Artículos de revistas
Boto, A Class Ii Transposon In Moniliophthora Perniciosa, Is The First Representative Of The Pif/ Harbinger Superfamily In A Phytopathogenic Fungus
Registro en:
Microbiology (united Kingdom). , v. 159, n. 1, p. 112 - 125, 2013.
13500872
10.1099/mic.0.062901-0
2-s2.0-84871697529
Autor
Pereira J.F.
Almeida A.P.M.M.
Cota J.
Pamphile J.A.
da Silva G.F.
de Araujo E.F.
Gramacho K.P.
Brommonschenkel S.H.
Pereira G.A.G.
de Queiroz M.V.
Institución
Resumen
Boto, a class II transposable element, was characterized in the Moniliophthora perniciosa genome. The Boto transposase is highly similar to plant PIF-like transposases that belong to the newest class II superfamily known as PIF/Harbinger. Although Boto shares characteristics with PIF-like elements, other characteristics, such as the transposase intron position, the position and direction of the second ORF, and the footprint, indicate that Boto belongs to a novel family of the PIF/Harbinger superfamily. Southern blot analyses detected 6-12 copies of Boto in C-biotype isolates and a ubiquitous presence among the C- and S-biotypes, as well as a separation in the C-biotype isolates from Bahia State in Brazil in at least two genotypic groups, and a new insertion in the genome of a C-biotype isolate maintained in the laboratory for 6 years. In addition to PCR amplification from a specific insertion site, changes in the Boto hybridization profile after the M. perniciosa sexual cycle and detection of Boto transcripts gave further evidence of Boto activity. As an active family in the genome of M. perniciosa, Boto elements may contribute to genetic variability in this homothallic fungus. This is the first report of a PIF/Harbinger transposon in the genome of a phytopathogenic fungus. © 2013 SGM. 159 1 112 125 Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: A new generation of protein database search programs (1997) Nucleic Acids Res, 25, pp. 3389-3402 Anaya, N., Roncero, M.I.G., Stress-induced rearrangement of Fusarium retrotransposon sequences (1996) Mol Gen Genet, 253, pp. 89-94 Andebrhan, T., Furtek, D.B., Random amplified polymorphic DNA (RAPD) analysis of Crinipellis perniciosa isolates from different hosts (1994) Plant Pathol, 43, pp. 1020-1027 Andebrhan, T., Figueira, A., Yamada, M.M., Cascardo, J., Furtek, D.B., Molecular fingerprinting suggests two primary outbreaks of witches' broom disease (Crinipellis perniciosa) of Theobroma cacao in Bahia, Brazil (1999) Eur J Plant Pathol, 105, pp. 167-175 Bastos, C.N., Evans, H.C., A new pathotype of Crinipellis perniciosa (Witches' broom disease) on solanaceous hosts (1985) Plant Pathol, 34, pp. 306-312 Bastos, C.N., Andebrhan, T., de Almeida, L.C., Comparação morfológica de isolados de Crinipellis perniciosa (1988) Fitopatol Bras, 13, pp. 202-205 Benton, W.D., Davis, R.W., Screening lambdagt recombinant clones by hybridization to single plaques in situ (1977) Science, 196, pp. 180-182 Bergemann, M., Lespinet, O., M'Barek, S.B., Daboussi, M.J., Dufresne, M., Genome-wide analysis of the Fusarium oxysporum mimp family of MITEs and mobilization of both native and de novo created mimps (2008) J Mol Evol, 67, pp. 631-642 Daboussi, M.J., Capy, P., Transposable elements in filamentous fungi (2003) Annu Rev Microbiol, 57, pp. 275-299 Daboussi, M.J., Langin, T., Transposable elements in the fungal plant pathogen Fusarium oxysporum (1994) Genetica, 93, pp. 49-59 Daboussi, M.J., Langin, T., Brygoo, Y., Fot1, a new family of fungal transposable elements (1992) Mol Gen Genet, 232, pp. 12-16 de Arruda, M.C., Ferreira, M.A., Miller, R.N., Resende, M.L., Felipe, M.S., Nuclear and mitochondrial rDNA variability in Crinipellis perniciosa from different geographic origins and hosts (2003) Mycol Res, 107, pp. 25-37 de Arruda, M.C., Miller, R.N., Ferreira, M.A., Felipe, M.S., Comparison of Crinipellis perniciosa isolates from Brazil by ERIC repetitive element sequence-based PCR genomic