S (1985a) Structure of major component of ACRL toxins, host-specific phytotoxic compound produced by Alternaria citri. Agri Biol Chem 49:1235–1238

    CAS  Google Scholar 

  26. Gardner JM, Kono Y, Tatum JH, Suzuki Y, Takeuchi S (1985b) Plant pathotoxins from Alternaria citri: the major toxin specific for rough lemon plants. Phytochemistry 24:2861–2867

    CAS  Google Scholar 

  27. Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197

    CAS  PubMed  Google Scholar 

  28. Gechev TS, Ferwerda MA, Mehterov N, Laloi C, Qureshi MK, Hille J (2008) Arabidopsis AAL-toxin-resistant mutant atr1 shows enhanced tolerance to programmed cell death induced by reactive oxygen species. Biochem Biophys Res Commun 375:639–644

    CAS  PubMed  Google Scholar 

  29. Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414

    CAS  PubMed  Google Scholar 

  30. Gilchrist DG, Grogan RG (1976) Production and nature of a host-specific toxin from Alternaria alternata f. sp. lycopersici. Phytopathology 66:165–171

    Google Scholar 

  31. Gilchrist DG, Bostock RM, Wang H (1995) Sphingosine-related mycotoxins in plant and animal disease. Can J Bot 73:459–467

    Google Scholar 

  32. Gomi K, Yamamoto H, Akimitsu K (2002a) Characterization of lipoxygenase gene in rough lemon induced by Alternaria alternata. J Gen Plant Pathol 68:21–30

    CAS  Google Scholar 

  33. Gomi K, Itoh N, Yamamoto H, Akimitsu K (2002b) Characterization and functional analysis of class I and II acidic chitinase cDNA from rough lemon. J Gen Plant Pathol 68:191–199

    CAS  Google Scholar 

  34. Gomi K, Yamamato H, Akimitsu K (2003a) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53:189–199

    CAS  PubMed  Google Scholar 

  35. Gomi K, Yamasaki Y, Yamamoto H, Akimitsu K (2003b) Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in Citrus. J Plant Physiol 160:1219–1231

    CAS  PubMed  Google Scholar 

  36. Gotoh Y, Nalumpang S, Isshiki A, Utsumi T, Gomi K, Yamamoto H, Akimitsu K (2002) A cDNA encoding polygalacturonase-inhibiting protein induced in citrus leaves by polygalacturonase of Alternaria citri. J Gen Plant Pathol 68:57–61

    CAS  Google Scholar 

  37. Grogan RG, Kimble KA, Misagi I (1975) A stem canker disease of tomato caused by Alternaria alternata f. sp. lycopersici. Phytopathology 65:880–886

    Google Scholar 

  38. Gross ML, McCrery D, Crow F, Tomer KB, Pope MR, Ciuffetti LM, Knoche HW, Daly JM, Dunkle LD (1982) The structure of the toxin from Helminthosporium carbonum. Tetrahedron Lett 23:5381–5384

    CAS  Google Scholar 

  39. Harimoto Y, Hatta R, Kodama M, Yamamoto M, Otani H, 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 20:1463–1476

    CAS  PubMed  Google Scholar 

  40. Harimoto Y, Tanaka T, Kodama M, Yamamoto M, Otani H, 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

    CAS  Google Scholar 

  41. Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A, Yamamoto M, Akimitsu K, Tsuge T (2002) A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59–70

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Hatta R, Shinjo A, Ruswandi S, Kitani K, Yamamoto M, Akimitsu K, Tsuge T (2006) DNA transposon fossils present on the conditionally dispensable chromosome controlling AF-toxin biosynthesis and pathogenicity of Alternaria alternata. J Gen Plant Pathol 72:210–219

    CAS  Google Scholar 

  43. Hayashi N, Tanabe K, Tsuge T, Nishimura S, Kohmoto K, Otani H (1990) Determination of host-selective toxin production during spore germination of Alternaria alternata by high-performance liquid chromatography. Phytopathology 80:1088–1091

    CAS  Google Scholar 

  44. Howlett BJ (2006) Secondary metabolite toxins and nutrition of plant pathogenic fungi. Curr Opin Plant Biol 9:371–375

    CAS  PubMed  Google Scholar 

  45. Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, 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

