Evolutionary and adaptive role of transposable elements in fungal genomes

Advances in Botanical Research

Volumn 70, Issue , 2014, Pages 79-107

  Grandaubert, Jonathan ^a   Balesdent, Marie Helene ^a   Rouxel, Thierry ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Adaptation to host; Effectors; Fungal genomes; Pathogenicity; Speciation; Transposable elements

Indexed keywords

EID: 84900851386     PISSN: 00652296     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-397940-7.00003-3     Document Type: Chapter

References (108)

1. Ambrozová K., Mandakova T., Bures P., Neumann P., Leitch I.J., Koblizkova A. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Annals of Botany 2011, 107:255-268.
2. Aramayo R., Metzenberg R.L. Meiotic transvection in fungi. Cell 1996, 86:103-113.
3. Balesdent M.H., Fudal I., Ollivier B., Bally P., Grandaubert J., Eber F., et al. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. The New Phytologist 2013, 198:887-898.
4. Bennetzen J.L., Ma J., Devos K.M. Mechanisms of recent genome size variation in flowering plants. Current Opinion in Genetics & Development 2005, 15:621-627.
5. Biémont C. A brief history of the status of transposable elements: From junk DNA to major players in evolution. Genetics 2010, 186:1085-1093.
6. Biémont C., Vieira C. Junk DNA as an evolutionary force. Nature 2006, 443:521-524.
7. Biémont C., Vieira C., Hoogland C., Cizeron G., Loevenbruck C., Arnault C., et al. Maintenance of transposable copy element number in natural populations of Drosophila melanogaster and D. simulans. Genetica 1997, 100:161-166.
8. Bird A. Perceptions of epigenetics. Nature 2007, 447:396-398.
9. Botstein D., Chervitz S.A., Cherry J.M. Yeast as a model organism. Science 1997, 277:1259-1260.
10. Chuma I., Isobe C., Hotta Y., Ibaragi K., Futamata N., Kusaba M. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathogens 2011, 7:e1002147.
11. Clutterbuck A.J. Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genetics and Biology 2011, 48:306-326.
12. Cogoni C., Irelan J.T., Schumacher M., Schmidhauser T.J., Selker E.U., Macino G. Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. The EMBO Journal 1996, 15:3153-3163.
13. Coleman J.J., Rounsley S.D., Rodriguez-Carres M., Kuo A., Wasmann C.C., Grimwood J., et al. The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genetics 2009, 5:e1000618.
14. Cuomo C.A., Guldener U., Xu J.R., Trail F., Turgeon B.G., Di Pietro A., et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
15. Daverdin G., Rouxel T., Gout L., Aubertot J.N., Fudal I., Meyer M., et al. Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathogens 2012, 8:e1003020.
16. Dean R.A., Talbot N.J., Ebbole D.J., Farman M.L., Mitchell T.K., Orbach M.J., et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 2005, 434:980-986.
17. De Jonge R., Bolton M.D., Kombrink A., van den Berg G.C., Yadeta K.A., Thomma B.P. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Research 2013, 23:1271-1282.
18. Delprat A., Negre B., Puig M., Ruiz A. The transposon Galileo generates natural chromosomal inversions in Drosophila by ectopic recombination. PLoS One 2009, 4:e7883.
19. De Wit P.J., van der Burgt A., Ökmen B., Stergiopoulos I., Abd-Elsalam K.A., Aerts A.L., et al. 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 Genetics 2012, 8:e1003088.
20. Drinnenberg I.A., Weinberg D.E., Xie K.T., Mower J.P., Wolfe K.H., Fink G.R., et al. RNAi in budding yeast. Science 2009, 326:544-550.
21. Duplessis S., Cuomo C.A., Lin Y.C., Aerts A., Tisserant E., Veneault-Fourrey C., et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:9166-9171.
22. Ellis J.G., Dodds P.N., Lawrence G.J. The role of secreted proteins in diseases of plants caused by rust, powdery mildew and smut fungi. Current Opinion in Microbiology 2007, 10:326-331.
23. Fablet M., Vieira C. Evolvability, epigenetics and transposable elements. Biomolecular Concepts 2011, 2:333-341.
24. Farman M.L. Telomeres in the rice blast fungus Magnaporthe oryzae: The world of the end as we know it. FEMS Microbiology Letters 2007, 273:125-132.
25. Fedoroff N.V. Transposable elements, epigenetics, and genome evolution. Science 2012, 338:758-767.
