Recent advances in genetic and molecular technologies gradually paved the way for the transition from traditional fungal karyotyping to more comprehensive chromosome biology studies. Extensive chromosomal polymorphisms largely resulting from chromosomal rearrangements (CRs) are widely documented in fungal genomes. These extraordinary CRs in fungi generate substantial genome plasticity compared to other eukaryotic organisms. Here, we review the most recent findings on fungal CRs and their underlying mechanisms and discuss the functional consequences of CRs for adaptation, fungal evolution, host range, and pathogenicity of fungal plant pathogens in the context of chromosome biology. In addition to a complement of permanent chromosomes called core chromosomes, the genomes of many fungal pathogens comprise distinct unstable chromosomes called dispensable chromosomes (DCs) that also contribute to chromosome polymorphisms. Compared to the core chromosomes, the structural features of DCs usually differ for gene density, GC content, housekeeping genes, and recombination frequency. Despite their dispensability for normal growth and development, DCs have important biological roles with respect to pathogenicity in some fungi but not in others. Therefore, their evolutionary origin is also reviewed in relation to overall fungal physiology and pathogenicity.

[Erratum, Closure]

An erratum has been published for this article:
Karyotype Variability in Plant-Pathogenic Fungi

Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Ahn J-H, Walton JD. 1.  1996. Chromosomal organization of TOX2, a complex locus controlling host-selective toxin biosynthesis in Cochliobolus carbonum. . Plant Cell 8:887–97 [Google Scholar]
  2. Akagi Y, Akamatsu H, Otani H, Kodama M. 2.  2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot. Cell 8:111732–38 [Google Scholar]
  3. Akagi Y, Taga M, Yamamoto M, Tsuge T, Fukumasa-Nakai Y. 3.  et al. 2009. Chromosome constitution of hybrid strains constructed by protoplast fusion between the tomato and strawberry pathotypes of Alternaria alternata. J. Gen. Plant Pathol. 75:101–9 [Google Scholar]
  4. Akamatsu H, Taga M, Kodama M, Johnson R, Otani H, Kohmoto K. 4.  1999. Molecular karyotypes for Alternaria plant pathogens known to produce host-specific toxins. Curr. Genet. 35:647–56 [Google Scholar]
  5. Andersen SL, Sekelsky J. 5.  2010. Meiotic versus mitotic recombination: two different routes for double‐strand break repair. Bioessays 32:1058–66 [Google Scholar]
  6. Austin B, Trivers R, Burt A. 6.  2009. Genes in Conflict: The Biology of Selfish Genetic Elements Cambridge, MA: Harvard Univ. Press [Google Scholar]
  7. Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J. 7.  et al. 2013. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. . New Phytol. 198:887–98 [Google Scholar]
  8. Beadle J, Wright M, McNeely L, Bennett J. 8.  2003. Electrophoretic karyotype analysis in fungi. Adv. Appl. Microbiol. 53:243–70 [Google Scholar]
  9. Chen W, Wellings C, Chen X, Kang Z, Liu T. 9.  2014. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. . Mol. Plant Pathol. 15:433–46 [Google Scholar]
  10. Coleman JJ. 10.  2016. The Fusarium solani species complex: ubiquitous pathogens of agricultural importance. Mol. Plant Pathol. 17:146–58 [Google Scholar]
  11. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC. 11.  et al. 2009. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLOS Genet 5:e1000618 [Google Scholar]
  12. Condon BJ, Leng Y, Wu D, Bushley KE, Ohm RA. 12.  et al. 2013. Comparative genome structure, secondary metabolite, and effector coding capacity across Cochliobolus pathogens. PLOS Genet 9:e1003233 [Google Scholar]
  13. Counter CM. 13.  1996. The roles of telomeres and telomerase in cell life span. Mutat. Res. 366:45–63 [Google Scholar]
  14. Covert SF. 14.  1998. Supernumerary chromosomes in filamentous fungi. Curr. Genet. 33:311–19 [Google Scholar]
  15. Croll D, Lendenmann MH, Stewart E, McDonald BA. 15.  2015. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201:1213–28 [Google Scholar]
  16. Croll D, Zala M, McDonald BA. 16.  2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLOS Genet 9:e1003567 [Google Scholar]