    CAS  PubMed  Google Scholar 

  46. Izumi Y, Kamei E, Miyamoto Y, Ohtani K, Masunaka A, Fukumoto T, Gomi K, Tada Y, Ichimura K, Peever TL, Akimitsu K (2012a) Role of 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 102:741–748

    CAS  PubMed  Google Scholar 

  47. Izumi Y, Ohtani K, Miyamoto Y, Masunaka A, Fukumoto T, Gomi K, Tada Y, Ichimura K, Peever TL, Akimitsu K (2012b) A polyketide synthase gene, ACRTS2, is responsible for biosynthesis of host-selective ACR-toxin in the rough lemon pathotype of Alternaria alternata. Mol Plant Microbe Interact 25:1419–1429

    CAS  PubMed  Google Scholar 

  48. Johal GS, Briggs SP (1992) Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258:985–987

    CAS  PubMed  Google Scholar 

  49. Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, 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

    CAS  PubMed  Google Scholar 

  50. Johnson LJ, Johnson RD, Akamatsu H, Salamiah A, Otani H, Kohmoto K, Kodama M (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

    CAS  PubMed  Google Scholar 

  51. Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Kim BG, Fukumoto T, Tatano S, Gomi K, Ohtani K, Tada Y, Akimitsu K (2009) Molecular cloning and characterization of a thaumatin-like protein-encoding cDNA from rough lemon. Physiol Mol Plant Pathol 74:3–10

    CAS  Google Scholar 

  53. Kodama M, Suzuki T, Otani H, Kohmoto K, Nishimura S (1990) Purification and bioassay of host-selective AT-toxin from Alternaria alternata causing brown spot of tobacco. Ann Phytopath Soc Japan 56:628–636

    CAS  Google Scholar 

  54. Kohmoto K, Otani H (1991) Host recognition by toxigenic plant pathogens. Experientia 47:755–764

    CAS  PubMed  Google Scholar 

  55. Kohmoto K, Scheffer RP, Whiteside JO (1979) Host-selective toxins from Alternaria citri. Phytopathology 69:667–671

    CAS  Google Scholar 

  56. Kohmoto K, Otani H, Nishimura S (1982) Action sites of AM-toxins produced by the apple pathotype of Alternaria alternata. In: Asada Y, Bushnell WR, Ouchi S, Vance CP (eds) Plant infection: the physiological and biochemical basis. Springer, Berlin, pp 81–136

    Google Scholar 

  57. Kohmoto K, Kondoh Y, Kohguchi T, Otani H, Nishimura S, Scheffer RP (1984) Ultrastructural changes in host leaf cells caused by host-selective toxin of Alternaria alternata from rough lemon. Can J Bot 62:2485–2492

    CAS  Google Scholar 

  58. Kohmoto K, Akimitsu K, Otani H (1991) Correlation of resistance and susceptibility of citrus to Alternaria alternata with sensitivity to host-specific toxins. Phytopathology 81:719–722

    Google Scholar 

  59. Kohmoto K, Itoh Y, Shimomura N, Kondoh Y, Otani H, Kodama M, Nishimura S, Nakatsuka S (1993) Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495–502

    CAS  Google Scholar 

  60. Kono Y, Daly JM (1979) Characterization of the host-specific pathotoxin produced by Helminthosporium maydis race T, affecting corn with Texas male sterile cytoplasm. Bioorg Chem 8:391–397

    CAS  Google Scholar 

  61. Kono Y, Gardner JM, Suzuki Y, Takeuchi S (1985) Plant pathotoxins from Alternaria citri: the minor ACRL toxins. Phytochemistry 24:2869–2874

    CAS  Google Scholar 

  62. Kozaki I (1973) Black spot disease resistance in Japanese pear, I: Heredity of the disease resistance (in Japanese with English summary). Bull Hort Res Sta Jpn 12:17–27

    Google Scholar 

  63. Kusaba M, Tsuge T (1994) Nuclear ribosomal DNA variation and pathogenic specialization in Alternaria fungi known to produce host-specific toxins. Appl Environ Microbol 60:3055–3062

    CAS  Google Scholar 

  64. Kusaba M, 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

    CAS  PubMed  Google Scholar 

  65. Lorang JM, Sweat TA, Wolpert TJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci USA 104:14861–14866

    CAS  PubMed Central  PubMed  Google Scholar 

  66. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, Tzeng SC, Maier CS, Wolpert TJ (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–662

