Abstract
Cacao production in Brazil was severely affected by the outbreak of witches’ broom disease (WBD) in the late 1980s. WBD is caused by the basidiomycete fungus Moniliophthora perniciosa, a hemibiotrophic pathogen that displays an uncommonly long-lasting biotrophic stage during which the host cacao suffers intense morphologic alterations in the infected shoots, giving rise to “green brooms.” Two months after infection, the fungus becomes necrotrophic resulting in the necrosis and destruction of the infected tissues that turn into a “dry broom.” During the last 15 years, the knowledge of this devastating and intriguing disease has been growing due to initiatives such as the WBD genome project. By using genomics and transcriptomics as tools to obtain insights about this disease, the WBD project has been elucidating the biochemistry and physiology of both plant host and pathogen, paving the way for practical applications to combat the fungus. In this chapter we present an overview of progress in the understanding of M. perniciosa genetics and the molecular mechanisms governing WBD, provide a model for the M. perniciosa–cacao interaction, and point to new directions to fight this disease.
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References
Aime, M. C., & Phillips-Mora, W. (2005). The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycologia, 97(5), 1012–1022.
Alvim, F. C., Carolino, S. M. B., Cascardo, J. C. M., Nunes, C. C., Martinez, C. A., Otoni, W. C., & Fontes, E. P. B. (2001). Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiology, 126(3), 1042–1054.
Alvim, F. C., Mattos, E. M., Pirovani, C. P., Gramacho, K., Pungartnik, C., Brendel, M., Cascardo, J. C., & Vincentz, M. (2009). Carbon source-induced changes in the physiology of the cacao pathogen Moniliophthora perniciosa (Basidiomycetes) affect mycelial morphology and secretion of necrosis-inducing proteins. Genetics and Molecular Research, 8, 1035–1050.
Andebrhan, T., Figueira, A., Yamada, M. M., Cascardo, J. C. M., & Furtek, D. B. (1999). Molecular fingerprinting suggests two primary outbreaks of witches’ broom disease (Crinipellis perniciosa) of Theobroma cacao in Bahia, Brazil. European Journal of Plant Pathology, 105(2), 167–175.
Apel, K., & Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399.
Barau, J., Grandis, A., Carvalho, V. M., Teixeira, G. S., Zaparoli, G. H., do Rio, M. C., Rincones, J., Buckeridge, M. S., & Pereira, G. A. (2015). Apoplastic and intracellular plant sugars regulate developmental transitions in witches’ broom disease of cacao. Journal of Experimental Botany, 66, 1325–1337.
Bastos, C. N., & Evans, H. C. (1985). A new pathotype of Crinipellis perniciosa (witches’ broom disease) on solanaceous hosts. Plant Pathology, 34, 306–312.
Benitez, Y., Botella, M. A., Trapero, A., Alsalimiya, M., Caballero, J. L., Dorado, G., & Blanco, J. M. (2005). Molecular analysis of the interaction between Olea europaea and the biotrophic fungus Spilocaea oleagina. Molecular Plant Pathology, 6, 425–438.
Berger, S., Sinha, A. K., & Roitsch, T. (2007). Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. Journal of Experimental Botany, 58, 4019–4026.
Bertrand, H., Chan, B. S., & Griffiths, A. J. (1985). Insertion of a foreign nucleotide sequence into mitochondrial DNA causes senescence in Neurospora intermedia. Cell, 41, 877–884.
Bolton, M. D., & Thomma, B. P. H. J. (2008). The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiological and Molecular Plant Pathology, 72, 104–110.
Bouklas, T., & Fries, B. C. (2013). Cryptococcus neoformans constitutes an ideal model organism to unravel the contribution of cellular aging to the virulence of chronic infections. Current Opinions in Microbiology, 16(4), 391–397.
Britto, D. S., Pirovani, C. P., Andrade, B. S., Dos Santos, T. P., Pungartnik, C., Cascardo, J. C., Micheli, F., & Gesteira, A. S. (2013). Recombinant β-1,3-1,4-glucanase from Theobroma cacao impairs Moniliophthora perniciosa mycelial growth. Molecular Biology Reports, 409, 5417–5427.
Brown, G. C. (1999). Nitric oxide and mitochondrial respiration. Biochimica et Biophysica Acta, 1411, 351–369.
