Artículos de revistas
High-resolution Transcript Profiling Of The Atypical Biotrophic Interaction Between Theobroma Cacao And The Fungal Pathogen Moniliophthora Perniciosa
Registro en:
Plant Cell. American Society Of Plant Biologists, v. 26, n. 11, p. 4245 - 4269, 2014.
10404651
10.1105/tpc.114.130807
2-s2.0-84919800656
Autor
Teixeira P.J.P.L.
De Toledo Thomazella D.P.
Reis O.
Prado P.F.V.D.
Rio M.C.S.D.
Fiorin G.L.
Jose J.
Costa G.G.L.
Negri V.A.
Mondego J.M.C.
Mieczkowski P.
Pereira G.A.G.
Institución
Resumen
Witches’ broom disease (WBD), caused by the hemibiotrophic fungus Moniliophthora perniciosa, is one of the most devastating diseases of Theobroma cacao, the chocolate tree. In contrast to other hemibiotrophic interactions, the WBD biotrophic stage lasts for months and is responsible for the most distinctive symptoms of the disease, which comprise drastic morphological changes in the infected shoots. Here, we used the dual RNA-seq approach to simultaneously assess the transcriptomes of cacao and M. perniciosa during their peculiar biotrophic interaction. Infection with M. perniciosa triggers massive metabolic reprogramming in the diseased tissues. Although apparently vigorous, the infected shoots are energetically expensive structures characterized by the induction of ineffective defense responses and by a clear carbon deprivation signature. Remarkably, the infection culminates in the establishment of a senescence process in the host, which signals the end of the WBD biotrophic stage. We analyzed the pathogen’s transcriptome in unprecedented detail and thereby characterized the fungal nutritional and infection strategies during WBD and identified putative virulence effectors. Interestingly,M. perniciosa biotrophic mycelia develop as long-termparasites that orchestrate changes in plantmetabolismto increase the availability of soluble nutrients before plant death. Collectively, our results provide unique insight into an intriguing tropical disease and advance our understanding of the development of (hemi)biotrophic plant-pathogen interactions. 26 11 4245 4269 Adhikari, T., Balaji, B., Breeden, J., Goodwin, S., Resistance of wheat to Mycosphaerella graminicola involves early and late peaks of gene expression. Physiol. Mol (2007) Plant Pathol, 71, pp. 55-68 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 Albersheim, P., Muhlethaler, K., Frey-Wyssling, A., Stained pectin as seen in the electron microscope (1960) J. Biophys. Biochem. Cytol, 8, pp. 501-506 Alvim, F.C., Mattos, E.M., Pirovani, C.P., Gramacho, K., Pungartnik, C., Brendel, M., Cascardo, J.C., Vincentz, M., Carbon sourceinduced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins (2009) Genet. Mol. Res, 8, pp. 1035-1050 Apel, K., Hirt, H., Reactive oxygen species: Metabolism, oxidative stress, and signal transduction (2004) Annu. Rev. Plant Biol, 55, pp. 373-399 ArgôLo Santos Carvalho, H., De Andrade Silva, E.M., Carvalho Santos, S., Micheli, F., Polygalacturonases from Moniliophthora perniciosa are regulated by fermentable carbon sources and possible post-translational modifications (2013) Fungal Genet. Biol, 60, pp. 110-121 Argout, X., The genome of Theobroma cacao (2011) Nat. Genet, 43, pp. 101-108 Azevedo, H., Lino-Neto, T., Tavares, R.M., An improved method for high-quality RNA isolation from needles of adult maritime pine trees (2003) Plant Mol. Biol. Rep, 21, pp. 333-338 Berger, S., Sinha, A.K., Roitsch, T., Plant physiology meets phytopathology: Plant primary metabolism and plant-pathogen interactions (2007) J. Exp. Bot, 58, pp. 4019-4026 Bonfig, K.B., Schreiber, U., Gabler, A., Roitsch, T., Berger, S., Infection with virulent and avirulent P. Syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves (2006) Planta, 225, pp. 1-12 Braun, B.R., Head, W.S., Wang, M.X., Johnson, A.D., Identification and characterization of TUP1-regulated genes in Candida albicans (2000) Genetics, 156, pp. 31-44 Buchanan-Wollaston, V., The molecular biology of leaf senescence (1997) J. Exp. Bot, 48, pp. 181-199 Caldo, R.A., Nettleton, D., Peng, J., Wise, R.P., Stagespecific suppression of basal defense discriminates barley plants containing fast- and delayed-acting Mla powdery mildew resistance alleles (2006) Mol. Plant Microbe Interact, 19, pp. 939-947 Cantacessi, C., Campbell, B.E., Visser, A., Geldhof, P., Nolan, M.J., Nisbet, A.J., Matthews, J.B., Gasser, R.B., A portrait of the “SCP/TAPS” proteins of eukaryotes—developing a framework for fundamental research and biotechnological outcomes (2009) Biotechnol. Adv, 27, pp. 376-388 Ceita, G.D., Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora pemiciosa (2007) Plant Sci, 173, pp. 106-117 Chandran, D., Inada, N., Hather, G., Kleindt, C.K., Andwildermuth, M.C., Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators (2010) Proc. Natl. Acad. Sci, 107, pp. 460-465. , USA Chou, H.M., Bundock, N., Rolfe, S.A., Scholes, J.D., Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism (2000) Mol. Plant Pathol, 1, pp. 99-113 Choudhary, V., Schneiter, R., Pathogen-Related Yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins (2012) Proc. Natl. Acad. Sci, 109, pp. 16882-16887. , USA Coleman, J.J., Mylonakis, E., Efflux in fungi: La pièce de résistance (2009) PLoS Pathog, 5 Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems (2013) Science, 339, pp. 819-823 Da Hora Junior, B.T., Poloni, J.F., Lopes, M.A., Dias, C.V., Gramacho, K.P., Schuster, I., Sabau, X., Andmicheli, F., Transcriptomics and systems biology analysis in identification of specific pathways involved in cacao resistance and susceptibility to witches’ broom disease. Mol (2012) Biosyst, 8, pp. 1507-1519 De O Barsottini, M.R., Functional diversification of cerato- platanins in Moniliophthora perniciosa as seen by differential expression and protein function specialization. Mol (2013) Plant Microbe Interact, 26, pp. 1281-1293 De Oliveira, B.V., Teixeira, G.S., Reis, O., Barau, J.G., Teixeira, P.J., Do Rio, M.C., Domingues, R.R., Pereira, G.A., A potential role for an extracellular methanol oxidase secreted by Moniliophthora perniciosa in Witches’ broom disease in cacao. Fungal Genet (2012) Biol, 49, pp. 922-932 De Wit, P.J., 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 (2012) PLoS Genet, 8 Deeken, R., Engelmann, J.C., Efetova, M., Czirjak, T., Müller, T., Kaiser, W.M., Tietz, O., Hedrich, R., An integrated view of gene expression and solute profiles of Arabidopsis tumors: A genomewide approach (2006) Plant Cell, 18, pp. 3617-3634 Dezwaan, T.M., Carroll, A.M., Valent, B., Sweigard, J.A., Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues (1999) Plant Cell, 11, pp. 2013-2030 Dias, C.V., Mendes, J.S., Dos Santos, A.C., Pirovani, C.P., Da Silva Gesteira, A., Micheli, F., Gramacho, K.P., De Mattos Cascardo, J.C., Hydrogen peroxide formation in cacao tissues infected by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Physiol (2011) Biochem, 49, pp. 917-922 Dodds, P.N., Rathjen, J.P., Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat (2010) Rev. Genet, 11, pp. 539-548 Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Kämper, J., Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis (2008) Plant J, 56, pp. 181-195 El Gueddari, N.E., Rauchhaus, U., Moerschbacher, B.M., Deising, H.B., Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi (2002) New Phytol, 156, pp. 103-112 