Artículos de revistas
A Potential Role For An Extracellular Methanol Oxidase Secreted By Moniliophthora Perniciosa In Witches' Broom Disease In Cacao
Registro en:
Fungal Genetics And Biology. , v. 49, n. 11, p. 922 - 932, 2012.
10871845
10.1016/j.fgb.2012.09.001
2-s2.0-84867903933
Autor
de Oliveira B.V.
Teixeira G.S.
Reis O.
Barau J.G.
Teixeira P.J.P.L.
do Rio M.C.S.
Domingues R.R.
Meinhardt L.W.
Paes Leme A.F.
Rincones J.
Pereira G.A.G.
Institución
Resumen
The hemibiotrophic basidiomycete fungus Moniliophthora perniciosa, the causal agent of Witches' broom disease (WBD) in cacao, is able to grow on methanol as the sole carbon source. In plants, one of the main sources of methanol is the pectin present in the structure of cell walls. Pectin is composed of highly methylesterified chains of galacturonic acid. The hydrolysis between the methyl radicals and galacturonic acid in esterified pectin, mediated by a pectin methylesterase (PME), releases methanol, which may be decomposed by a methanol oxidase (MOX). The analysis of the M. pernciosa genome revealed putative mox and pme genes. Real-time quantitative RT-PCR performed with RNA from mycelia grown in the presence of methanol or pectin as the sole carbon source and with RNA from infected cacao seedlings in different stages of the progression of WBD indicate that the two genes are coregulated, suggesting that the fungus may be metabolizing the methanol released from pectin. Moreover, immunolocalization of homogalacturonan, the main pectic domain that constitutes the primary cell wall matrix, shows a reduction in the level of pectin methyl esterification in infected cacao seedlings. Although MOX has been classically classified as a peroxisomal enzyme, M. perniciosa presents an extracellular methanol oxidase. Its activity was detected in the fungus culture supernatants, and mass spectrometry analysis indicated the presence of this enzyme in the fungus secretome. Because M. pernciosa possesses all genes classically related to methanol metabolism, we propose a peroxisome-independent model for the utilization of methanol by this fungus, which begins with the extracellular oxidation of methanol derived from the demethylation of pectin and finishes in the cytosol. © 2012 Elsevier Inc. 49 11 922 932 Aime, M.C., Phillips-Mora, W., The causal agents of Witches' broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae (2005) Mycologia, 97, pp. 1012-1022 Buckeridge, M.S., Reid, J.S., Purification and properties of a novel beta-galactosidase or exo-(1→4)-beta-d-galactanase from the cotyledons of germinated Lupinus angustifolius L. seeds (1994) Planta, 192, pp. 502-511 Daniel, G., Volc, J., Filonova, L., Plihal, O., Kubatova, E., Halada, P., Characteristics of Gloeophyllum trabeum alcohol oxidase, an extracellular source of H2O2 in brown rot decay of wood (2007) Appl. Environ. Microbiol., 73, pp. 6241-6253 de Hoop, M.J., Ab, G., Import of proteins into peroxisomes and other microbodies (1992) Biochem. J., 286 (PART 3), pp. 657-669 de Souza, T.A., Soprano, A.S., de Lira, N.P., Quaresma, A.J., Pauletti, B.A., Paes Leme, A.F., Benedetti, C.E., The TAL effector PthA4 interacts with nuclear factors involved in RNA-dependent processes including a HMG protein that selectively binds poly(U) RNA (2012) PLoS One, 7, pp. e32305 Delgado, J.C., Cook, A.A., Nuclear condition of basidia, basidiospores, and