fingerprint (2003) Plant Pathol, 52, pp. 236-244 Dobinson, K.F., Harris, R.E., Hamer, J.E., Grasshopper, a long terminal repeat (LTR) retroelement in the phytopathogenic fungus Magnaporthe grisea (1993) Mol Plant Microbe Interact, 6, pp. 114-126 Dufresne, M., Hua-Van, A., El Wahab, H.A., Ben M'Barek, S., Vasnier, C., Teysset, L., Kema, G.H.J., Daboussi, M.J., Transposition of a fungal miniature inverted-repeat transposable element through the action of a Tc1-like transposase (2007) Genetics, 175, pp. 441-452 Evans, H.C., Witches' broom disease of cocoa (Crinipellis perniciosa) in Ecuador (1978) Ann Appl Biol, 89, pp. 185-192 Felipe, M.S.S., Azevedo, M.A., Vainstein, M.H., Schrank, A., Biologia molecular de fungos filamentosos: Construção de banco genômico e de cDNA (1992) Manual Técnico, p. 99. , In, Piracicaba, SP, Brazil: Escola Superior de Agricultura 'Luiz de Queiroz' Fleetwood, D.J., Scott, B., Lane, G.A., Tanaka, A., Johnson, R.D., A complex ergovaline gene cluster in epichloe endophytes of grasses (2007) Appl Environ Microbiol, 73, pp. 2571-2579 Fleetwood, D.J., Khan, A.K., Johnson, R.D., Young, C.A., Mittal, S., Wrenn, R.E., Hesse, U., Scott, B., Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses (2011) Genome Biol Evol, 3, pp. 1253-1264 Gómez-Gómez, E., Anaya, N., Roncero, M.I.G., Hera, C., Folyt1, a new member of the hAT family, is active in the genome of the plant pathogen Fusarium oxysporum (1999) Fungal Genet Biol, 27, pp. 67-76 Goodwin, T.J., Poulter, R.T., The DIRS1 group of retrotransposons (2001) Mol Biol Evol, 18, pp. 2067-2082 Goodwin, T.J., Butler, M.I., Poulter, R.T., Cryptons: A group of tyrosine-recombinase-encoding DNA transposons from pathogenic fungi (2003) Microbiology, 149, pp. 3099-3109 Griffith, G.W., Hedger, J.N., A novel method for producing basidiocarps of the cocoa pathogen Crinipellis perniciosa using a branvermiculite medium (1993) Eur J Plant Pathol, 99, pp. 227-230 Grzebelus, D., Yau, Y.Y., Simon, P.W., Master: A novel family of PIF/Harbinger-like transposable elements identified in carrot (Daucus carota L.) (2006) Mol Genet Genomics, 275, pp. 450-459 Hancock, C.N., Zhang, F., Wessler, S.R., Transposition of the Tourist-MITE mPing in yeast: An assay that retains key features of catalysis by the class 2 PIF/Harbinger superfamily (2010) Mob DNA, 1, p. 5 He, C., Nourse, J.P., Irwin, J.A.G., Manners, J.M., Kelemu, S., CgT1: A non-LTR retrotransposon with restricted distribution in the fungal phytopathogen Colletotrichum gloeosporioides (1996) Mol Gen Genet, 252, pp. 320-331 Hedger, J.N., Pickering, V., Aragundi, J., Variability of populations of the witches' broom disease of cocoa (Crinipellis perniciosa) (1987) Trans Br Mycol Soc, 88, pp. 533-546 Hua-Van, A., Davière, J.M., Kaper, F., Langin, T., Daboussi, M.J., Genome organization in Fusarium oxysporum: Clusters of class II transposons (2000) Curr Genet, 37, pp. 339-347 Ignacchiti, M.D.C., Santana, M.F., Araújo, E.F., Queiroz, M.V., The distribution of a transposase sequence in Moniliophthora perniciosa confirms the occurrence of two genotypes in Bahia, Brazil (2011) Trop Plant Pathol, 36, pp. 276-286 Jiang, N., Bao, Z., Zhang, X., Hirochika, H., Eddy, S.R., McCouch, S.R., Wessler, S.R., An active DNA transposon family in rice (2003) Nature, 421, pp. 163-167 Jurka, J., Kapitonov, V.V., PIFs meet Tourists and Harbingers: A superfamily reunion (2001) Proc Natl Acad Sci U S A, 98, pp. 12315-12316 Kaneko, I., Tanaka, A., Tsuge, T., REAL, an LTR retrotransposon from the plant pathogenic fungus Alternaria alternata (2000) Mol Gen Genet, 263, pp. 625-634 Kapitonov, V.V., Jurka, J., Molecular paleontology of transposable elements from Arabidopsis thaliana (1999) Genetica, 107, pp. 27-37 Kapitonov, V.V., Jurka, J., Harbinger transposons and an ancient HARBI1 gene derived from a transposase (2004) DNA Cell Biol, 23, pp. 311-324 Keyhani, N.O., Fungal genomes and beyond (2011) Fungal Genom Biol, 