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  • Review Article
  • Published:

Evolution and genome architecture in fungal plant pathogens

Nature Reviews Microbiology volume 15, pages 756–771 (2017)Cite this article

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A Corrigendum to this article was published on 10 November 2017

This article has been updated

Key Points

  • During crop production, fungal plant pathogens cause severe yield losses. Uniform agricultural ecosystems are conducive for the rapid evolution and dissemination of pathogens.

  • The genomes of fungal plant pathogens can vary in size and composition, even between closely related species. Differences in the content of transposable elements cause variation in genome architecture.

  • Variation in genome architecture results from differences in population genetic factors, including effective population size and the strength of genetic drift.

  • During periods of low effective population size, non-adaptive mutations, such as transposable elements, can invade genomes and shape their architecture.

  • Transposable elements contribute to the establishment and maintenance of rapidly evolving genome compartments that can comprise virulence genes. High mutation rates in these compartments support the evolution of new virulence phenotypes.

Abstract

The fungal kingdom comprises some of the most devastating plant pathogens. Sequencing the genomes of fungal pathogens has shown a remarkable variability in genome size and architecture. Population genomic data enable us to understand the mechanisms and the history of changes in genome size and adaptive evolution in plant pathogens. Although transposable elements predominantly have negative effects on their host, fungal pathogens provide prominent examples of advantageous associations between rapidly evolving transposable elements and virulence genes that cause variation in virulence phenotypes. By providing homogeneous environments at large regional scales, managed ecosystems, such as modern agriculture, can be conducive for the rapid evolution and dispersal of pathogens. In this Review, we summarize key examples from fungal plant pathogen genomics and discuss evolutionary processes in pathogenic fungi in the context of molecular evolution, population genomics and agriculture.

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Figure 1: Fungal plant pathogens with diverse lifestyles and hosts.
Figure 2: Models of host–pathogen co-evolution.
Figure 3: Characteristics of fungal plant pathogen genomes.
Figure 4: Accessory chromosome dynamics and hybridization in pathogenic fungi.

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Change history

  • 31 August 2017

    In Table 1 of this article, the species-specific hosts for both Leptosphaeria species should be crucifers (currently it is written as conifers). The mistakes have been corrected in the PDF and online. The authors apologize to the readers for any confusion caused.

References

  1. Fisher, M., Henk, D. & Briggs, C. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

    Article  CAS  PubMed  Google Scholar 

  2. James, T. Y. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818–822 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Lo Presti, L. et al. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66, 513–545 (2015).

    Article  CAS  PubMed  Google Scholar 

  4. Wolpert, T. J., Dunkle, L. D. & Ciuffetti, L. M. Host-selective toxins and avirulence determinants: what's in a name? Annu. Rev. Phytopathol. 40, 251–285 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Friesen, T. L., Faris, J. D., Solomon, P. S. & Oliver, R. P. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell. Microbiol. 10, 1421–1428 (2008).

    Article  CAS  PubMed  Google Scholar 

  6. Javelle, M., Vernoud, V., Rogowsky, P. M. & Ingram, G. C. Epidermis: the formation and functions of a fundamental plant tissue. New Phytol. 189, 17–39 (2011).

    Article  CAS  PubMed  Google Scholar 

  7. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  8. Weiberg, A. et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118–123 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Manning, V. A. & Ciuffetti, L. M. Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17, 3203–3212 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Djamei, A. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Bergelson, J., Kreitman, M., Stahl, E. A. & Tian, D. Evolutionary dynamics of plant R-genes. Science 292, 2281–2285 (2001).

    Article  CAS  PubMed  Google Scholar 

  12. Barrett, L. G. et al. Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini. Mol. Biol. Evol. 26, 2499–2513 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Dodds, P. N. et al. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl Acad. Sci. USA 103, 8888–8893 (2006).