26. Finnegan D.J. Eukaryotic transposable elements and genome evolution. Trends in Genetics 1989, 5:103-107.
27. Flor A.H. Host-parasite interactions in flax rust-its genetics and other implications. Phytopathology 1955, 45:680-685.
28. Freitag M., Williams R.L., Kothe G.O., Selker E.U. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:8802-8807.
29. Friesen T.L., Stukenbrock E.H., Liu Z., Meinhardt S., Ling H., Faris J.D., et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 2006, 38:953-956.
30. Frost L.S., Leplae R., Summers A.O., Toussaint A. Mobile genetic elements: The agents of open source evolution. Nature Reviews. Microbiology 2005, 3:722-732.
31. Fudal I., Böhnert H.U., Tharreau D., Lebrun M.H. Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea. Fungal Genetics and Biology 2005, 42:761-772.
32. Fudal I., Ross S., Brun H., Besnard A.L., Ermel M., Kuhn M.L., et al. Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Molecular Plant-Microbe Interactions 2009, 22:932-941.
33. Fudal I., Ross S., Gout L., Blaise F., Kuhn M.L., Eckert M.R., et al. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: Map-based cloning of AvrLm6. Molecular Plant-Microbe Interactions 2007, 20:459-470.
34. Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
35. Galagan J.E., Calvo S.E., Cuomo C., Ma L.J., Wortman J.R., Batzoglou S., et al. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438:1105-1115.
36. Galagan J.E., Henn M.R., Ma L.J., Cuomo C.A., Birren B. Genomics of the fungal kingdom: Insights into eukaryotic biology. Genome Research 2005, 15:1620-1631.
37. Galagan J.E., Selker E.U. RIP: The evolutionary cost of genome defense. Trends in Genetics 2004, 20:417-423.
38. Gan P., Ikeda K., Irieda H., Narusaka M., O'Connell R.J., Narusaka Y., et al. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. The New Phytologist 2013, 197:1236-1249.
39. Godfrey D., Böhlenius H., Pedersen C., Zhang Z., Emmersen J., Thordal-Christensen H. Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 2010, 11:317.
40. Goffeau A., Barrell B.G., Bussey H., Davis R.W., Dujon B., Feldmann H., et al. Life with 6000 genes. Science 1996, 274:563-567.
41. Goodwin S.B., M'Barek S.B., Dhillon B., Wittenberg A.H., Crane C.F., Hane J.K., et al. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics 2011, 7:e1002070.
42. Gout L., Fudal I., Kuhn M.L., Blaise F., Eckert M., Cattolico L., et al. Lost in the middle of nowhere: The AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Molecular Microbiology 2006, 60:67-80.
43. Gout L., Kuhn M.L., Vincenot L., Bernard-Samain S., Cattolico L., Barbetti M., et al. Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environmental Microbiology 2007, 9:2978-2992.
44. Goyon C., Rossignol J.L., Faugeron G. Native DNA repeats and methylation in Ascobolus. Nucleic Acids Research 1996, 24:3348-3356.
45. Graïa F., Lespinet O., Rimbault B., Dequard-Chablat M., Coppin E., Picard M. Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Molecular Microbiology 2001, 40:586-595.
46. Grandaubert J. Génomique comparative et évolutive au sein du complexe d'espèces Leptosphaeria maculans-Leptosphaeria biglobosa 2013, 363. Ph.D. Thesis, Paris XI-Orsay University, France.
47. Gregory, T.R. (2013). Animal Genome Size Database. http://www.genomesize.com.
48. Greilhuber J., Borsch T., Muller K., Worberg A., Porembski S., Barthlott W. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biology 2006, 8:770-777.
49. Hacquard S., Petre B., Frey P., Hecker A., Rouhier N., Duplessis S. The poplar-poplar rust interaction: Insights from genomics and transcriptomics. Journal of Pathogens 2011, 2011:716041.
50. Hane J.K., Lowe R.G.T., Solomon P.S., Tan K.C., Schoch C.L., Spatafora J.W., et al. Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. The Plant Cell 2007, 19:3347-3368.
51. Hane J.K., Rouxel T., Howlett B.J., Kema G.H., Goodwin S.B., Oliver R.P. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biology 2011, 12:R45.
52. Howlett B.J. Secondary metabolite toxins and nutrition of plant pathogenic fungi. Current Opinion in Plant Biology 2006, 9:371-375.