mycelium of Marasmius-Perniciosus (1976) Can. J. Bot. - Rev. Can. Bot., 54, pp. 66-72 Evans, H.C., Witches broom disease of cocoa (Crinipellis-Perniciosa) in Ecuador 1. Fungus (1978) Ann. Appl. Biol., 89, pp. 185-192 Evans, H.C., Pleomorphism in Crinipellis-Perniciosa, causal agent of Witches broom disease of cocoa (1980) Trans. Brit. Mycol. Soc., 74, pp. 515-523 Evans, H.C., Bastos, C.N., Basidiospore germination as a means of assessing resistance to Crinipellis-Perniciosa (Witches broom disease) in cocoa cultivars (1980) Trans. Brit. Mycol. Soc., 74, pp. 525-536 Frias, G.A., Purdy, L.H., Schmidt, R.A., Infection biology of Crinipellis-Perniciosa on vegetative flushes of cacao (1991) Plant Dis., 75, pp. 552-556 Giuseppin, M.L., Van Eijk, H.M., Bes, B.C., Molecular regulation of methanol oxidase activity in continuous cultures of Hansenula polymorpha (1988) Biotechnol. Bioeng., 32, pp. 577-583 Gould, S.G., Keller, G.A., Subramani, S., Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase (1987) J. Cell Biol., 105, pp. 2923-2931 Griffith, G.W., Hedger, J.N., The breeding biology of biotypes of the Witches-broom pathogen of cocoa Crinipellis-Perniciosa (1994) Heredity., 72, pp. 278-289 Griffith, G.W., Nicholson, J., Nenninger, A., Birch, R.N., Hedger, J.N., Witches' brooms and frosty pods: two major pathogens of cacao (2003) NZ J. Bot., 41, pp. 423-435 Guimaraes, R.L., Stotz, H.U., Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection (2004) Plant Physiol., 136, pp. 3703-3711 Gunkel, K., van Dijk, R., Veenhuis, M., van der Klei, I.J., Routing of Hansenula polymorpha alcohol oxidase: an alternative peroxisomal protein-sorting machinery (2004) Mol. Biol. Cell, 15, pp. 1347-1355 Han, Y., Joosten, H.J., Niu, W., Zhao, Z., Mariano, P.S., McCalman, M., van Kan, J., Dunaway-Mariano, D., Oxaloacetate hydrolase, the C-C bond lyase of oxalate secreting fungi (2007) J. Biol. Chem., 282, pp. 9581-9590 Hanna, S.L., Sherman, N.E., Kinter, M.T., Goldberg, J.B., Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry (2000) Microbiology, 146 (PSRT 10), pp. 2495-2508 Karnovsky, M.J., A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy (1965) J. Cell Biol., 27, p. 137 Kaszycki, P., Koloczek, H., Formaldehyde and methanol biodegradation with the methylotrophic yeast Hansenula polymorpha in a model wastewater system (2000) Microbiol. Res., 154, pp. 289-296 Langmead, B., Aligning short sequencing reads with Bowtie (2010) Curr. Protoc. Bioinfor, , Unit 11 7 (Chapter 11) Lazarow, P.B., The import receptor Pex7p and the PTS2 targeting sequence (2006) Biochim. Biophys. Acta, 1763, pp. 1599-1604 Martinez, D., Challacombe, J., Morgenstern, I., Hibbett, D., Schmoll, M., Kubicek, C.P., Ferreira, P., Cullen, D., Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion (2009) Proc. Natl. Acad. Sci. USA, 106, pp. 1954-1959 Meinhardt, L.W., Bellato Cde, M., Rincones, J., Azevedo, R.A., Cascardo, J.C., Pereira, G.A., In vitro production of biotrophic-like cultures of Crinipellis perniciosa, the causal agent of Witches' broom disease of Theobroma cacao (2006) Curr. Microbiol., 52, pp. 191-196 Mondego, J.M., Carazzolle, M.F., Costa, G.G., Formighieri, E.F., Parizzi, L.P., Rincones, J., Cotomacci, C., Pereira, G.A., A genome survey of Moniliophthora perniciosa gives new insights into Witches' broom disease of cacao (2008) BMC Genom., 9, p. 548 Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B., Mapping and quantifying mammalian transcriptomes by RNA-Seq (2008) Nat. Methods, 5, pp. 621-628 Nakagawa, T., Miyaji, T., Yurimoto, H., Sakai, Y., Kato, N., Tomizuka, N., A methylotrophic pathway participates in pectin utilization by Candida boidinii (2000) Appl. Environ. Microbiol., 66, pp. 4253-4257 Nakagawa, T., Yamada, K., Fujimura, S., Ito, T., Miyaji, T., Tomizuka, N., Pectin utilization by the methylotrophic yeast Pichia methanolica (2005) Microbiology, 151, pp. 2047-2052 Nemecek-Marshall, M., MacDonald, R.C., Franzen, J.J., Wojciechowski, C.L., Fall, R., Methanol emission from leaves (enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development) (1995) Plant Physiol., 108, pp. 1359-1368 Orfila, C., Knox, J.P., Spatial regulation of pectic polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp (2000) Plant Physiol., 122, pp. 775-781 Ozimek, P., Kotter, P., Veenhuis, M., van der Klei, I.J., Hansenula polymorpha and Saccharomyces cerevisiae Pex5p's recognize different, independent peroxisomal targeting signals in alcohol oxidase (2006) FEBS Lett., 580, pp. 46-50 Ozimek, P., Veenhuis, M., van der Klei, I.J., Alcohol oxidase: a complex peroxisomal, oligomeric flavoprotein (2005) FEMS Yeast Res., 5, pp. 975-983 Pelloux, J., Rusterucci, C., Mellerowicz, E.J., New insights into pectin methylesterase structure and function (2007) Trends Plant Sci., 12, pp. 267-277 Penman, D., Britton, G., Hardwick, K., Collin, H.A., Isaac, S., Chitin as a measure of biomass of Crinipellis perniciosa, causal agent of witches' broom disease of Theobroma cacao (2000) Mycol. Res., 104, pp. 671-675 Pereira, J.L., Ram, A., Figuereido, J.M., de Almeida, L.C., La primera aparición de la " Escoba de Bruja" en la principal región productora de cacao del Brasil (1989) Turrialba, 36, pp. 459-461 Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR (2001) Nucl. Acids Res., 29, pp. e45 Rincones, J., Scarpari, L.M., Carazzolle, M.F., Mondego, J.M., Formighieri, E.F., Barau, J.G., Costa, G.G., Pereira, G.A., 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 Rio, M.C., de Oliveira, B.V., de Tomazella, D.P., Silva, J.A., Pereira, G.A., Production of calcium oxalate crystals by the basidiomycete Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao (2008) Curr. Microbiol., 56, pp. 363-370 Roggenkamp, R., Janowicz, Z., Stanikowski, B., Hollenberg, C.P., Biosynthesis and regulation of the peroxisomal methanol oxidase from the methylotrophic yeast Hansenula polymorpha (1984) Mol. Gen. Genet., 194, pp. 489-493 Rozen, S., Skaletsky, H., Primer3 on the WWW for general users and for biologist programmers (2000) Methods Mol. Biol., 132, pp. 365-386 Sahm, H., Wagner, F., Microbial assimilation of methanol. The ethanol- and methanol-oxidizing enzymes of the yeast Candida boidinii (1973) Eur. J. Biochem., 36, pp. 250-256 Sakai, T., Sakamoto, T., Hallaert, J., Vandamme, E.J., Pectin, pectinase and protopectinase: production, properties, and applications (1993) Adv. Appl. Microbiol., 39, pp. 213-294 Scarpari, L.M., Meinhardt, L.W., Mazzafera, P., Pomella, A.W., Schiavinato, M.A., Cascardo, J.C., Pereira, G.A., Biochemical changes during the development of Witches' broom: the most important disease of cocoa in Brazil caused by Crinipellis perniciosa (2005) J. Exp. Bot., 56, pp. 865-877 