Buchanan-Wollaston, V. (1997). The molecular biology of leaf senescence. Journal of Experimental Botany, 8, 181–199.
Buzeli, R. A. A., Cascardo, J. C. M., Rodrigues, L. A. Z., Andrade, M. O., Almeida, R. S., Loureiro, M. E., Otoni, W. C., & Fontes, E. P. B. (2002). Tissue-specific regulation of BiP genes: a cis-acting regulatory domain is required for BiP promoter activity in plant meristems. Plant Molecular Biology, 50(4–5), 757–771.
Carvalho, L. J. C. B., Souza, C. R. B., Cascardo, J. C. M., Bloch, C., Jr., & Campos, L. (2004). Identification and characterization of a novel cassava (Manihot esculenta Crantz) clone with high free sugar content and novel starch. Plant Molecular Biology, 56(4), 643–659.
Cascardo, J. C. M., Almeida, R. W., Buzeli, R. A. A., Carolino, S. M. B., Otoni, W. C., & Fontes, E. P. B. (2000). The phosphorylation state and expression of soybean BiP isoforms are differentially regulated following abiotic stresses. Journal of Biological Chemistry, 275(19), 14494–14500.
Cascardo, J. C. M., Buzeli, R. A. A., Almeida, R. S., Otoni, W. C., & Fontes, E. P. B. (2001). Differential expression of the soybean BiP gene family. Plant Science, 160(2), 273–281.
Cascardo, J. C. M., Oliveira, L. E. M., & Alves, J. D. (1993a). Açúcares e compostos nitrogenados orgânicos na seringueira cultivada em solos com diferentes doses de gesso agrícola sob dois regimes hídricos. Revista Brasileira de Fisiologia Vegetal, 5(1), 31–34.
Cascardo, J. C. M., Oliveira, L. E. M., & Soares, A. M. (1993b). Disponibilidade de água e doses de gesso agrícola nas relações hídricas da seringueira. Revista Brasileira de Fisiologia Vegetal, 5(1), 35–40.
Ceita, G. O., Macêdo, J. N. A., Santos, T. B., Alemanno, L., Gesteira, A. S., Micheli, F., Mariano, A. C., Gramacho, K. P., Silva, D. C., Meinhardt, L. W., Mazzafera, P., Pereira, G. A. G., & Cascardo, J. M. (2007). Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Science, 173(2), 106–117.
Choudhary, V., & Schneiter, R. (2012). Pathogen-Related Yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins. Proceedings of the National Academy of Sciences USA, 109(42), 16882–16887.
Clausen, M., Kräuter, R., Schachermayr, G., Potrykus, I., & Sautter, C. (2000). Antifungal activity of a virally encoded gene in transgenic wheat. Nature Biotechnology, 18, 446–449.
da Hora, B. T., Jr., Poloni, J. F., Lopes, M. A., Dias, C. V., Gramacho, K. P., Schuster, I., Sabau, X., Cascardo, J. C., Mauro, S. M., Gesteira, A. S., Bonatto, D., & Micheli, F. (2012). Transcriptomics and systems biology analysis in identification of specific pathways involved in cacao resistance and susceptibility to witches’ broom disease. Molecular Biosystems, 8, 1507–1519.
da Silva, L. F., Dias, C. V., Cidade, L. C., Mendes, J. S., Pirovani, C. P., Alvim, F. C., Pereira, G. A. G., Aragão, F. J. L., Cascardo, J. C. M., & Costa, M. G. C. (2011). Expression of an oxalate decarboxylase impairs the necrotic effect induced by Nep1-like Protein (NLP) of Moniliophthora perniciosa in transgenic tobacco. Molecular Plant-Microbe Interactions, 24(7), 839–848.
de Almeida, D. F., Hungria, M., Guimarães, C. T., Antonio, R. V., Almeida, F. C., de Almeida, L. G. P., de Almeida, R., Alves-Gomes, J. A., Andrade, E. M., Araripe, J., et al. (2003). The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proceedings of the National Academy of Sciences USA, 100(20), 11660–11665.