    CAS  PubMed  Google Scholar 

  67. Lucas GB (1975) Disease of tobacco, 3rd edn. Biological Consulting Associates, Raleigh

    Google Scholar 

  68. Maekawa N, Yamamoto M, Nishimura S, Kohmoto K, Kuwada M, Watanabe Y (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 activities. Ann Phytopath Soc Japan 50:600–609

    CAS  Google Scholar 

  69. Markham JE, Hille J (2001) Host-selective toxins as agents of cell death in plant–fungus interactions. Mol Plant Pathol 2:229–239

    CAS  PubMed  Google Scholar 

  70. Masunaka A, Tanaka A, Tsuge T, Peever TL, Timmer LW, Yamamoto M, Yamamoto H, Akimitsu K (2000) Distribution and characterization of AKT homologs in the tangerine pathotype of Alternaria alternata. Phytopathology 90:762–768

    CAS  PubMed  Google Scholar 

  71. Masunaka A, Ohtani K, Peever TL, Timmer LW, Tsuge T, Yamamoto M, Yamamoto H, Akimitsu K (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

    CAS  PubMed  Google Scholar 

  72. Meeley RB, Johal GS, Briggs SP, Walton JD (1992) A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4:71–77

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Miyamoto Y, Masunaka A, Tsuge T, Yamamoto M, Ohtani K, Fukumoto T, Gomi K, Peever TL, 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

    CAS  PubMed  Google Scholar 

  74. Miyamoto Y, Ishii Y, Honda A, Masunaka A, Tsuge T, Yamamoto M, Ohtani K, Fukumoto T, Gomi K, Peever TL, 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

    CAS  PubMed  Google Scholar 

  75. Miyamoto Y, Masunaka A, Tsuge T, Yamamoto M, Ohtani K, Fukumoto T, Gomi K, Peever TL, Tada Y, Ichimura K, 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 Interac 23:406–414

    CAS  Google Scholar 

  76. Mullen TD, Jenkins RW, Clarke CJ, Bielawski J, Hannun YA, Obeid LM (2011) Ceramide synthase-dependent ceramide generation and programmed cell death: involvement of salvage pathway in regulating postmitochondrial events. J Biol Chem 286:15929–15942

    CAS  PubMed Central  PubMed  Google Scholar 

  77. 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

    CAS  Google Scholar 

  78. Nakatsuka S, Goto T, Kohmoto K, Nishimura S (1986a) Host-specific phytotoxins. In: Imura H, Goto T, Murachi T, Nakajima T (eds) Natural products and biological activities. University of Tokyo Press, Tokyo, pp 11–18

    Google Scholar 

  79. Nakatsuka S, Ueda K, Goto T, Yamamoto M, Nishimura S, Kohmoto K (1986b) Structure of AF-toxin II, one of the host-specific toxins produced by Alternaria alternata strawberry pathotype. Tetrahedron Lett 27:2753–2756

    CAS  Google Scholar 

  80. Nalumpang S, Gotoh Y, Tsuboi H, Gomi K, Yamamoto H, Akimitsu K (2002a) Functional characterization of citrus polygalacturonase-inhibiting protein. J Gen Plant Pathol 68:118–127

    CAS  Google Scholar 

  81. Nalumpang S, Gotoh Y, Yamasaki Y, Gomi K, Yamamoto H, Akimitsu K (2002b) Comparison and characterization of polygalacturonase-inhibiting protein genes from the genus of Citrus and its close related genera. Thai J Agr Sci 35:147–164

    CAS  Google Scholar 

  82. Namiki F, Okamoto H, Katou K, Yamamoto M, Nishimura S, Nakatsuka S, Goto T, Kohmoto K, Otani H, Novacky A (1986) Studies on host-specific AF-toxins produced by Alternaria alternata strawberry pathotype causing Alternaria black spot of strawberry (5) Effect of toxins on membrane potential of susceptible plants as assessed by electrophysiological method. Ann Phytopath Soc Japan 52:610–619

    Google Scholar 

  83. Neergaard P (1945) Danish species of Alternaria and Stemphylium. Ejnar Munksgaard, Copenhagen

    Google Scholar 

  84. Nishimura S (1980) Host-specific toxins from Alternaria alternata: problems and prospects. Proc Jpn Acad (Ser B) 56:362–366