Schlosser, D., Fahr, K., Karl, W., Wetzstein, H.G., Hydroxylated metabolites of 2,4-dichlorophenol imply a Fenton-type reaction in Gloeophyllum striatum (2000) Appl. Environ. Microbiol., 66, pp. 2479-2483 Segers, G., Bradshaw, N., Archer, D., Blissett, K., Oliver, R.P., Alcohol oxidase is a novel pathogenicity factor for Cladosporium fulvum, but aldehyde dehydrogenase is dispensable (2001) Mol. Plant-Microbe Interact., 14, pp. 367-377 Silva, S., Histologia da Interação Crinipellis perniciosa em Cacaueiros Suscetível e Resistente à Vassoura-de-Bruxa (1999) Fitopatol. Bras., 24, pp. 54-59 Teixeira, P.J.P.L., Mondego, J.M.C., Pereira, G.A.G., A method for production of Moniliophthora perniciosa basidiospores in vitro Manuscript in preparationThomazella, D.P., Teixeira, P.J., Oliveira, H.C., Saviani, E.E., Rincones, J., Toni, I.M., Reis, O., Pereira, G.A., The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development (2012) New Phytol Tiburcio, R.A., Costa, G.G., Carazzolle, M.F., Mondego, J.M., Schuster, S.C., Carlson, J.E., Guiltinan, M.J., Pereira, G.A., Genes acquired by horizontal transfer are potentially involved in the evolution of phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, two of the major pathogens of cacao (2010) J. Mol. Evol., 70, pp. 85-97 Valette-Collet, O., Cimerman, A., Reignault, P., Levis, C., Boccara, M., Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants (2003) Mol. Plant-Microbe Interact., 16, pp. 360-367 Van der Klei, I.J., Bystrykh, L.V., Harder, W., Alcohol oxidase from Hansenula polymorpha CBS 4732 (1990) Methods Enzymol., 188, pp. 420-427 Veenhuis, M., Van Dijken, J.P., Harder, W., The significance of peroxisomes in the metabolism of one-carbon compounds in yeasts (1983) Adv. Microb. Physiol., 24, pp. 1-82 Vidal, R.O., Mondego, J.M., Pot, D., Ambrosio, A.B., Andrade, A.C., Pereira, L.F., Colombo, C.A., Pereira, G.A., A high-throughput data mining of single nucleotide polymorphisms in Coffea species expressed sequence tags suggests differential homeologous gene expression in the allotetraploid Coffea arabica (2010) Plant Physiol., 154, pp. 1053-1066 Waterham, H.R., Russell, K.A., Vries, Y., Cregg, J.M., Peroxisomal targeting, import, and assembly of alcohol oxidase in Pichia pastoris (1997) J. Cell Biol., 139, pp. 1419-1431 Wierenga, R.K., Terpstra, P., Hol, W.G.J., Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint (1986) J. Mol. Biol., 187, pp. 101-107 Willats, W.G., Limberg, G., Buchholt, H.C., van Alebeek, G.J., Benen, J., Christensen, T.M., Visser, J., Knox, J.P., Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation (2000) Carbohydrate Res., 327, pp. 309-320 Willats, W.G., McCartney, L., Mackie, W., Knox, J.P., Pectin: cell biology and prospects for functional analysis (2001) Plant Mol. Biol., 47, pp. 9-27 Wymelenberg, A.V., Gaskell, J., Mozuch, M., Sabat, G., Ralph, J., Skyba, O., Mansfield, S.D., Cullen, D., Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium (2010) Appl. Environ. Microbiol., 76, pp. 3599-3610 Yurimoto, H., Komeda, T., Lim, C.R., Nakagawa, T., Kondo, K., Kato, N., Sakai, Y., Regulation and evaluation of five methanol-inducible promoters in the methylotrophic yeast Candida boidinii (2000) Biochim. Biophys. Acta, 1493, pp. 56-63 Yurimoto, H., Oku, M., Sakai, Y., Yeast methylotrophy: metabolism, gene regulation and peroxisome homeostasis (2011) Int. J. Microbiol., 2011, p. 101298