Abstract
A family of transposable elements belonging to the hAT group of DNA transposons is described from an oomycete, the plant pathogen Phytophthora infestans. The family, named DodoPi, was identified by studying a hotspot for retro- and DNA transposon insertions adjacent to the mating type locus. The DodoPi family comprises a small number of full-length copies, each of which is 2.7 kb long and predicted to encode a transposase-like protein consisting of 617 amino acids, and several truncated copies. Both types contain 12-bp terminal inverted repeats and are flanked by 8-bp target site duplications. Despite the detection of a DodoPi transcript and of many polymorphisms between isolates, conclusive evidence of recent transposition was not obtained. A phylogenetic analysis indicated that DodoPi was novel, with only modest similarity to some elements from plants and fungi. Relatives were detected in only some members of the genus. This is the first DNA transposon identified in the stramenopile group of eukaryotes.
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Abu-El Samen F, Secor GA, Gudmestad NC (2003) Variability in virulence among sexual progenies of Phytophthora infestans. Phytopathology 93:293–304
Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977
Bigot Y, Auge-Gouillou C, Periquet G (1996) Computer analyses reveal a hobo -like element in the nematode Caenorhabditis elegans, which presents a conserved transposase domain common with the Tc1 - Mariner transposon family. Gene 174:265–271
Buddenhagen IW (1958) Induced mutations and variability in Phytophthora cactorum. Am J Bot 45:355–365
Calvi BR, Hong TJ, Findley SD, Gelbart WM (1991) Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: Hobo, Activator , and Tam 3. Cell 66:465–472
Chamnanpunt J, Shan W-X, Tyler, BM (2001) High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae. Proc Natl Acad Sci USA 98:14530–14535
Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033
Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32
Craig NL, Craigie R, Gellert M, Lambowitz AM (2002) Mobile DNA II. ASM Press, Washington, D.C.
Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. Proc Natl Acad Sci USA 91:942–946
Emerson RA (1914) The inheritance of a recurring somatic variation in variegated ears of maize. Am Nat 48:87–115
Erwin DC, Zentmeyer GA, Galindo J, Niederhauser JS (1963) Variation in the genus Phytophthora. Annu Rev Phytopathol 1:375–396
Essers L, Adolphs RH, Kunze R (2000) A highly conserved domain of the maize Activator transposase is involved in dimerization. Plant Cell 12:211–224
Fabritius A-L, Cvitanich C, Judelson HS (2002) Stage-specific gene expression during sexual development in Phytophthora infestan s. Mol Microbiol 45:1057–1066
Fedoroff NV (1999) The Suppressor -mutator element and the evolutionary riddle of transposons. Genes Cells 4:11–19
Feschotte C, Zhang X, Wessler SR (2002). Miniature inverted-repeat transposable elements and their relationship to established DNA transposons. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington, D.C., pp 1147–1158
Finnegan DJ (1990) Transposable elements and DNA transposition in eukaryotes. Curr Opin Cell Biol 2:471–477
Fry WE, Goodwin SB (1997) Resurgence of the Irish potato famine fungus. Bioscience 47:363–371
Gomez-Gomez E, Anaya N, Roncero MIG, Hera C (1999) Folyt1, a new member of the hAT family, is active in the genome of the plant pathogen Fusarium oxysporum. Fungal Genet Biol 27:67–76
Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci USA 84:5823–5827
He ZH, Dong HT, Dong JX, Li DB, Ronald PC (2000) The rice Rim2 transcript accumulates in response to Magnaporthe grisea and its predicted protein product shares similarity with TNP2-like proteins encoded by CACTA transposons. Mol Gen Genet 264:2–10
Holyoake AJ, Kidwell MG (2003) Vege and Mar: two novel hAT MITE families from Drosophila willistoni. Mol Biol Evol 20:163–167
Judelson HS (1996) Genetic and physical variability at the mating type locus of the oomycete, Phytophthora infestans. Genetics 144:1005–1013
Judelson HS (2002) Sequence variation and genomic amplification of a family of Gypsy-like elements in the oomycete genus Phytophthora. Mol Biol Evol 19:1313–1322
Judelson HS, Randall TA (1998) Families of repeated DNA in the oomycete Phytophthora infestans and their distribution within the genus. Genome 41:605–615
Judelson HS, Spielman LJ, Shattock RC (1995) Genetic mapping and non-Mendelian segregation of mating type loci in the oomycete, Phytophthora infestans. Genetics 141:503–512
Kamoun S (2003) Molecular genetics of pathogenic oomycetes. Eukaryotic Cell 2:191–199
Kamoun S, Hraber P, Sobral B, Nuss D, Govers F (1999) Initial assessment of gene diversity for the oomycete pathogen Phytophthora infestans based on expressed sequences. Fungal Genet Biol 28:94–106.