    Google Scholar 

  85. Nishimura S, Kohmoto K (1983) Host-specific toxins and chemical structures from Alternaria species. Annu Rev Phytopathol 21:87–116

    CAS  Google Scholar 

  86. Nishimura S, Nakatsuka S (1989) Trends in host-selective toxin research in Japan. In: Kohmoto K, Durbin RD (eds) Host-specific toxins: recognition and specificity factors in plant disease. Tottori University Press, Tottori, pp 19–31

    Google Scholar 

  87. Nishimura S, Scheffer RP (1965) Interactions between Helminthosporium victoriae spores and oat tissue. Phytopathology 55:629–634

    Google Scholar 

  88. Nishimura S, Sugihara M, Kohmoto K, Otani H (1978) Two different phases in pathogenicity of the Alternaria pathogen causing black spot disease of Japanese pear. J Fac Agric Tottori Univ 13:1–10

    Google Scholar 

  89. Nishimura S, Tatano S, Gomi K, Ohtani K, Fukumoto T, Akimitsu K (2008) Chloroplast-localized nonspecific lipid transfer protein with anti-fungal activity from rough lemon. Physiol Mol Plant Pathol 72:134–140

    CAS  Google Scholar 

  90. Nutsugah SK, Park P, Otani H, Kodama M, Kohmoto K (1993) Ultrastructural changes in pigeon pea cells caused by a host-specific toxin from Alternaria tenuissima. Ann Phytopath Soc Japan 59:407–415

    Google Scholar 

  91. Ohtani K, Yamamoto H, Akimitsu K (2002) Sensitivity to Alternaria alternata toxin in citrus because of altered mitochondrial RNA processing. Proc Natl Acad Sci USA 99:2439–2444

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Okuno T, Ishita Y, Sawai K, Matsumoto T (1974) Characterization of alternariolide, a host-specific toxin produced by Alternaria mali Roberts. Chem Lett 3:635–638

    Google Scholar 

  93. Otani H, Nishimura S, Kohmoto K, Yano K, Seno T (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 Phytopath Soc Japan 41:467–476

    Google Scholar 

  94. Otani H, Kohmoto K, Nishimura S, Nakashima T, Ueno T, Fukami H (1985) Biological activities of AK-toxins I and II, host-specific toxins from Alternaria alternata Japanese pear pathotype. Ann Phytopath Soc Japan 51:285–293

    CAS  Google Scholar 

  95. Otani H, Tomiyama K, Okamoto H, Nishimura S, Kohmoto K (1989) Effect of AK-toxin produced by Alternaria alternata Japanese pear pathotype on membrane potential of pear cells. Ann Phytopath Soc Japan 55:466–468

    Google Scholar 

  96. Otani H, Kohmoto K, Kodama M, Nishimura S (1991) Role of host-specific toxins in the pathogenesis of Alternaria alternata. In: Patil SS, Ouchi S, Mills D, Vance C (eds) Molecular strategies of pathogens and host plants. Springer, New York, pp 139–149

    Google Scholar 

  97. Otani H, Kohmoto K, Kodama M (1995) Alternaria toxins and their effects on host plants. Can J Bot 73:453–458

    Google Scholar 

  98. Otani H, Kohnobe A, Kodama M, Kohmoto K (1998) Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiol Mol Plant Pathol 52:285–295

    CAS  Google Scholar 

  99. Parada RY, Sakuno E, Mori N, Oka K, Egusa M, Kodama M, Otani H (2008) Alternaria brassicae produces a host-specific protein toxin from germinating spores on host leaves. Phytopathology 98:458–463

    CAS  PubMed  Google Scholar 

  100. Park P, Ikeda K (2008) Ultrastructural analysis of responses of host and fungal cells during plant infection. J Gen Plant Pathol 74:2–14

    Google Scholar 

  101. Park P, Nishimura S, Kohmoto K, Otani H, Tsujimoto K (1981) Two action sites of AM-toxin I produced by apple pathotype of Alternaria alternata in host cells: an ultrastructural study. Can J Bot 59:301–310

    Google Scholar 

  102. Peever TL, Su G, Carpenter-Boggs L, Timmer LW (2004) Molecular systematics of citrus-associated Alternaria species. Mycologia 96:119–134

    CAS  PubMed  Google Scholar 

  103. Pegg KG (1966) Studies of a strain of Alternaria citri Pierce, the causal organism of brown spot of emperor mandarin (Citrus reticulata). Queensl J Agric Anim Sci 23:15–28