Evans, H.C., Pleomorphism in Crinipellis perniciosa, causal agent of Witches’ broom disease of cocoa (1980) Trans. Br. Mycol. Soc, 74, pp. 515-526 Fernandez, D., Tisserant, E., Talhinhas, P., Azinheira, H., Vieira, A., Petitot, A.S., Loureiro, A., Duplessis, S., 454-pyrosequencing of Coffea arabica leaves infected by the rust fungus Hemileia vastatrix reveals in planta-expressed pathogen-secreted proteins and plant functions in a late compatible plant-rust interaction. Mol (2012) Plant Pathol, 13, pp. 17-37 Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., Gurr, S.J., Emerging fungal threats to animal, plant and ecosystem health (2012) Nature, 484, pp. 186-194 Fotopoulos, V., Gilbert, M.J., Pittman, J.K., Marvier, A.C., Buchanan, A.J., Sauer, N., Hall, J.L., Williams, L.E., The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum (2003) Plant Physiol, 132, pp. 821-829 Frias, G., Purdy, L.H., Schmidt, R.A., An inoculation method for evaluating resistence of cacao to Crinipellis perniciosa (1995) Plant Dis, 79, pp. 787-791 Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Nishida, I., Watanabe, A., Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol (2001) Plant, 111, pp. 345-352 Gan, S., Amasino, R.M., Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence) (1997) Plant Physiol, 113, pp. 313-319 Garnica, D.P., Upadhyaya, N.M., Dodds, P.N., Rathjen, J.P., Strategies for wheat stripe rust pathogenicity identified by transcriptome sequencing (2013) PLoS ONE, 8 Gerrits, P.O., Smid, L., A new, less toxic polymerization system for the embedding of soft tissues in glycol methacrylate and subsequent preparing of serial sections (1983) J. Microsc, 132, pp. 81-85 Gesteira, A.S., Micheli, F., Carels, N., Da Silva, A.C., Gramacho, K.P., Schuster, I., Macêdo, J.N., Cascardo, J.C., Comparative analysis of expressed genes from cacao meristems infected by Moniliophthora perniciosa (2007) Ann. Bot. (Lond.), 100, pp. 129-140 Gibbs, G.M., Roelants, K., O’bryan, M.K., The CAP superfamily: Cysteine-rich secretory proteins, antigen 5, and pathogenesis- related 1 proteins—roles in reproduction, cancer, and immune defense. Endocr (2008) Rev, 29, pp. 865-897 Glazebrook, J., Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu (2005) Rev. Phytopathol, 43, pp. 205-227 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 (2010) BMC Genomics, 11, p. 317 Goldman, N., Yang, Z., A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol (1994) Evol, 11, pp. 725-736 Graham, I.A., Seed storage oil mobilization. Annu (2008) Rev. Plant Biol, 59, pp. 115-142 Griffith, G.W., Nicholson, J., Nenninger, A., Birch, R.N., Hedger, J.N., Witches’ brooms and frosty pods: Two major pathogens of cacao. N.Z (2003) J. Bot, 41, pp. 423-435 Guyon, K., Balagué, C., Roby, D., Raffaele, S., Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum (2014) BMC Genomics, 15, p. 336 Horst, R.J., Engelsdorf, T., Sonnewald, U., Voll, L.M., Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis (2008) J. Plant Physiol, 165, pp. 19-28 Joly, D.L., Feau, N., Tanguay, P., Hamelin, R.C., Comparative analysis of secreted protein evolution using expressed sequence tags from four poplar leaf rusts (Melampsora spp.) (2010) BMC Genomics, 11, p. 422 Jones, J.D., Dangl, J.L., The plant immune system (2006) Nature, 444, pp. 323-329 Kale, S.D., External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells (2010) Cell, 142, pp. 284-295 Karnovsky, M.J., A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy (1965) J. Cell Biol, 27, pp. 137-139 Kawahara, Y., Oono, Y., Kanamori, H., Matsumoto, T., Itoh, T., Minami, E., Simultaneous RNA-seq analysis of a mixedtranscriptome of rice and blast fungus interaction (2012) PLoS ONE, 7 Kemen, E., Gardiner, A., Schultz-Larsen, T., Kemen, A.C., Balmuth, A.L., Robert-Seilaniantz, A., Bailey, K., Jones, J.D., Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana (2011) PLoS Biol, 9 Kilaru, A., Bailey, B.A., Hasenstein, K.H., Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves. FEMS Microbiol (2007) Lett, 274, pp. 238-244 Kulkarni, R.D., Kelkar, H.S., Dean, R.A., An eight-cysteine- containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem (2003) Sci, 28, pp. 118-121 Kunjeti, S.G., Evans, T.A., Marsh, A.G., Gregory, N.F., Kunjeti, S., Meyers, B.C., Kalavacharla, V.S., Donofrio, N.M., RNA-Seq reveals infection-related global gene changes in Phytophthora phaseoli, the causal agent of lima bean downy mildew. Mol (2012) Plant Pathol, 13, pp. 454-466 Lam, H.M., Peng, S.S., Coruzzi, G.M., Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana (1994) Plant Physiol, 106, pp. 1347-1357 Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome (2009) Genome Biol, 10, p. R25 Leal, G.A., Jr., Albuquerque, P.S., Figueira, A., Genes differentially expressed in Theobroma cacao associated with resistance to witches’ broom disease caused by Crinipellis perniciosa. Mol (2007) Plant Pathol, 8, pp. 279-292 Leal, G.A., Gomes, L.H., Albuquerque, P.S., Tavares, F.C., Figueira, A., Searching for Moniliophthora perniciosa pathogenicity genes (2010) Fungal Biol, 114, pp. 842-854 Li, L., Stoeckert, C.J., Jr., Roos, D.S., OrthoMCL: Identification of ortholog groups for eukaryotic genomes (2003) Genome Res, 13, pp. 2178-2189 Link, T.I., Lang, P., Scheffler, B.E., Duke, M.V., Graham, M.A., Cooper, B., Tucker, M.L., Whitham, S.A., The haustorial transcriptomes of Uromyces appendiculatus and Phakopsora pachyrhizi and their candidate effector families. Mol (2014) Plant Pathol, 15, pp. 379-393 Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method (2001) Methods, 25, pp. 402-408 Loqué, D., Ludewig, U., Yuan, L., Von WiréN, N., Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole (2005) Plant Physiol, 137, pp. 671-680 Lowe, R.G., Cassin, A., Grandaubert, J., Clark, B.L., Van Dewouw, A.P., Rouxel, T., Howlett, B.J., Genomes and transcriptomes of partners in plant-fungal-interactions between canola (Brassica napus) and two Leptosphaeria species (2014) PLoS ONE, 9 Maere, S., Heymans, K., Kuiper, M., BiNGO: A Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks (2005) Bioinformatics, 21, pp. 3448-3449 Marcel, S., Sawers, R., Oakeley, E., Angliker, H., Paszkowski, U., Tissue-adapted invasion strategies of the rice blast fungus Magnaporthe oryzae (2010) Plant Cell, 22, pp. 3177-3187 Meinhardt, L.W., Genome and secretome analysis of the hemibiotrophic fungal pathogen, Moniliophthora roreri, which causes frosty pod rot disease of cacao: Mechanisms of the biotrophic and necrotrophic phases (2014) BMC Genomics, 15, p. 164 Meinhardt, L.W., Rincones, J., Bailey, B.A., Aime, M.C., Griffith, G.W., Zhang, D., Pereira, G.A., Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: What’s new from this old foe? Mol (2008) Plant Pathol, 9, pp. 577-588 Melnick, R.L., Marelli, J.P., Sicher, R.C., Strem, M.D., Bailey, B.A., The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy. Tree Genet (2012) Genomes, 8, pp. 1261-1279 Moktali, V., Park, J., Fedorova-Abrams, N.D., Park, B., Choi, J., Lee, Y.H., Kang, S., Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes (2012) BMC Genomics, 13, p. 525 Monaghan, J., Zipfel, C., Plant pattern recognition receptor complexes at the plasma membrane (2012) Curr. Opin. Plant Biol, 15, pp. 349-357 Mondego, J.M., A genome survey of Moniliophthora perniciosa gives new insights into Witches’ Broom Disease