    Article  CAS  PubMed  Google Scholar 

  14. Kanzaki, H. et al. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 72, 894–907 (2012).

    Article  CAS  PubMed  Google Scholar 

  15. Stukenbrock, E. H. et al. The making of a new pathogen: Insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21, 2157–2166 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. de Jonge, R. et al. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23, 1271–1282 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Menardo, F. et al. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat. Genet. 48, 201–205 (2016). This study provides an example of rapid adaptation to new host plants. The hybridization of two Blumeria graminis formae speciales resulted in the emergence of a new pathogen that infects a hybrid crop of wheat and rye.

    Article  CAS  PubMed  Google Scholar 

  18. Selmecki, A., Forche, A. & Berman, J. Genomic plasticity of the human fungal pathogen Candida albicans. Eukaryot. Cell 9, 991–1008 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Farrer, R. A. et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc. Natl Acad. Sci. USA 108, 18732–18736 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Raffaele, S. & Kamoun, S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat. Rev. Microbiol. 10, 417–430 (2012).

    Article  CAS  PubMed  Google Scholar 

  21. Seidl, M. F. & Thomma, B. P. Sex or no sex: evolutionary adaptation occurs regardless. Bioessays 36, 335–345 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Galazka, J. M. & Freitag, M. Variability of chromosome structure in pathogenic fungi — of 'ends and odds'. Curr. Opin. Microbiol. 20, 19–26 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Allen, R. L. et al. Host–parasite coevolutionary conflict between Arabidopsis and Downy Mildew. Science 306, 1957–1960 (2004).

    Article  CAS  PubMed  Google Scholar 

  24. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956–963 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. Thrall, P. H. et al. Rapid genetic change underpins antagonistic coevolution in a natural host–pathogen metapopulation. Ecol. Lett. 15, 425–435 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Laine, A.-L., Burdon, J. J., Nemri, A. & Thrall, P. H. Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation. Proc. R. Soc. B Biol. Sci. 281, 20140522 (2014).

    Article  Google Scholar 

  27. Persoons, A. et al. The escalatory Red Queen: population extinction and replacement following arms-race dynamics in poplar rust. Mol. Ecol. 26, 1902–1918 (2016).

    Article  Google Scholar 

  28. Daverdin, G. et al. Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog. 8, e1003020 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rouxel, T. et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat. Commun. 2, 202 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Brown, J. K. & Hovmøller, M. S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541 (2002).

    Article  CAS  PubMed  Google Scholar 

  31. Islam, M. T. et al. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 14, 84 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Castroagudin, V. L. et al. Wheat blast disease caused by Pyricularia graminis-tritici sp. nov. Preprint at bioRxiv http://dx.doi.org/10.1101/051151 (2016).

  33. Brasier, C. M. Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience 51, 123 (2001).

    Article  Google Scholar 

  34. Brasier, C. M. & Kirk, S. A. Rapid emergence of hybrids between the two subspecies of Ophiostoma novo-ulmi with a high level of pathogenic fitness. Plant Pathol. 59, 186–199 (2010).

    Article  CAS  Google Scholar 

  35. McDonald, B. A. & Stukenbrock, E. H. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Phil. Trans. R. Soc. B 371, 20160026 (2016).

    Article  PubMed  Google Scholar 

  36. Stukenbrock, E. H. Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens. New Phytol. 199, 895–907 (2013).

    Article  PubMed  Google Scholar 

  37. Brown, J. K. & Tellier, A. Plant–parasite coevolution: bridging the gap between genetics and ecology. Annu. Rev. Phytopathol. 49, 345–367 (2011).

    Article  CAS  PubMed  Google Scholar 

  38. Hörger, A. C. et al. Balancing selection at the tomato RCR3 guardee gene family maintains variation in strength of pathogen defense. PLoS Genet. 8, e1002813 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Tellier, A., Moreno-Gámez, S. & Stephan, W. Speed of adaptation and genomic footprints of host–parasite coevolution under arms race and trench warfare dynamics. Evolution. 68, 2211–2224 (2014).