de Arruda, M. C., Sepulveda, G. F., Miller, R. N., Ferreira, M. A., Santiago, D. V., Resende, M. L., Dianese, J. C., & Felipe, M. S. (2005). Crinipellis brasiliensis, a new species based on morphological and molecular data. Mycologia, 97, 1348–1361.
de O. Barsottini, M. R., de Oliveira, J. F., Adamoski, D., Teixeira, P. J., do Prado, P. F., Tiezzi, H. O., Sforça, M. L., Cassago, A., Portugal, R. V., de Oliveira, P. S., de M. Zeri, A. C., Dias, S. M., Pereira, G. A., & Ambrosio, A. L. (2013). Functional diversification of cerato-platanins in Moniliophthora perniciosa as seen by differential expression and protein function specialization. Molecular Plant Microbe Interactions, 26, 1281–1293.
de Oliveira, B. V. (2012). Vassoura-de-bruxa: caracterização de um metanol oxidase extracelular e do secretoma de Moniliophthora perniciosa. PhD Thesis. Universidade Estadual de Campinas.
de Oliveira, G. A. P., Pereira, E. G., Dias, C. V., Souza, T. L. F., Ferretti, G. D. S., Cordeiro, Y., Camillo, L. R., Cascardo, J., Almeida, F. C., Valente, A. P., & Silva, J. L. (2012a). Moniliophthora perniciosa Necrosis- and ethylene-inducing protein 2 (MpNep2) as a metastable dimer in solution: structural and functional implications. PLoS One, 7(9), e45620.
de Oliveira, B. V., Teixeira, G. S., Reis, O., Barau, J. G., Teixeira, P. J., do Rio, M. C., Domingues, R. R., Meinhardt, L. W., Paes Leme, A. F., Rincones, J., & Pereira, G. A. (2012b). A potential role for an extracellular methanol oxidase secreted by Moniliophthora perniciosa in Witches’ broom disease in cacao. Fungal Genetics and Biology, 49, 922–932.
De Vleesschauwer, D., Xu, J., & Höfte, M. (2014). Making sense of hormone-mediated defense networking: from rice to Arabidopsis. Frontiers in Plant Science, 5, 611.
Deganello, J., Leal, G. A., Jr., Rossi, M. L., Peres, L. E., & Figueira, A. (2014). Interaction of Moniliophthora perniciosa biotypes with Micro-Tom tomato: a model system to investigate the witches’ broom disease of Theobroma cacao. Plant Pathology, 63, 1251–1263.
Delgado, J. C., & Cook, A. A. (1976). Nuclear condition of the basidia, basidiospores, and mycelium of Marasmius perniciosus. Canadian Journal of Botany, 54, 66–72.
Dias, C. V., Mendes, J. S., dos Santos, A. C., Pirovani, C. P., da Silva Gesteira, A., Micheli, F., Gramacho, K. P., Hammerstone, J., Mazzafera, P., & de Mattos Cascardo, J. C. (2011). Hydrogen peroxide formation in cacao tissues infected by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Physiology and Biochemistry, 49, 917–922.
dos Santos, A. C. C., Sena, J. A. L., Santos, S. C., Dias, C. V., Pirovani, C. P., Pungartnik, C., Valle, R. R., Cascardo, J. C. M., & Vincentz, M. (2009). dsRNA-induced gene silencing in Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao. Fungal Genetics and Biology, 46(11), 825–836.
Duarte, E. A. A., Lacerda, G. V., Jr., de Oliveira, T. A. S., Brendel, M., Loguercio, L. L., & Cascardo, J. C. M. (2013). Bioprospection of bacteria and yeasts from Atlantic Rainforest soil capable of growing in crude-glycerol residues. Genetics and Molecular Research, 12(4), 4422–4433.
El Gueddari, N. E., Rauchhaus, U., Moerschbacher, B. M., & Deising, H. B. (2002). Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytologist, 156, 103–112.
Elthon, T. E., & McIntosh, L. (1987). Identification of the alternative terminal oxidase of higher plant mitochondria. Proceedings of the National Academy of Sciences USA, 84, 8399–8403.
Evans, H. C. (1978). Witches’ broom disease of cocoa (Crinipellis perniciosa) in Ecuador. Annals of Applied Biology, 89, 185–192.
Evans, H. C. (1980). Pleomorphism in Crinipellis perniciosa, causal agent of witches broom disease of cocoa. Transactions of the British Mycological Society, 74, 515–523.