  17. da Silva Franco CC, de Sant'Anna JR, Rosada LJ, Kaneshima EN, Stangarlin JR, De Castro-Prado MAA. 17.  2011. Vegetative compatibility groups and parasexual segregation in Colletotrichum acutatum isolates infecting different hosts. Phytopathology 101:923–28 [Google Scholar]
  18. Declercq B, Van Buyten E, Claeys S, Cap N, De Nies J. 18.  et al. 2010. Molecular characterization of Phytophthora porri and closely related species and their pathogenicity on leek (Allium porrum). Eur. J. Plant Pathol 127:341–50 [Google Scholar]
  19. Delserone LM, McCluskey K, Matthews D, VanEtten H. 19.  1999. Pisatin demethylation by fungal pathogens and nonpathogens of pea: association with pisatin tolerance and virulence. Physiol. Mol. Plant Pathol. 55:6317–26 [Google Scholar]
  20. Depotter JRL, Seidl MF, Wood TA, Thomma BPHJ. 20.  2016. Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Curr. Opin. Microbiol. 32:7–13 [Google Scholar]
  21. de Visser JAG, Elena SF. 21.  2007. The evolution of sex: empirical insights into the roles of epistasis and drift. Nat. Rev. Genet. 8:139–49 [Google Scholar]
  22. De Wit PJ, Van Der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA. 22.  et al. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLOS Genet 8:e1003088 [Google Scholar]
  23. Dhillon B, Gill N, Hamelin RC, Goodwin SB. 23.  2014. The landscape of transposable elements in the finished genome of the fungal wheat pathogen Mycosphaerella graminicola. . BMC Genom. 15:1132 [Google Scholar]
  24. Farman ML, Leong SA. 24.  1995. Genetic and physical mapping of telomeres in the rice blast fungus. Magnaporthe grisea. Genetics 140:479–92 [Google Scholar]
  25. Fierro F, Martín JF. 25.  1999. Molecular mechanisms of chromosomal rearrangement in fungi. Crit. Rev. Microbiol. 25:1–17 [Google Scholar]
  26. Fitt BD, Brun H, Barbetti M, Rimmer S. 26.  2006. World-wide importance of phoma stem canker (Leptosphaeriamaculans and L. biglobosa) on oilseed rape (Brassica napus). Sustainable Strategies for Managing Brassica napus (oilseed rape) Resistance to Leptosphaeria maculans (phoma stem canker) BDL Fitt, N Evans, BJ Howlett, BM Cooke 3–15 Dordrecht, Neth.: Springer [Google Scholar]
  27. Flot J-F, Hespeels B, Li X, Noel B, Arkhipova I. 27.  et al. 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. . Nature 500:453–57 [Google Scholar]
  28. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, Bennett RJ. 28.  2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLOS Biol 6:e110 [Google Scholar]
  29. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H. 29.  et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:953–56 [Google Scholar]
  30. Galazka JM, Freitag M. 30.  2014. Variability of chromosome structure in pathogenic fungi: of “ends and odds.”. Curr. Opin. Microbiol. 20:19–26 [Google Scholar]
  31. Gardiner DM, McDonald MC, Covarelli L, Solomon PS, Rusu AG. 31.  et al. 2012. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLOS Pathog 8:e1002952 [Google Scholar]
  32. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD. 32.  2000. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. . PNAS 97:11383–90 [Google Scholar]
  33. Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME. 33.  2008. Speciation in fungi. Fungal Genet. Biol. 45:791–802 [Google Scholar]
  34. Glass NL, Jacobson DJ, Shiu PK. 34.  2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu. Rev. Genet. 34:165–86 [Google Scholar]
  35. Goodwin SB, M'Barek SB, Dhillon B, Wittenberg AHJ, Crane CF. 35.  et al. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLOS Genet 7:6e1002070 [Google Scholar]
  36. Goss EM, Cardenas ME, Myers K, Forbes GA, Fry WE. 36.  et al. 2011. The plant pathogen Phytophthora andina emerged via hybridization of an unknown Phytophthora species and the Irish potato famine pathogen, P. infestans. . PLOS ONE 6:e24543 [Google Scholar]
  37. Grandaubert J, Bhattacharyya A, Stukenbrock EH. 37.  2015. RNA-seq-based gene annotation and comparative genomics of four fungal grass pathogens in the genus Zymoseptoria identify novel orphan genes and species-specific invasions of transposable elements. G3 (Bethesda) 5:71323–33 [Google Scholar]