    Google Scholar 

  104. Pringle RB, Scheffer RP (1964) Host-specific plant toxins. Annu Rev Phytopathol 2:133–156

    CAS  Google Scholar 

  105. Proctor RH, Desjardins AE, Plattner RD, Hohn TM (1999) A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol 27:100–112

    CAS  PubMed  Google Scholar 

  106. Proctor RH, Brown DW, Plattner RD, Desjardins AE (2003) Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol 38:237–249

    CAS  PubMed  Google Scholar 

  107. Pryor BM, Bigelow DM (2003) Molecular characterization of Embellisia and Nimbya species and their relationship to Alternaria, Ulocladium and Stemphylium. Mycologia 95:1141–1154

    CAS  PubMed  Google Scholar 

  108. Pryor BM, Gilbertson RL (2000) Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycol Res 104:1312–1321

    CAS  Google Scholar 

  109. Richael C, Gilchrist D (1999) The hypersensitive response: a case of hold or fold? Physiol Mol Plant Pathol 55:5–12

    CAS  Google Scholar 

  110. Rotem J (1994) The genus Alternaria: biology, epidemiology, and pathogenicity. APS Press, St. Paul

    Google Scholar 

  111. Ruswandi S, Kitani K, Akimitsu K, Tsuge T, Shiraishi T, Yamamoto M (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

    CAS  Google Scholar 

  112. Saito K, Takeda K (1984) Genetic analysis of resistance to Alternaria blotch (Alternaria mali Roberts) in apple. (Studies on the breeding of the apple VIII). Japan J Breed 34:197–209

    Google Scholar 

  113. Salamiah Akamatsu H, Fukumasa-Nakai Y, Otani H, Kodama M (2001) Construction and genetic analysis of hybrid strains between apple and tomato pathotypes of Alternaria alternata by protoplast fusion. J Gen Plant Pathol 67:97–105

    CAS  Google Scholar 

  114. Sanada T (1988) Selection of resistant mutants to black spot disease of Japanese pear by using host-specific toxin. Japan J Breed 38:198–204

    Google Scholar 

  115. Sawamura K (1962) Studies on spotted disease of apples. I. Causal agent of Alternaria blotch. Bull Tohoku Natl Agric Exp Stn 23:163–175

    Google Scholar 

  116. Scheffer RP, Livingston RS (1984) Host-selective toxins and their role in plant diseases. Science 223:17–21

    CAS  PubMed  Google Scholar 

  117. Seo JA, Proctor RH, Plattner RD (2001) Characterization of four clustered and coregulated genes associated with fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet Biol 34:155–165

    CAS  PubMed  Google Scholar 

  118. Shishido H, Miyamoto Y, Ozawa R, Taniguchi S, Takabayashi J, Akimitsu K, Gomi K (2012) Geraniol synthase whose mRNA is induced by host-selective ACT-toxin in the ACT-toxin-insensitive rough lemon (Citrus jambhiri). J Plant Physiol 169:1401–1407

    CAS  PubMed  Google Scholar 

  119. Simmons EG, Roberts RG (1993) Alternaria themes and variations (73). Mycotaxon 48:109–140

    Google Scholar 

  120. Spassieva SD, Markham JE, Hille J (2002) The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32:561–572

    CAS  PubMed  Google Scholar 

  121. Spassieva S, Seo JG, Jiang JC, Bielawski J, Alvarez-Vasquez F, Jazwinski SM, Hannun YA, Obeid LM (2006) Necessary role for the Lag1p motif in (dihydro) ceramide synthase activity. J Biol Chem 281:33931–33938

    CAS  PubMed  Google Scholar 

  122. Tabira H, Otani H, Shimomura N, Kodama M, Kohmoto K, Nishimura S (1989) Light-induced insensitivity of apple and Japanese pear leaves to AM-toxin from Alternaria alternata apple pathotype. Ann Phytopath Soc Japan 55:567–578

    CAS  Google Scholar 

  123. Tabira H, Shimonaka M, Kohmoto K, Otani H, Banno K (1998) Selection of a resistant mutant to Alternaria blotch in apple and analysis of proteins associated with the susceptibility by 2-D gel electrophoresis. In: Kohmoto K, Yoder OC (eds) Molecular genetics of host-specific toxins in plant disease. Kluwer, Dordrecht, pp 387–397