1, pp. e101 Kito, H., Takahashi, Y., Sato, J., Fukiya, S., Sone, T., Tomita, F., Occan, a novel transposon in the Fot1 family, is ubiquitously found in several Magnaporthe grisea isolates (2003) Curr Genet, 42, pp. 322-331 Langin, T., Capy, P., Daboussi, M.J., The transposable element impala, a fungal member of the Tc1-mariner superfamily (1995) Mol Gen Genet, 246, pp. 19-28 Marchler-Bauer, A., Bryant, S.H., CD-Search: Protein domain annotations on the fly (2004) Nucleic Acids Res, 32, pp. W327-W331. , WEB SERVER ISSUE Maurer, P., Réjasse, A., Capy, P., Langin, T., Riba, G., Isolation of the transposable element hupfer from the entomopathogenic fungus Beauveria bassiana by insertion mutagenesis of the nitrate reductase structural gene (1997) Mol Gen Genet, 256, pp. 195-202 McClintock, B., The significance of responses of the genome to challenge (1984) Science, 226, pp. 792-801 Mes, J.J., Haring, M.A., Cornelissen, B.J.C., Foxy: An active family of short interspersed nuclear elements from Fusarium oxysporum (2000) Mol Gen Genet, 263, pp. 271-280 Mondego, J.M.C., Carazzolle, M.F., Costa, G.G.L., Formighieri, E.F., Parizzi, L.P., Rincones, J., Cotomacci, C., Cunha, A.F., A genome survey of Moniliophthora perniciosa gives new insights into Witches' Broom Disease of cacao (2008) BMC Genomics, 9, p. 548 Nakayashiki, H., Nishimoto, N., Ikeda, K., Tosa, Y., Mayama, S., Degenerate MAGGY elements in a subgroup of Pyricularia grisea: A possible example of successful capture of a genetic invader by a fungal genome (1999) Mol Gen Genet, 261, pp. 958-966 Niella, G., Resende, M.L., Castro, H.A., de Carvalho, G.A., Silva, L.H.C.P., Aperfeiçoamento da metodologia de produção artificial de basidiocarpos de Crinipellis perniciosa (1999) Fitopatol Bras, 24, pp. 523-527 Ogasawara, H., Obata, H., Hata, Y., Takahashi, S., Gomi, K., Crawler, a novel Tc1/mariner-type transposable element in Aspergillus oryzae transposes under stress conditions (2009) Fungal Genet Biol, 46, pp. 441-449 Okuda, M., Ikeda, K., Namiki, F., Nishi, K., Tsuge, T., Tfo1: An Ac-like transposon from the plant pathogenic fungus Fusarium oxysporum (1998) Mol Gen Genet, 258, pp. 599-607 Pereira, J.L., de Almeida, L.C.C., Santos, S.M., Witches' broom disease of cocoa in Bahia: Attempts at eradication and containment (1996) Crop Prot, 15, pp. 743-752 Pereira, J.F., Araújo, E.F., Brommonschenkel, S.H., Queiroz, M.V., Elementos transponíveis em fungos fitopatogênicos (2006) Rev Anual Patol Plant, 14, pp. 303-362 Pereira, J.F., Ignacchiti, M.D.C., Araújo, E.F., Brommonschenkel, S.H., Cascardo, J.C.M., Pereira, G.A.G., Queiroz, M.V., PCR amplification and sequence analyses of reverse transcriptaselike genes in Crinipellis perniciosa isolates (2007) Fitopatol Bras, 32, pp. 373-380 Ploetz, R.C., Schnell, R.J., Ying, Z.T., Zheng, Q., Olano, C.T., Motamayor, J.C., Johnson, E.S., Analysis of molecular diversity in Crinipellis perniciosa with AFLP markers (2005) Eur J Plant Pathol, 111, pp. 317-326 Pontecorvo, G., Roper, J.A.L., Hemmons, L.M., McDonald, K.D., Bufton, A.W.J., The genetics of Aspergillus nidulans (1953) Adv Genet, 5, pp. 141-238 Rep, M., van der Does, H.C., Cornelissen, B.J., Drifter, a novel, low copy hAT-like transposon in Fusarium oxysporum is activated during starvation (2005) Fungal Genet Biol, 42, pp. 546-553 Rincones, J., Meinhardt, L.W., Vidal, B.C., Pereira, G.A.G., Electrophoretic karyotype analysis of Crinipellis perniciosa, the causal agent of witches' broom disease of Theobroma cacao (2003) Mycol Res, 107, pp. 452-458 Rincones, J., Mazotti, G.D., Griffith, G.W., Pomela, A., Figueira, A., Leal Jr., G.A., Queiroz, M.V., Azevedo, R.A., Genetic variability and chromosome-length polymorphisms of the witches' broom pathogen Crinipellis perniciosa from various plant hosts in South America (2006) Mycol Res, 110, pp. 821-832 Rincones, J., Scarpari, L.M., Carazzolle, M.F., Mondego, J.M.C., Formighieri, E.F., Barau, J.G., Costa, G.G.L., Brentani, H.P., Differential