  38. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE. 38.  et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. . Nature 461:393–98 [Google Scholar]
  39. Han Y, Liu X, Benny U, Kistler HC, VanEtten HD. 39.  2001. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. . Plant J. Cell Mol. Biol. 25:3305–14 [Google Scholar]
  40. Harimoto Y, Hatta R, Kodama M, Yamamoto M, Otani H, Tsuge T. 40.  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. 20:1463–76 [Google Scholar]
  41. Harimoto Y, Tanaka T, Kodama M, Yamamoto M, Otani H, Tsuge T. 41.  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. 74:3222–29 [Google Scholar]
  42. He C, Rusu AG, Poplawski AM, Irwin JA, Manners JM. 42.  1998. Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. . Genetics 150:1459–66 [Google Scholar]
  43. Hedges D, Deininger P. 43.  2007. Inviting instability: transposable elements, double-strand breaks, and the maintenance of genome integrity. Mutat. Res. 616:46–59 [Google Scholar]
  44. Heitman J, Kronstad JW, Taylor J, Casselton L. 44.  2007. Sex in Fungi: Molecular Determination and Evolutionary Implications Washington, DC: ASM Press [Google Scholar]
  45. Hirschi K, VanEtten H. 45.  1996. Expression of the pisatin detoxifying genes (PDA) of Nectria haematococca in vitro and in planta. Mol. Plant-Microbe Interact. 9:483–91 [Google Scholar]
  46. Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T. 46.  2012. Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genom 13:171 [Google Scholar]
  47. Hurtado-Gonzales O, Aragon-Caballero L, Flores-Torres J, Man W, Lamour K. 47.  2009. Molecular comparison of natural hybrids of Phytophthora nicotianae and P. cactorum infecting loquat trees in Peru and Taiwan. Mycologia 101:496–502 [Google Scholar]
  48. Isaza REA, Diaz-Trujillo C, Dhillon B, Aerts A, Carlier J. 48.  et al. 2016. Combating a global threat to a clonal crop: banana black Sigatoka pathogen Pseudocercospora fijiensis (synonym Mycosphaerella fijiensis) genomes reveal clues for disease control. PLOS Genet 12:e1005876 [Google Scholar]
  49. Johnson LJ, Johnson RD, Akamatsu H, Salamiah A, Otani H. 49.  et al. 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 [Google Scholar]
  50. Jones RN. 50.  1995. Tansley review no. 85. B chromosomes in plants. New Phytol 131:411–34 [Google Scholar]
  51. Jones RN, Viegas W, Houben A. 51.  2008. A century of B chromosomes in plants: so what?. Ann. Bot. 101:767–75 [Google Scholar]
  52. Kallioniemi A, Kallioniemi OP, Sudar D, Rutovitz D, Gray JW. 52.  et al. 1992. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258:818–21 [Google Scholar]
  53. Kellner R, Bhattacharyya A, Poppe S, Hsu TY, Brem RB, Stukenbrock EH. 53.  2014. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol. Evol. 6:1353–65 [Google Scholar]
  54. Klein HL. 54.  1995. Genetic control of intrachromosomal recombination. Bioessays 17:147–59 [Google Scholar]
  55. Kodama M, Rose M, Yang G, Yun S, Yoder O, Turgeon B. 55.  1999. The translocation-associated Tox1 locus of Cochliobolus heterostrophus is two genetic elements on two different chromosomes. Genetics 151:585–96 [Google Scholar]
  56. Kohn LM. 56.  2005. Mechanisms of fungal speciation. Annu. Rev. Phytopathol. 43:279–308 [Google Scholar]
  57. Langer-Safer PR, Levine M, Ward DC. 57.  1982. Immunological method for mapping genes on Drosophila polytene chromosomes. PNAS 79:4381–85 [Google Scholar]
  58. Lemmens BB, Tijsterman M. 58.  2011. DNA double-strand break repair in Caenorhabditis elegans. . Chromosoma 120:1–21 [Google Scholar]
  59. Lieber MR. 59.  2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end joining pathway. Annu. Rev. Biochem. 79:181–211 [Google Scholar]
  60. Liu X, Inlow M, VanEtten HD. 60.  2003. Expression profiles of pea pathogenicity (PEP) genes in vivo and in vitro, characterization of the flanking regions of the PEP cluster and evidence that the PEP cluster region resulted from horizontal gene transfer in the fungal pathogen Nectria haematococca. Curr. Genet. 44:295–103 [Google Scholar]
  61. Ma LJ, Does HC, Borkovich KA, Coleman JJ, Daboussi MJ. 61.  et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–73 [Google Scholar]