of cacao (2008) BMC Genomics, 9, p. 548 Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B., Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat (2008) Methods, 5, pp. 621-628 Motamayor, J.C., The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color (2013) Genome Biol, r53, p. 14 Münch, S., Lingner, U., Floss, D.S., Ludwig, N., Sauer, N., Deising, H.B., The hemibiotrophic lifestyle of Colletotrichum species (2008) J. Plant Physiol, 165, pp. 41-51 Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., Jones, J.D., A plant miRNA contributes to antibacterial resistance by repressing auxin signaling (2006) Science, 312, pp. 436-439 O’ Brien, T.P., Feder, N., McCully, M.E., Polychromatic staining of plant cell walls by Toluidine blue O (1964) Protoplasma, 59, p. 368 Orchard, J., Collin, H.A., Hardwick, K., Isaac, S., Changes in morphology and measurement of cytokinin levels during the development of witches’ brooms on cocoa (1994) Plant Pathol, 43, pp. 65-72 Panstruga, R., Establishing compatibility between plants and obligate biotrophic pathogens (2003) Curr. Opin. Plant Biol, 6, pp. 320-326 Pazzagli, L., Seidl-Seiboth, V., Barsottini, M., Vargas, W., Scala, A., Mukherjee, P., Cerato-platanins: Elicitors and effectors (2014) Plant Sci, , http://dx.doi.org/10.1016/j.plantsci.2014.02.009 Pedersen, C., Structure and evolution of barley powdery mildew effector candidates (2012) BMC Genomics, 13, p. 694 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. Mycol (2000) Res, 104, pp. 671-675 Perfect, S.E., Green, J.R., Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol (2001) Plant Pathol, 2, pp. 101-108 Petre, B., Morin, E., Tisserant, E., Hacquard, S., Da Silva, C., Poulain, J., Delaruelle, C., Duplessis, S., RNA-Seq of early-infected poplar leaves by the rust pathogen Melampsora larici-populina uncovers PtSultr3;5, a fungal-induced host sulfate transporter (2012) PLoS ONE, 7 Pires, A.B., Gramacho, K.P., Silva, D.C., Góes-Neto, A., Silva, M.M., Muniz-Sobrinho, J.S., Porto, R.F., Pereira, G.A., Early development of Moniliophthora perniciosa basidiomata and developmentally regulated genes (2009) BMC Microbiol, 9, p. 158 Prados-Rosales, R.C., Roldán-Rodríguez, R., Serena, C., LóPez-Berges, M.S., Guarro, J., Martínez-Del-Pozo, Á., Di Pietro, A., A PR-1-like protein of Fusarium oxysporum functions in virulence on mammalian hosts (2012) J. Biol. Chem, 287, pp. 21970-21979 Pungartnik, C., Melo, S.C., Basso, T.S., Macena, W.G., Cascardo, J.C., Brendel, M., Reactive oxygen species and autophagy play a role in survival and differentiation of the phytopathogen Moniliophthora perniciosa. Fungal Genet (2009) Biol, 46, pp. 461-472 Purdy, L.H., Schmidt, R.A., Status of cacao witches’ broom: Biology, epidemiology, and management. Annu (1996) Rev. Phytopathol, 34, pp. 573-594 Ranwez, V., Harispe, S., Delsuc, F., Douzery, E.J., MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons (2011) PLoS ONE, 6 Rashotte, A.M., Carson, S.D., To, J.P., Kieber, J.J., Expression profiling of cytokinin action in Arabidopsis (2003) Plant Physiol, 132, pp. 1998-2011 Reich, M., Liefeld, T., Gould, J., Lerner, J., Tamayo, P., Mesirov, J.P., GenePattern 2.0. Nat (2006) Genet, 38, pp. 500-501 Rincones, J., Differential gene expression between the biotrophic-like and saprotrophic mycelia of the witches’ broom pathogen Moniliophthora perniciosa. Mol (2008) Plant Microbe Interact, 21, pp. 891-908 Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: A Bioconductor package for differential expression analysis of digital gene expression data (2010) Bioinformatics, 26, pp. 139-140 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 Skibbe, D.S., Doehlemann, G., Fernandes, J., Walbot, V., Maize