Lam ST (2001) Phytophthora genomics consortium. Phytopathology 91:S158
Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110:1–9
Kidwell MG, Lisch DR (2000) Transposable elements and host genome evolution. Trends Ecol Evol 15:95–99
Kidwell MG, Kidwell JF, Sved JA (1977) Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86:813–833.
Kunze R, Weil CF (2002) The hAT and CACTA superfamilies of plant transposons. In: Craig NL, R Craigie, M Gellert, AM Lambowitz (eds) Mobile DNA II. ASM Press, Washington, D. C., pp. 565–610.
Kunze R, Stochaj U, Lauf S, Starlinger P (1987) Transcription of transposable element Activator (Ac) of Zea mays. EMBO J 6:1555–1563
Langley CH, Montgomery EA, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of copy number. Genet Res (Camb) 52:223–235
Linder-Basso D, Foglia R, Zhu P, Hillman BI (2001) Crypt1, an active Ac -like transposon from the chestnut blight fungus, Cryphonectria parasitica. Mol Gen Genet 265:730–738
Margulis L, Schwartz KV (2000). Five kingdoms: an illustrated guide to the phyla of life on earth. WH Freeman, New York
Michel K, O’Brochta DA, Atkinson PW (2002) Does the DSE motif form the active center in the Hermes transposase? Gene 298:141–146
Nitta N, Farman ML, Leong SA (1997) Genome organization of Magnaporthe grisea: integration of genetic maps, clustering of transposable elements and identification of genome duplications and rearrangements. Theor Appl Genet 95:20–32
O’Brochta DA, Atkinson PW (1996) Transposable elements and gene transformation in non-drosophilid insects. Insect Bioch Mol Biol 26:739–753
Olasz F, Kiss J, Koenig P, Buzas Z, Stalder R, Arber W (1998) Target specificity of insertion element IS30. Mol Microbiol 28:691–704
Randall TA, Judelson HS (1999) Construction of a bacterial artificial chromosome library of Phytophthora infestans and transformation of clones into P. infestans. Fungal Genet Biol 28:160–170
Randall TA, Ah Fong A, Judelson H (2003) Chromosomal heteromorphism and an apparent translocation detected using a BAC contig spanning the mating type locus of Phytophthora infestans. Fungal Genet Biol 38:75–84
Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957
San Miguel P, Tikhonov A, Jin Y-K, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards Keith J, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
Sansome E (1980) Reciprocal translocation heterozygosity in heterothallic species of Phytophthora and its significance. Nature 241:344–345
Tooley PW, Garfinkel DJ (1996) Presence of Ty1-copia group retrotransposon sequences in the potato late blight pathogen Phytophthora infestans. Mol Plant-Microbe Interact 9:305–309
Tooley PW, Therrien CD (1987) Cytophotometric determination of the nuclear DNA content of 23 Mexican and 18 non-Mexican isolates of Phytophthora infestans. Exp Mycol 11:19–26
Tooley PW, Carras MM, Falkenstein KF (1996) Relationships among group IV Phytophthora species inferred by restriction analysis of the ITS2 region. J Phytopathol 144:363–369
Van-Der-Lee T, De-Witte I, Drenth A, Alfonso C, Govers F (1997) AFLP linkage map of the oomycete Phytophthora infestans. Fungal Genet Biol 21:278–291
Villalba F, Lebrun M-H, Hua-Van A, Daboussi M-J, Grosjean-Cournoyer M-C (2001) Transposon impala, a novel tool for gene tagging in the rice blast fungus Magnaporthe grisea. Molec Plant-Microbe Interac 14:308–315
Waterhouse GM (1963) Key to the species of Phytophthora de Bary. CMI Mycological Paper No. 92, Commonwealth Mycological Institute, Kew, UK
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362
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We thank Martha Salcido for assistance. This work was supported by an award to H. S. J. from the National Science Foundation of the United States
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Communicated by C. P. Hollenberg
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Ah Fong, A.M.V., Judelson, H.S. The hAT -like DNA transposon DodoPi resides in a cluster of retro- and DNA transposons in the stramenopile Phytophthora infestans . Mol Genet Genomics 271, 577–585 (2004). https://doi.org/10.1007/s00438-004-1004-x
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DOI: https://doi.org/10.1007/s00438-004-1004-x