    PubMed  Google Scholar 

  40. Van der Hoorn, R. A., De Wit, P. J. & Joosten, M. H. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7, 67–71 (2002).

    Article  CAS  PubMed  Google Scholar 

  41. Badouin, H. et al. Widespread selective sweeps throughout the genome of model plant pathogenic fungi and identification of effector candidates. Mol. Ecol. 26, 2041–2062 (2016).

    Article  CAS  Google Scholar 

  42. Chuma, I. et al. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathog. 7, e1002147 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ma, L.-J. et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367–373 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Faino, L. et al. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Res. 26, 1091–1100 (2016). This study describes the importance of transposable elements in the formation of lineage-specific regions and their differential regulation in distinct genome compartments in V. dahliae.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Goodwin, S. B. et al. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7, e1002070 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Coleman, J. J. et al. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5, e1000618 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Williams, A. H. et al. Comparative genomics and prediction of conditionally dispensable sequences in legume-infecting Fusarium oxysporum formae speciales facilitates identification of candidate effectors. BMC Genomics 17, 191 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Dutheil, J. Y. et al. A tale of genome compartmentalization: the evolution of virulence clusters in smut fungi. Genome Biol. Evol. 8, 681–704 (2016). This study provides details of the evolution of virulence-associated gene clusters in S. scitamineum that are driven by tandem gene duplication and transposable elements.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Dong, S., Raffaele, S. & Kamoun, S. The two-speed genomes of filamentous pathogens: waltz with plants. Curr. Opin. Genet. Dev. 35, 57–65 (2015).

    Article  CAS  PubMed  Google Scholar 

  50. Stukenbrock, E. H. et al. Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet. 6, e1001189 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Houben, A., Banaei-Moghaddam, A. M., Klemme, S. & Timmis, J. N. Evolution and biology of supernumerary B chromosomes. Cell. Mol. Life Sci. 71, 467–478 (2014).

    Article  CAS  PubMed  Google Scholar 

  52. Miao, V. P., Covert, S. F. & VanEtten, H. D. A fungal gene for antibiotic resistance on a dispensable ('B') chromosome. Science 254, 1773 (1991).

    Article  CAS  PubMed  Google Scholar 

  53. Temporini, E. D. & VanEtten, H. D. Distribution of the pea pathogenicity (PEP) genes in the fungus Nectria haematococca mating population VI. Curr. Genet. 41, 107–114 (2002).

    Article  CAS  PubMed  Google Scholar 

  54. van der Does, H. C. et al. Transcription factors encoded on core and accessory chromosomes of Fusarium oxysporum induce expression of effector genes. PLoS Genet. 12, e1006401 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wittenberg, A. H. J. et al. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS ONE 4, e5863 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Croll, D., Zala, M. & McDonald, B. A. Breakage–fusion–bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet. 9, e1003567 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Stewart, E. l. et al. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol. Plant Pathol. http://dx.doi.org/10.1111/mpp.12515 (2017).

  58. Plissonneau, C. & Stürchler, A. The evolution of orphan regions in genomes of a fungal pathogen of wheat. mBio 7, e01231-16 (2016). In this study, comparison of the genome structure of two Z. tritici isolates identifies large chromosomal inversions and losses and/or gains of transposable element clusters, which highlights intraspecies genome diversity.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Chiara, M. et al. Genome sequencing of multiple isolates highlights subtelomeric genomic diversity within Fusarium fujikuroi. Genome Biol. Evol. 7, 3062–3069 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Soyer, J. L. et al. Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet. 10, e1004227 (2014). Effectors in L. maculans are located in AT-rich genome compartments. In this study, their regulation is shown to be mediated by the presence and absence of heterochromatin during infection.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Schotanus, K. et al. Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenetics Chromatin 8, 1 (2015). In this study, Genome-wide comparison of histone methylation marks reveals distinct patterns of the facultative heterochromatin mark H3K27me3 on core and accessory chromosomes.