  62. Masel AM, Struijk N, McIntyre CL, Irwin JAG, Manners JM. 62.  1993. A strain-specific cyclin homolog in the fungal phytopathogen Colletotrichum gloeosporioides. . Gene 133:141–45 [Google Scholar]
  63. Masunaka A, Ohtani K, Peever TL, Timmer LW, Tsuge T. 63.  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 95:3241–47 [Google Scholar]
  64. Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, M'Barek SB. 64.  et al. 2011. Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol. Rev. 35:542–54 [Google Scholar]
  65. Mehrabi R, Taga M, Kema GH. 65.  2007. Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range. Mycologia 99:868–76 [Google Scholar]
  66. Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S. 66.  et al. 2016. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat. Genet. 48:201–5 [Google Scholar]
  67. Meurant G. 67.  2012. More Gene Manipulations in Fungi Cambridge, MA: Academic [Google Scholar]
  68. Miao VP, Covert SF, VanEtten HD. 68.  1991. A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254:1773–76 [Google Scholar]
  69. Milani NA, Lawrence DP, Arnold AE, VanEtten HD. 69.  2012. Origin of pisatin demethylase (PDA) in the genus Fusarium. . Fungal Genet. Biol. 49:11933–42 [Google Scholar]
  70. Milgroom MG, Sotirovski K, Risteski M, Brewer MT. 70.  2009. Heterokaryons and parasexual recombinants of Cryphonectria parasitica in two clonal populations in southeastern Europe. Fungal Genet. Biol. 46:849–54 [Google Scholar]
  71. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA. 71.  et al. 2012. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLOS Pathog 8:e1003037 [Google Scholar]
  72. Orbach MJ, Chumley FG, Valent B. 72.  1996. Electrophoretic karyotypes of Magnaporthe grisea pathogens of diverse grasses. Mol. Plant-Microbe Interact. 9:261–71 [Google Scholar]
  73. Perkins DD. 73.  1997. Chromosome rearrangements in Neurospora and other filamentous fungi. Adv. Genet. 36:239–40 [Google Scholar]
  74. Plissonneau C, Stürchler A, Croll D. 74.  2016. The evolution of orphan regions in genomes of a fungal pathogen of wheat. mBio 7:e01231–16 [Google Scholar]
  75. Pontecorvo G, Roper J, Forbes E. 75.  1953. Genetic recombination without sexual reproduction in Aspergillus niger. . Microbiology 8:198–210 [Google Scholar]
  76. Randolph LF. 76.  1928. Types of supernumerary chromosomes in maize. Anat. Rec. 41:102 [Google Scholar]
  77. Rosada LJ, Franco C, Sant'Anna JR, Kaneshima EN, Gonçalves‐Vidigal MC, Castro‐Prado MA. 77.  2010. Parasexuality in Race 65 Colletotrichum lindemuthianum isolates. J. Eukaryot. Microbiol. 57:383–84 [Google Scholar]
  78. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP. 78.  et al. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2:202 [Google Scholar]
  79. Salamiah H, Yukitaka F, Hiroshi O, Motoichiro K. 79.  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 [Google Scholar]
  80. Schardl C, Craven K. 80.  2003. Interspecific hybridization in plant‐associated fungi and oomycetes: a review. Mol. Ecol. 12:2861–73 [Google Scholar]
  81. Schmidt SM, Houterman PM, Schreiver I, Ma L, Amyotte S. 81.  et al. 2013. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. . BMC Genom. 14:119 [Google Scholar]
  82. Schotanus K, Soyer JL, Connolly LR, Grandaubert J, Happel P. 82.  et al. 2015. Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenet. Chromatin 8:41 [Google Scholar]
  83. Schoustra SE, Debets AJ, Slakhorst M, Hoekstra RF. 83.  2007. Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLOS Genet 3:e68 [Google Scholar]
  84. Schwartz DC, Cantor CR. 84.  1984. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 37:67–75 [Google Scholar]
  85. Seervai RN, Jones SK, Hirakawa MP, Porman AM, Bennett RJ. 85.  2013. Parasexuality and ploidy change in Candida tropicalis. . Eukaryot. Cell 12:1629–40 [Google Scholar]
  86. Seidl MF, Thomma BPHJ. 86.  2014. Sex or no sex: Evolutionary adaptation occurs regardless. Bioessays 36:335–45 [Google Scholar]
  87. Sherwood RK, Bennett RJ. 87.  2009. Fungal meiosis and parasexual reproduction: lessons from pathogenic yeast. Curr. Opin. Microbiol. 12:599–607 [Google Scholar]
  88. Singh US, Singh RP. 88.  1995. Molecular Methods in Plant Pathology Boca Raton, FL: CRC Press [Google Scholar]