53. Hua-Van A., Le Rouzic A., Boutin T.S., Filee J., Capy P. The struggle for life of the genome's selfish architects. Biology Direct 2011, 6:19.
54. 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 Genetics and Biology 2003, 39:31-37.
55. Irelan J.T., Selker E.U. Gene silencing in filamentous fungi: RIP, MIP and quelling. Journal of Genetics 1996, 75:313-324.
56. Jaenisch R., Bird A. Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetics 2003, 33(Suppl.):245-254.
57. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
58. Joosten M.H., Vogelsang R., Cozijnsen T.J., Verberne M.C., De Wit P.J. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. The Plant Cell 1997, 9:367-379.
59. Kamoun S. Groovy times: Filamentous pathogen effectors revealed. Current Opinion in Plant Biology 2007, 10:358-365.
60. Kämper J., Kahmann R., Bolker M., Ma L.J., Brefort T., Saville B.J., et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 2006, 444:97-101.
61. Kang S., Lebrun M.H., Farrall L., Valent B. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Molecular Plant-Microbe Interactions 2001, 14:671-674.
62. Kapitonov V.V., Jurka J. Helitrons on a roll: Eukaryotic rolling-circle transposons. Trends in Genetics 2007, 23:521-529.
63. Kobayashi S., Goto-Yamamoto N., Hirochika H. Retrotransposon-induced mutations in grape skin color. Science 2004, 304:982.
64. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
65. Laurie J.D., Ali S., Linning R., Mannhaupt G., Wong P., Güldener U., et al. Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. The Plant Cell 2012, 24:1733-1745.
66. Lewis Z.A., Honda S., Khlafallah T.K., Jeffress J.K., Freitag M., Mohn F., et al. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Research 2008, 19:427-437.
67. Ma L.J., van der Does H.C., Borkovich K.A., Coleman J.J., Daboussi M.J., Di Pietro A., et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373.
68. Manning V.A., Pandelova I., Dhillon B., Wilhelm L.J., Goodwin S.B., Berlin A.M., et al. Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence. G3 (Bethesda) 2013, 3:41-63.
69. Martin F., Aerts A., Ahren D., Brun A., Danchin E.G., Duchaussoy F., et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
70. Martin F., Kamoun S. Effectors in plant-microbe interactions 2012, 426. Wiley-Blackwell (Press), Chichester, UK.
71. Martin F., Kohler A., Murat C., Balestrini R., Coutinho P.M., Jaillon O., et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038.
72. Maside X., Bartolome C., Assimacopoulos S., Charlesworth B. Rates of movement and distribution of transposable elements in Drosophila melanogaster: In situ hybridization vs. Southern blotting data. Genetical Research 2001, 78:121-136.
73. McClintock B. The origin and behavior of mutable loci in maize. Proceedings of the National Academy of Sciences of the United States of America 1950, 36:344-355.
74. McDonald B.A., Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 2002, 40:349-379.
75. Mehrabi R., Bahkali A.H., Abd-Elsalam K.A., Moslem M., Ben M'barek S., Gohari A.M., et al. Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiology Reviews 2011, 35:542-554.
76. Moazed D., Bühler M., Buker S.M., Colmenares S.U., Gerace E.L., et al. Studies on the mechanism of RNAi-dependent heterochromatin assembly. Cold Spring Harbor Symposia on Quantitative Biology 2006, 71:461-471.
77. Nekrutenko A., Li W.H. Transposable elements are found in a large number of human protein-coding genes. Trends in Genetics 2001, 17:619-621.
78. O'Connell R.J., Thon M.R., Hacquard S., Amyotte S.G., Kleemann J., Torres M.F., et al. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics 2012, 44:1060-1065.
79. Ohm R.A., Feau N., Henrissat B., Schoch C.L., Horwitz B.A., Barry K.W., et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathogens 2012, 8:e1003037.
80. Ohno S. So much "junk" DNA in our genome 1972, 366-370. Gordon & Breach, New York. H.H. Smith (Ed.).
81. Oliver K.R., Greene W.K. Transposable elements and viruses as factors in adaptation and evolution: An expansion and strengthening of the TE-thrust hypothesis. Ecology and Evolution 2012, 2:2912-2933.