    Article  CAS  Google Scholar 

  62. Kellner, R. et al. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol. Evol. 6, 1353–1365 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Miao, V. P., Freitag, M. & Selker, E. U. Short TpA-rich segments of the ζ-η region induce DNA methylation in Neurospora crassa. J. Mol. Biol. 300, 249–273 (2000).

    Article  CAS  PubMed  Google Scholar 

  64. Tamaru, H. & Selker, E. U. Synthesis of signals for de novo DNA methylation in Neurospora crassa. Mol. Cell. Biol. 23, 2379–2394 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Fontanillas, E. et al. Degeneration of the non-recombining regions in the mating-type chromosomes of the anther-smut fungi. Mol. Biol. Evol. 32, 928–943 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Kämper, J. et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97–101 (2006).

    Article  CAS  PubMed  Google Scholar 

  67. Schirawski, J. et al. Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330, 1546–1548 (2010).

    Article  CAS  PubMed  Google Scholar 

  68. Croll, D., Lendenmann, M. H., Stewart, E. & McDonald, B. A. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201, 1213–1228 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ohm, R. A. et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog. 8, e1003037 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Hane, J. K. et al. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol. 12, 1 (2011).

    Article  Google Scholar 

  71. Grandaubert, J. et al. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans–Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 15, 891 (2014). This study shows that the expansion of transposable elements in one member of the L. maculans–L. biglobosa species complex correlates to the evolution of pathogenicity in this species.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Chang, T.-C. et al. Comparative genomics of the sigatoka disease complex on banana suggests a link between parallel evolutionary changes in Pseudocercospora fijiensis and Pseudocercospora eumusae and increased virulence on the banana host. PLoS Genet. 12, e1005904 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Duplessis, S. et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl Acad. Sci. USA 108, 9166–9171 (2011).

    Article  CAS  PubMed  Google Scholar 

  74. Niehaus, E.-M. et al. Comparative 'omics' of the Fusarium fujikuroi species complex highlights differences in genetic potential and metabolite synthesis. Genome Biol. Evol. 8, 3574 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lynch, M. & Walsh, B. The origins of genome architecture (Sinauer Associates Sunderland, 2007).

    Google Scholar 

  76. McDonald, B. A. & Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40, 349–379 (2002).

    Article  CAS  PubMed  Google Scholar 

  77. Marais, G. & Charlesworth, B. Genome evolution: recombination speeds up adaptive evolution. Curr. Biol. 13, R68–R70 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. Feldbrügge, M., Kämper, J., Steinberg, G. & Kahmann, R. Regulation of mating and pathogenic development in Ustilago maydis. Curr. Opin. Microbiol. 7, 666–672 (2004).

    Article  CAS  PubMed  Google Scholar 

  79. Stukenbrock, E. H. & Dutheil, J. Y. Comparison of fine-scale recombination maps in fungal plant pathogens reveals dynamic recombination landscapes and intragenic hotspots. Preprint at bioRxiv https://dx.doi.org/10.1101/158907 (2017).

  80. Zheng, Y. et al. Development of microsatellite markers and construction of genetic map in rice blast pathogen Magnaporthe grisea. Fungal Genet. Biol. 45, 1340–1347 (2008).

    Article  CAS  PubMed  Google Scholar 

  81. Talas, F. & McDonald, B. A. Genome-wide analysis of Fusarium graminearum field populations reveals hotspots of recombination. BMC Genomics 16, 996 (2015). This study provides details of the genomic structure of Fusarium graminearum field populations, which reveals a high degree of sexual recombination and gene flow that enables rapid adaptation to changing environments.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Muller, H. J. Some genetic aspects of sex. Am. Nat. 66, 118–138 (1932).

    Article  Google Scholar 

  83. Taylor, J. W., Jacobson, D. J. & Fisher, M. C. The evolution of asexual fungi: reproduction, speciation and classification. Annu. Rev. Phytopathol. 37, 197–246 (1999).