  89. Solinas-Toldo S, Lampel S, Stilgenbauer S, Nickolenko J, Benner A. 89.  et al. 1997. Matrix-based comparative genomic hybridization: biochips to screen for genomic imbalances. Genes Chromosom. Cancer 20:399–407 [Google Scholar]
  90. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE. 90.  et al. 2017. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. . Mol. Plant Pathol. https://doi.org/10.1111/mpp.12515 [Crossref] [Google Scholar]
  91. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA. 91.  2007. Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol. Biol. Evol. 24:398–411 [Google Scholar]
  92. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 92.  2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. PNAS 109:10954–59 [Google Scholar]
  93. Sturtevant A. 93.  1921. Genetic studies on Drosophila simulans. III. Autosomal genes. General discussion. Genetics 6:179–207 [Google Scholar]
  94. Taga M, Murata M. 94.  1994. Visualization of mitotic chromosomes in filamentous fungi by fluorescence staining and fluorescence in situ hybridization. Chromosoma 103:408–13 [Google Scholar]
  95. Taga M, Murata M, VanEtten HD. 95.  1999. Visualization of a conditionally dispensable chromosome in the filamentous ascomycete Nectria haematococca by fluorescence in situ hybridization. Fungal Genet. Biol. 26:169–77 [Google Scholar]
  96. Temporini ED, VanEtten HD. 96.  2002. Distribution of the pea pathogenicity (PEP) genes in the fungus Nectria haematococca mating population VI. Curr. Genet. 41:107–14 [Google Scholar]
  97. Thomma BP. 97.  2003. Alternaria spp.: from general saprophyte to specific parasite. Mol. Plant Pathol. 4:225–36 [Google Scholar]
  98. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M. 98.  et al. 2013. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol. Rev. 37:44–66 [Google Scholar]
  99. Tsuge T, Harimoto Y, Hanada K, Akagi Y, Kodama M. 99.  et al. 2016. Evolution of pathogenicity controlled by small, dispensable chromosomes in Alternaria alternata pathogens. Physiol. Mol. Plant Pathol. 95:27–31 [Google Scholar]
  100. Turgeon BG, Lu S-W. 100.  2000. Evolution of host specific virulence in Cochliobolus heterostrophus. Fungal Pathology JW Kronstad 93–126 Dordrecht, Neth.: Springer [Google Scholar]
  101. Tzeng T-H, Lyngholm L, Ford C, Bronson C. 101.  1992. A restriction fragment length polymorphism map and electrophoretic karyotype of the fungal maize pathogen Cochliobolus heterostrophus. . Genetics 130:81–96 [Google Scholar]
  102. VanEtten H, Jorgensen S, Enkerli J, Covert SF. 102.  1998. Inducing the loss of conditionally dispensable chromosomes in Nectria haematococca during vegetative growth. Curr. Genet. 33:299–303 [Google Scholar]
  103. Vlaardingerbroek I, Beerens B, Schmidt SM, Cornelissen BJC, Rep M. 103.  2016. Dispensable chromosomes in Fusarium oxysporum f. sp. lycopersici. . Mol. Plant Pathol. 17:91455–66 [Google Scholar]
  104. Walton JD. 104.  2006. HC-toxin. Phytochemistry 67:1406–13 [Google Scholar]
  105. Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M. 105.  et al. 2013. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat. Genet. 45:1092–96 [Google Scholar]
  106. Wieloch W. 106.  2006. Chromosome visualisation in filamentous fungi. J. Microbiol. Methods 67:1–8 [Google Scholar]
  107. Wilson E. 107.  1907. The supernumerary chromosomes of Hemiptera. Science 26:870–71 [Google Scholar]
  108. Wittenberg AH, van der Lee TA, M'Barek SB, Ware SB, Goodwin SB. 108.  et al. 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. . PLOS ONE 4:e5863 [Google Scholar]
  109. Xu JR, Leslie JF. 109.  1996. A genetic map of Gibberella fujikuroi mating population A (Fusarium moniliforme). Genetics 143:175–89 [Google Scholar]
  110. Zhan J, Mundt C, McDonald B. 110.  2007. Sexual reproduction facilitates the adaptation of parasites to antagonistic host environments: evidence from empirical study in the wheat–Mycosphaerella graminicola system. Int. J. Parasitol. 37:861–70 [Google Scholar]
  111. Zolan ME. 111.  1995. Chromosome-length polymorphism in fungi. Microbiol. Rev. 59:686–98 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error