    Google Scholar 

  124. Tanaka S (1933) Studies on black spot disease of the Japanese pear (Pyrus serotina Rehd.). Mem Coll Agric Kyoto Imp Univ 28:1–31

    Google Scholar 

  125. 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

    CAS  PubMed  Google Scholar 

  126. Tanaka A, Shiotani H, Yamamoto M, 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

    CAS  PubMed  Google Scholar 

  127. Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236

    CAS  PubMed  Google Scholar 

  128. Tsukuda S, Gomi K, Yamamoto H, Akimitsu K (2006) Characterization of cDNA encoding two distinct miraculin-like proteins and stress-related modulation of the corresponding mRNAs in Citrus jambhiri Lush. Plant Mol Biol 60:125–136

    CAS  PubMed  Google Scholar 

  129. Ueno T, Nakashima T, Hayashi Y, Fukami H (1975) Structures of AM-toxin I and II, host specific phytotoxic metabolites produced by Alternaria mali. Agric Biol Chem 39:1115–1122

    CAS  Google Scholar 

  130. Ueno T, Nakashima T, Uemoto M, Fukami H, Lee SN, Izumiya N (1977) Mass spectrometry of Alternaria mali toxins and related cyclodepsipeptides. Biol Mass Spectrom 4:134–142

    CAS  Google Scholar 

  131. Walton JD (1996) Host-selective toxins: agents of compatibility. Plant Cell 8:1723–1733

    CAS  PubMed Central  PubMed  Google Scholar 

  132. Walton JD, Earle ED, Gibson BW (1982) Purification and structure of the host-specific toxin from Helminthosporium carbonum race 1. Biochem Biophys Res Commun 107:785–794

    CAS  PubMed  Google Scholar 

  133. Wang H, Li J, Bostock RM, Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8:375–391

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Wolpert TJ, Macko V (1989) Specific binding of victorin to a 100-kDa protein from oats. Proc Natl Acad Sci USA 86:4092–4096

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285

    CAS  PubMed  Google Scholar 

  136. Yamagishi D, Akamatsu H, Otani H, Kodama M (2006) Pathological evaluation of host-specific AAL-toxins and fumonisin mycotoxins produced by Alternaria and Fusarium species. J Gen Plant Pathol 72:323–327

    CAS  Google Scholar 

  137. Yamamoto M, Nishimura S, Kohmoto K, Otani H (1984) Studies on host-specific AF-toxins produced by Alternaria alternata strawberry pathotype causing Alternaria black spot of strawberry (2) Role of toxins in pathogenesis. Ann Phytopath Soc Japan 50:610–619

    CAS  Google Scholar 

  138. Yamamoto M, Namiki F, Nishimura S, Kohmoto K (1985) Studies on host-specific AF-toxins produced by Alternaria alternata strawberry pathotype causing Alternaria black spot of strawberry (3) Use of toxin for determining inheritance of disease reaction in strawberry cultivar Morioka-16. Ann Phytopath Soc Japan 51:530–535

    Google Scholar 

  139. Yoder OC (1980) Toxins in pathogenesis. Annu Rev Phytopathol 18:103–129

    CAS  Google Scholar 

  140. Yoder OC, Scheffer RP (1969) Role of toxin in early interactions of Helminthosporium victoriae with susceptible and resistant oat tissues. Phytopathology 59:1954–1959

    Google Scholar 

Download references

Acknowledgments

The authors are deeply indebted to the late Dr. S. Nishimura and Dr. K. Kohmoto for their vision and efforts on Alternaria HST studies. This work was supported by Grants-in-Aids for Scientific Research (S) (21228001 to KA), Scientific Research (A) (23248007 to TT) and Scientific Research (B) (20380028 and 23380025 to MK) from the Japanese Society for Promotion of Sciences and Special Coordination Funds for Promoting Sciences from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kazuya Akimitsu.

About this article

Cite this article

Akimitsu, K., Tsuge, T., Kodama, M. et al. Alternaria host-selective toxins: determinant factors of plant disease. J Gen Plant Pathol 80, 109–122 (2014). https://doi.org/10.1007/s10327-013-0498-7

Download citation

Keywords

  • Host selectivity
  • Pathogenicity
  • Virulence
  • Conditionally dispensable chromosome
  • Effector
  • Secondary metabolite