    Article  CAS  PubMed  Google Scholar 

  84. Milgroom, M. G., del Mar Jiménez-Gasco, M., García, C. O., Drott, M. T. & Jiménez-Díaz, R. M. Recombination between clonal lineages of the asexual fungus Verticillium dahliae detected by genotyping by sequencing. PLoS ONE 9, e106740 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Short, D. P. G., Gurung, S., Hu, X., Inderbitzin, P. & Subbarao, K. V. Maintenance of sex-related genes and the co-occurrence of both mating types in Verticillium dahliae. PLoS ONE 9, e112145 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Ni, M. et al. Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol. 11, e1001653 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Couch, B. C. et al. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170, 613–630 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Jin, Y., Szarbo, L. J. & Carson, M. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100, 432–435 (2010).

    Article  PubMed  Google Scholar 

  89. Xhaard, C. et al. The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication. Mol. Ecol. 20, 2739–2755 (2011).

    Article  CAS  PubMed  Google Scholar 

  90. Ali, S. et al. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PLoS Pathog. 10, e1003903 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Saleh, D. et al. Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol. Ecol. 21, 1330–1344 (2012).

    Article  PubMed  Google Scholar 

  92. Ali, S., Leconte, M., Walker, A. S., Enjalbert, J. & Vallavieille-Pope, C. Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp tritici. Fungal Genet. Biol. 47, 828–838 (2010).

    Article  PubMed  Google Scholar 

  93. Smith, K. M. et al. Epigenetics of filamentous fungi. Rev. Cell Biol. Mol. Med. http://dx.doi.org/10.1002/3527600906.mcb.201100035 (2012).

  94. Dhillon, B., Cavaletto, J. R., Wood, K. V. & Goodwin, S. B. Accidental amplification and inactivation of a methyltransferase gene eliminates cytosine methylation in Mycosphaerella grami nicola. Genetics 186, 67–77 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Levin, H. L. & Moran, J. V. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615–627 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Daboussi, M.-J. & Capy, P. Transposable elements in filamentous fungi. Annu. Rev. Microbiol. 57, 275–299 (2003).

    Article  CAS  PubMed  Google Scholar 

  97. Capy, P., Gasperi, G., Biémont, C. & Bazin, C. Stress and transposable elements: co-evolution or useful parasites? Heredity (Edinb.) 85, 101–106 (2000).

    Article  CAS  Google Scholar 

  98. Dolgin, E. S. & Charlesworth, B. The fate of transposable elements in asexual populations. Genetics 174, 817–827 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 1401–1404 (2003).

    Article  CAS  PubMed  Google Scholar 

  100. Halkett, F. et al. Genetic discontinuities and disequilibria in recently established populations of the plant pathogenic fungus Mycosphaerella fijiensis. Mol. Ecol. 19, 3909–3923 (2010).

    Article  CAS  PubMed  Google Scholar 

  101. Munkacsi, A. B., Stoxen, S. & May, G. Ustilago maydis populations tracked maize through domestication and cultivation in the Americas. Proc. R. Soc. B Biol. Sci. 275, 1037–1046 (2008).

    Article  Google Scholar 

  102. Whittle, C. A. & Johannesson, H. Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma. Heredity (Edinb.) 107, 305–314 (2011).

    Article  CAS  Google Scholar 

  103. Badouin, H. et al. Chaos of rearrangements in the mating-type chromosomes of the anther-smut fungus Microbotryum lychnidis-dioicae. Genetics 200, 1275–1284 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Perlin, M. H. et al. Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus. BMC Genomics 16, 1 (2015).

    Article  CAS  Google Scholar 

  105. Okasha, S. Evolution and the Levels of Selection. (Oxford Univ. Press, 2006).

    Book  Google Scholar 

  106. Anderson, J. B. & Kohn, L. M. in Sex in Fungi: Molecular Determination and Evolutionary Implications. (eds Heitman J. et al.)333–348 (ASM Press, 2007).