gene expression between the biotrophic-like and saprotrophic mycelia of the witches' broom pathogen Moniliophthora perniciosa (2008) Mol Plant Microbe Interact, 21, pp. 891-908 Saitou, N., Nei, M., The neighbor-joining method: A new method for reconstructing phylogenetic trees (1987) Mol Biol Evol, 4, pp. 406-425 Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular Cloning: A Laboratory Manual, , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Sanger, F., Nicklen, S., Coulson, A.R., DNA sequencing with chain-terminating inhibitors (1977) Proc Natl Acad Sci U S A, 74, pp. 5463-5467 Schmidt, S.M., Panstruga, R., Pathogenomics of fungal plant parasites: What have we learnt about pathogenesis? (2011) Curr Opin Plant Biol, 14, pp. 392-399 Shim, W.B., Dunkle, L.D., Malazy, a degenerate, speciesspecific transposable element in Cercospora zeae-maydis (2005) Mycologia, 97, pp. 349-355 Shnyreva, A.V., Transposable elements are the factors involved in various rearrangements and modifications of fungal genomes (2003) Russ J Genet, 39, pp. 505-518 Shull, V., Hamer, J.E., Genetic differentiation in the rice blast fungus revealed by the distribution of the Fosbury retrotransposon (1996) Fungal Genet Biol, 20, pp. 59-69 Sinzelle, L., Kapitonov, V.V., Grzela, D.P., Jursch, T., Jurka, J., Izsvák, Z., Ivics, Z., Transposition of a reconstructed Harbinger element in human cells and functional homology with two transposon-derived cellular genes (2008) Proc Natl Acad Sci U S A, 105, pp. 4715-4720 Specht, C.A., DiRusso, C.C., Novotny, C.P., Ullrich, R.C., A method for extracting high-molecular-weight deoxyribonucleic acid from fungi (1982) Anal Biochem, 119, pp. 158-163 Stanke, M., Morgenstern, B., AUGUSTUS: A web server for gene prediction in eukaryotes that allows user-defined constraints (2005) Nucleic Acids Res, 33, pp. W465-W467. , WEB SERVER ISSUE Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice (1994) Nucleic Acids Res, 22, pp. 4673-4680 Walker, E.L., Eggleston, W.B., Demopulos, D., Kermicle, J., Dellaporta, S.L., Insertions of a novel class of transposable elements with a strong target site preference at the r locus of maize (1997) Genetics, 146, pp. 681-693 Wessler, S.R., Bureau, T.E., White, S.E., LTRretrotransposons and MITEs: Important players in the evolution of plant genomes (1995) Curr Opin Genet Dev, 5, pp. 814-821 Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Morgante, M., A unified classification system for eukaryotic transposable elements (2007) Nat Rev Genet, 8, pp. 973-982 Wöstemeyer, J., Kreibich, A., Repetitive DNA elements in fungi (Mycota): Impact on genomic architecture and evolution (2002) Curr Genet, 41, pp. 189-198 Yang, G.J., Zhang, F., Hancock, C.N., Wessler, S.R., Transposition of the rice miniature inverted repeat transposable element mPing in Arabidopsis thaliana (2007) Proc Natl Acad Sci U S A, 104, pp. 10962-10967 Yeadon, P.J., Catcheside, D.E., Guest: A 98 bp inverted repeat transposable element in Neurospora crassa (1995) Mol Gen Genet, 247, pp. 105-109 Zhang, X., Feschotte, C., Zhang, Q., Jiang, N., Eggleston, W.B., Wessler, S.R., P instability factor: An active maize transposon system associated with the amplification of Tourist-like MITEs and a new superfamily of transposases (2001) Proc Natl Acad Sci U S A, 98, pp. 12572-12577 Zhang, X., Jiang, N., Feschotte, C., Wessler, S.R., PIF-and Pong-like transposable elements: Distribution, evolution and relationship with Tourist-like miniature inverted-repeat transposable elements (2004) Genetics, 166, pp. 971-986 Zhou, M.B., Lu, J.-J., Zhong, H., Liu, X.-M., Tang, D.-Q., Distribution and diversity of PIF-like transposable elements in the Bambusoideae subfamily (2010) Plant Sci, 179, pp. 257-266 Zhou, M.B., Liu, X.M., Tang, D.Q., PpPIF-1: First isolated full-length PIF-like element from the bamboo Phyllostachys pubescens (2012) Genet Mol Res, 11, pp. 810-820