tumors caused by Ustilago maydis require organspecific genes in host and pathogen (2010) Science, 328, pp. 89-92 Stergiopoulos, I., De Wit, P.J., Fungal effector proteins. Annu (2009) Rev. Phytopathol, 47, pp. 233-263 Studholme, D.J., Glover, R.H., Boonham, N., Application of high-throughput DNA sequencing in phytopathology. Annu (2011) Rev. Phytopathol, 49, pp. 87-105 Teixeira, P.J., Thomazella, D.P., Vidal, R.O., Do Prado, P.F., Reis, O., Baroni, R.M., Franco, S.F., Mondego, J.M., The fungal pathogen Moniliophthora perniciosa has genes similar to plant PR-1 that are highly expressed during its interaction with cacao (2012) PLoS ONE, 7 Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Stitt, M., MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J, 37, pp. 914-939 Thomazella, 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, 194, pp. 1025-1034 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 Tierney, L., Linde, J., Müller, S., Brunke, S., Molina, J.C., Hube, B., Schöck, U., Kuchler, K., An interspecies regulatory network inferred from simultaneous RNA-seq of Candida albicans invading innate immune cells. Front (2012) Microbiol, 3, p. 85 Vargas, W.A., Martín, J.M., Rech, G.E., Rivera, L.P., Benito, E.P., Díaz-Mínguez, J.M., Thon, M.R., Sukno, S.A., Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize (2012) Plant Physiol, 158, pp. 1342-1358 Volodarsky, D., Leviatan, N., Otcheretianski, A., Fluhr, R., HORMONOMETER: A tool for discerning transcript signatures of hormone action in the Arabidopsis transcriptome (2009) Plant Physiol, 150, pp. 1796-1805 Walters, D.R., McRoberts, N., Plants and biotrophs: A pivotal role for cytokinins? (2006) Trends Plant Sci, 11, pp. 581-586 Wang, D., Pajerowska-Mukhtar, K., Culler, A.H., Dong, X., Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway (2007) Curr. Biol, 17, pp. 1784-1790 Wäspi, U., Schweizer, P., Dudler, R., Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew (2001) Plant Cell, 13, pp. 153-161 Weßling, R., Schmidt, S.M., Micali, C.O., Knaust, F., Reinhardt, R., Neumann, U., Ver Loren Van Themaat, E., Panstruga, R., Transcriptome analysis of enriched Golovinomyces orontii haustoria by deep 454 pyrosequencing. Fungal Genet (2012) Biol, 49, pp. 470-482 Westermann, A.J., Gorski, S.A., Vogel, J., Dual RNA-seq of pathogen and host. Nat (2012) Rev. Microbiol, 10, pp. 618-630 Wise, R.P., Moscou, M.J., Bogdanove, A.J., Whitham, S.A., Transcript profiling in host-pathogen interactions. Annu (2007) Rev. Phytopathol, 45, pp. 329-369 Xu, L., Zhu, L., Tu, L., Liu, L., Yuan, D., Jin, L., Long, L., Zhang, X., Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNASeq- dependent transcriptional analysis and histochemistry (2011) J. Exp. Bot, 62, pp. 5607-5621 Yamagishi, J., Natori, A., Tolba, M.E., Mongan, A.E., Sugimoto, C., Katayama, T., Kawashima, S., Suzuki, Y., Interactive transcriptome analysis of malaria patients and infecting Plasmodium falciparum (2014) Genome Res, 24, pp. 1433-1444 Yang, Z., PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol (2007) Evol, 24, pp. 1586-1591 Zaparoli, G., Barsottini, M.R., De Oliveira, J.F., Dyszy, F., Teixeira, P.J., Barau, J.G., Garcia, O., Dias, S.M., The crystal structure of necrosis- and ethylene-inducing protein 2 from the causal agent of cacao’s Witches’ Broom disease reveals key elements for its activity (2011) Biochemistry, 50, pp. 9901-9910 Zhang, X.W., Jia, L.J., Zhang, Y., Jiang, G., Li, X., Zhang, D., Tang, W.H., In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles (2012) Plant Cell, 24, pp. 5159-5176 Zuccaro, A., Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica (2011) PLoS Pathog, 7