    Google Scholar 

  107. James, T. Y., Stenlid, J., Olson, Å. & Johannesson, H. Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the Basidiomycete fungus Heterobasidion parviporum. Evolution. 62, 2279–2296 (2008).

    Article  CAS  PubMed  Google Scholar 

  108. Olson, A. & Stenlid, J. Plant pathogens: mitochondrial control of fungal hybrid virulence. Nature 411, 438 (2001).

    Article  CAS  PubMed  Google Scholar 

  109. Zheng, W. et al. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat. Commun. 4, 2673 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Stukenbrock, E. H. The role of hybridization in the evolution and emergence of new fungal plant pathogens. Phytopathology 106, 104–112 (2016).

    Article  CAS  PubMed  Google Scholar 

  111. Stukenbrock, E. H., Christiansen, F. B., Hansen, T. T., Dutheil, J. Y. & Schierup, M. H. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc. Natl Acad. Sci. USA 109, 10954–10959 (2012).

    Article  CAS  PubMed  Google Scholar 

  112. Inderbitzin, P., Davis, R. M., Bostock, R. M. & Subbarao, K. V. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS ONE 6, e18260 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Shoji, J.-Y., Charlton, N. D., Yi, M., Young, C. A. & Craven, K. D. Vegetative hyphal fusion and subsequent nuclear behavior in Epichloë grass endophytes. PLoS ONE 10, e0121875 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Schardl, C. & Craven, K. Interspecific hybridization in plant-associated fungi and oomycetes: a review. Mol. Ecol. 12, 2861–2873 (2003).

    Article  CAS  PubMed  Google Scholar 

  115. Baack, E. J. & Rieseberg, L. H. A genomic view of introgression and hybrid speciation. Curr. Opin. Genet. Dev. 17, 513–518 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Richards, T. A. et al. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21, 1897–1911 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Friesen, T. L. et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38, 953–956 (2006).

    Article  CAS  PubMed  Google Scholar 

  118. Liu, Z. et al. The Tsn1–ToxA interaction in the wheat–Stagonospora nodorum pathosystem parallels that of the wheat–tan spot system. Genome 49, 1265–1273 (2006).

    Article  CAS  PubMed  Google Scholar 

  119. Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl Acad. Sci. USA 107, 13544–13549 (2010).

    Article  CAS  PubMed  Google Scholar 

  120. Mcdonald, M. C., Ahren, D., Simpfendorfer, S., Milgate, A. & Solomon, P. S. The discovery of the virulence gene ToxA in the wheat and barley pathogen Bipolaris sorokiniana. Mol. Plant Pathol. http://dx.doi.org/10.1111/mpp.12535 (2017). This study shows that horizontal gene transfer of ToxA confers host-specific virulence across pathogens that infect wheat.

  121. Nikolaidis, N., Doran, N. & Cosgrove, D. J. Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol. Biol. Evol. 31, 376–386 (2014).

    Article  CAS  PubMed  Google Scholar 

  122. de Jonge, R. et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl Acad. Sci. USA 109, 5110–5115 (2012).

    Article  CAS  PubMed  Google Scholar 

  123. Gardiner, D. M. et al. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathog. 8, e1002952 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Burrell, R. A., McGranahan, N., Bartek, J. & Swanton, C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338–345 (2013).

    Article  CAS  PubMed  Google Scholar 

  125. Garsed, D. W. et al. The architecture and evolution of cancer neochromosomes. Cancer Cell 26, 653–667 (2014).

    Article  CAS  PubMed  Google Scholar 

  126. Wright, S. & Finnegan, D. Genome evolution: sex and the transposable element. Curr. Biol. 11, R296–R299 (2001).

    Article  CAS  PubMed  Google Scholar 

  127. Dang, Y., Yang, Q., Xue, Z. & Liu, Y. RNA interference in fungi: pathways, functions, and applications. Eukaryot. Cell 10, 1148–1155 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Cambareri, E. B., Jensen, B. C., Schabtach, E. & Selker, E. U. Repeat-induced G-C to A-T mutations in Neurospora. Science 244, 1571–1575 (1989).