82. Orbach M.J., Farrall L., Sweigard J.A., Chumley F.G., Valent B. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. The Plant Cell 2000, 12:2019-2032.
83. Orgel L.E., Crick F.H.C. Selfish DNA: The ultimate parasite. Nature 1980, 284:604-607.
84. Parlange F., Daverdin G., Fudal I., Kuhn M.L., Balesdent M.H., Blaise F., et al. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Molecular Microbiology 2009, 71:851-863.
85. Pritham E.J. Transposable elements and factors influencing their success in eukaryotes. Journal of Heredity 2009, 100:648-655.
86. Raffaele S., Kamoun S. Genome evolution in filamentous plant pathogens: Why bigger can be better. Nature Reviews. Microbiology 2012, 10:417-430.
87. Rebollo R., Horard B., Hubert B., Vieira C. Jumping genes and epigenetics: Towards new species. Gene 2010, 454:1-7.
88. Rep M., Meijer M., Houterman P.M., van der Does H.C., Cornelissen B.J. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Molecular Microbiology 2004, 53:1373-1383.
89. Richards T.A., Soanes D.M., Jones M.D., Vasieva O., Leonard G., Paszkiewicz K., et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:15258-15263.
90. Rouxel T., Grandaubert J., Hane J.K., Hoede C., van de Wouw A.P., Couloux A., et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point Mutations. Nature Communications 2011, 2:202.
91. Sacristan S., Vigouroux M., Pedersen C., Skamnioti P., Thordal-Christensen H., Micali C., et al. Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons. PLoS One 2009, 4:e7463.
92. Schardl C.L., Young C.A., Hesse U., Amyotte S.G., Andreeva K., Calie P.J., et al. Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 2013, 9:e1003323.
93. Schürch S., Linde C.C., Knogge W., Jackson L.F., McDonald B.A. Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Molecular Plant-Microbe Interactions 2004, 17:1114-1125.
94. Spanu P.D. The genomics of obligate (and nonobligate) biotrophs. Annual Review of Phytopathology 2012, 50:91-109.
95. Spanu P.D., Abbott J.C., Amselem J., Burgis T.A., Soanes D.M., Stuber K., et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 2010, 330:1543-1546.
96. Stergiopoulos I., De Kock M.J., Lindhout P., De Wit P.J. Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions 2007, 20:1271-1283.
97. Tyler B.M., Rouxel T. Effectors of fungi and oomycetes: Their virulence and avirulence functions and translocation from pathogen to host. Molecular plant immunity 2013, 123-167. John Wiley & Sons, Inc., Ames, USA; Chichester, UK & Oxford, UK. G. Sessa (Ed.).
98. Valent B., Khang C.H. Recent advances in rice blast effector research. Current Opinion in Plant Biology 2010, 13:434-441.
99. van de Lagemaat L.N., Landry J.R., Mager D.L., Medstrand P. Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends in Genetics 2003, 19:530-536.
100. van't Slot K.A.E., Knogge W. A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Critical Reviews in Plant Sciences 2002, 21:229-271.
101. Weiberg A., Wang M., Lin F.M., Zhao H., Zhang Z., Kaloshian I., et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 2013, 342:118-123.
102. Wicker T., Oberhaensli S., Parlange F., Buchmann J.P., Shatalina M., Roffler S., et al. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nature Genetics 2013, 45:1092-1096.
103. Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., et al. A unified classification system for eukaryotic transposable elements. Nature Reviews. Genetics 2007, 8:973-982.
104. Wolpert T.J., Dunkle L.D., Ciuffetti L.M. Host-selective toxins and avirulence determinants: What's in a name?. Annual Review of Phytopathology 2002, 40:251-285.
105. Wood V., Gwilliam R., Rajandream M.A., Lyne M., Lyne R., Stewart A., et al. The genome sequence of Schizosaccharomyces pombe. Nature 2002, 415:871-880.
106. Zhao H., Bourque G. Recovering genome rearrangements in the mammalian phylogeny. Genome Research 2009, 19:934-942.
107. Zheng A., Lin R., Zhang D., Qin P., Xu L., Ai P., et al. The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nature Communications 2013, 4:1424.
108. Zhou E., Jia Y., Singh P., Correll J.C., Lee F.N. Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genetics and Biology 2007, 44:1024-1034.