    Article  CAS  PubMed  Google Scholar 

  129. Gladyshev, E. & Kleckner, N. Direct recognition of homology between double helices of DNA in Neurospora crassa. Nat. Commun. 5, 3509 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Laurie, J. D. et al. Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24, 1733–1745 (2012). This study details a genome comparison of three closely related smut fungi that reveals transposable element expansion in Ustilago hordei and the loss of RNAi components in U. maydis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Hood, M. E., Katawczik, M. & Giraud, T. Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170, 1081–1089 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Idnurm, A. & Howlett, B. J. Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet. Biol. 39, 31–37 (2003).

    Article  CAS  PubMed  Google Scholar 

  133. Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916–919 (2010).

    Article  CAS  PubMed  Google Scholar 

  134. Galagan, J. E. & Selker, E. U. RIP: The evolutionary cost of genome defense. Trends Genet. 20, 417–423 (2004).

    Article  CAS  PubMed  Google Scholar 

  135. Studt, L. et al. Knock-down of the methyltransferase Kmt6 relieves H3K27me3 and results in induction of cryptic and otherwise silent secondary metabolite gene clusters in Fusarium fujikuroi. Environ. Microbiol. 18, 4037–4054 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Connolly, L. R., Smith, K. M. & Freitag, M. The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters. PLoS Genet. 9, e1003916 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Letunic, I. & Bork, P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007).

    Article  CAS  PubMed  Google Scholar 

  138. Grandaubert, J., Bhattacharyya, A. & Stukenbrock, E. H. 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, 1323–1333 (2015).

    Article  CAS  Google Scholar 

  139. Vanheule, A. et al. Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen. BMC Genomics 17, 670 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Spanu, P. D. et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543–1546 (2010).

    Article  CAS  PubMed  Google Scholar 

  141. Wicker, T. et al. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat. Genet. 45, 1092–1096 (2013).

    Article  CAS  PubMed  Google Scholar 

  142. Hacquard, S. et al. Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc. Natl Acad. Sci. USA 110, E2219–E2228 (2013).

    Article  CAS  PubMed  Google Scholar 

  143. Dean, R. A. et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980–986 (2005).

    Article  CAS  PubMed  Google Scholar 

  144. Forgetta, V. et al. Sequencing of the Dutch elm disease fungus genome using the Roche/454 GS-FLX Titanium System in a comparison of multiple genomics core facilities. J. Biomol. Tech. 24, 39–49 (2013).

    PubMed  PubMed Central  Google Scholar 

  145. Cuomo, C. A. et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317, 1400–1402 (2007).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank B. McDonald, M. Freitag, J. Haueisen and J. Dutheil for helpful discussions and comments in regard to a previous version of this Review. Research carried out in the group of E.H.S. is funded by the Max Planck Society, Germany, and a personal grant from the State of Schleswig-Holstein, Germany, to E.H.S.

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Authors and Affiliations

  1. Environmental Genomics, Christian-Albrechts University of Kiel, Am Botanischen Garten 1–9, Kiel, 24118, Germany

    Mareike Möller & Eva H. Stukenbrock

  2. Max Planck Institute of Evolutionary Biology, August-Thienemann-Straße 2, Plön, 24306, Germany

    Mareike Möller & Eva H. Stukenbrock

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Correspondence to Eva H. Stukenbrock.

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FURTHER INFORMATION

phyloT

PowerPoint slides

Glossary

Biotrophs

Pathogens that manipulate host defences and obtain their nutrients from living plant cells through specialized 'feeding' structures or hyphae formed intracellularly in the host.

Necrotrophs

Pathogens that kill host cells by secreting toxins and enzymes to obtain nutrients for growth and reproduction.

Hemibiotrophs

Pathogens that undergo a longer latent or biotrophic phase followed by a switch to necrotrophic growth.

Effectors

Pathogen-produced molecules that are secreted during infection to manipulate host defences and facilitate pathogen invasion.

Apoplastic space

Space outside of the plant plasma membrane.

Symplastic space

Space on the inner side of the plant plasma membrane.

Cultivars

Varieties of crop plants of the same species that have distinct phenotypes and genotypes. Distinct cultivars are obtained by plant breeding, whereby desired traits are selected and propagated.

Transposable elements

Genetic elements that move from one location in the genome of their host to another. Transposable elements are also known as transposons.

Metapopulation dynamics

Local fluctuations in the (actual as well as effective) population size of spatially separated populations that belong to the same species.

Non-synonymous mutations

Nucleotide changes in coding sequences that alter the amino acid sequence in the translated proteins.

Synonymous mutations

Nucleotide changes in coding sequences that alter the codons, but not the amino acid sequence, in translated proteins.

Trench warfare

A model that predicts constant diversity in a host–pathogen system, due to the maintenance of multiple alleles at a co-evolving locus by positive diversifying selection or balancing selection.

'Arms race' evolution

The co-evolution of host and pathogen alleles, which results in the recurrent fixation of advantageous alleles at a co-evolving locus. The fixation of advantageous alleles is mediated by positive directional selection.

Tajimas D

A statistical test parameter that is used in population genetics and DNA sequence analyses. Tajima's test is used to identify sequences that do not fit the neutral theory model, by which the fate of any mutation is determined by genetic drift.

Divergence patterns

The distribution of substitutions varies along the genome, as different parts of the genome evolve by processes and by different rates. The underlying pattern of divergence can be investigated to unravel the history of mutational events and the effect of selection versus neutral processes on the sequence evolution.

Selective sweep

An increase in the frequency of an advantageous allele (and closely linked chromosomal segments) that is caused by positive selection. Sweeps initially decrease genetic variation and subsequently lead to a local excess of rare alleles (homozygosity excess) as new unique mutations accumulate.

Linkage disequilibrium

The non-random association of alleles at different loci.

Accessory chromosomes

Chromosomes that are not present in all isolates of the same pathogenic species. Such chromosomes often encode determinants of host specificity.

Heterothallic

In heterothallic species, two individuals that have opposite mating types are required for sexual reproduction. By contrast, homothallic organisms have both mating types in one thallus.

Mesosynteny

A term that refers to the conservation of gene content on chromosomes, but a variation in the gene order and orientation. This is a phenomenon that is, thus far, particularly described in dothideomycete fungi.

Effective population size

(Ne). The approximate number of breeding individuals that produce offspring that live to reproductive age. This number influences the rate of loss of genetic variation, the efficiency of natural selection, and the accumulation of beneficial and deleterious mutations. It is frequently much smaller than the number of individuals in a population.

Sexual spores

Spores that originate from sexual crossings that differ morphologically from asexual spores.

Muller's ratchet

The irreversible accumulation of deleterious mutations in organisms that reproduce asexually.

Parasexual

A process whereby genetic material is exchanged between fused hyphae or cells without meiosis. Parasexuality enables the organism to recombine its genome and generate new genotypes in the absence of sexual mating.

Selection coefficient

The average proportional reduction in fitness of one genotype relative to another owing to selection (designated by 's').

Heterokaryons

Cells that contain two or more genetically distinct nuclei.

Introgressive hybridization

The transfer of genes from one species to another through hybridization followed by backcrossing with the parental species.

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Möller, M., Stukenbrock, E. Evolution and genome architecture in fungal plant pathogens. Nat Rev Microbiol 15, 756–771 (2017). https://doi.org/10.1038/nrmicro.2017.76

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