Evans, H. C. (2007). Cacao diseases-the trilogy revisited. Phytopathology, 97, 1640–1643.
Evans, H. C., & Barreto, R. W. (1996). Crinipellis perniciosa: a much investigated but little understood fungus. Mycologist, 10, 58–61.
Fernandez, D., Tisserant, E., Talhinhas, P., Azinheira, H., Vieira, A., Petitot, A. S., Loureiro, A., Poulain, J., Da Silva, C., Silva Mdo, C., & Duplessis, S. (2012). 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. Molecular Plant Pathology, 13, 17–37.
Figueira, A., Lambert, S., Carpenter, D., Pires, J. L., Cascardo, J. C. M., & Romanczyk, L. (1997). The similarity of cocoa flavour of fermented seeds from fingerprinted genotypes of Theobroma cacao L. from Brazil and Malaysia. Tropical Agriculture, 74(2), 132–139.
Flament, M. H., Kebe, I., Clément, D., Pieretti, I., Risterucci, A. M., N'Goran, J. A., Cilas, C., Despréaux, D., & Lanaud, C. (2001). Genetic mapping of resistance factors to Phytophthora palmivora in cocoa. Genome, 44, 79–85.
Formighieri, E. F., Tiburcio, R. A., Armas, E. D., Medrano, F. J., Shimo, H., Carels, N., Góes-Neto, A., Cotomacci, C., Carazzolle, M. F., Sardinha-Pinto, N., Thomazella, D. P., Rincones, J., Digiampietri, L., Carraro, D. M., Azeredo-Espin, A. M., Reis, S. F., Deckmann, A. C., Gramacho, K., Gonçalves, M. S., Moura Neto, J. P., Barbosa, L. V., Meinhardt, L. W., Cascardo, J. C., & Pereira, G. A. (2008). The mitochondrial genome of the phytopathogenic basidiomycete Moniliophthora perniciosa is 109 kb in size and contains a stable integrated plasmid. Mycological Research, 112, 1136–1152.
Franco, S. F., Baroni, R. M., Carazzolle, M. F., Teixeira, P. J., Reis, O., Pereira, G. A., & Mondego, J. M. (2015). Genomic analyses and expression evaluation of thaumatin-like gene family in the cacao fungal pathogen Moniliophthora perniciosa. Biochemical and Biophysical Research Communications, 466, 629–636.
Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Nishida, I., & Watanabe, A. (2001). Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiologia Plantarum, 111, 345–352.
Galante, R. S., Taranto, A. G., Koblitz, M. G. B., Goes-Neto, A., Pirovani, C. P., Cascardo, J. C. M., Cruz, S. H., Pereira, G. A. G., & de Assisi, S. A. (2012). Purification, characterization and structural determination of chitinases produced by Moniliophthora perniciosa. Anais da Academia Brasileira de Ciências, 84(2), 469–486.
Garcia, D., Carels, N., Koop, D. M., de Sousa, L. A., de Andrade Jr, S. J., Pujade-Renaud, V., Mattos, C. R. R., & Cascardo, J. C. M. (2011). EST profiling of resistant and susceptible Hevea infected by Microcyclus ulei. Physiological and Molecular Plant Pathology, 76(2), 126–136.
Garcia, O., Macedo, J. A., Tiburcio, R., Zaparoli, G., Rincones, J., Bittencourt, L. M., Ceita, G. O., Micheli, F., Gesteira, A., Mariano, A. C., Schiavinato, M. A., Medrano, F. J., Meinhardt, L. W., Pereira, G. A., & Cascardo, J. C. (2007). Characterization of necrosis and ethylene-inducing proteins (NEP) in the basidiomycete Moniliophthora perniciosa, the causal agent of witches’ broom in Theobroma cacao. Mycological Research, 111, 443–455.
Gesteira, A. S., Micheli, F., Carels, N., Da Silva, A. C., Gramacho, K. P., Schuster, I., Macedo, J. N., Pereira, G. A., & Cascardo, J. C. (2007). Comparative analysis of expressed genes from cacao meristems infected by Moniliophthora perniciosa. Annals of Botany, 100(1), 129–140.
Gijzen, M., & Nurnberger, T. (2006). Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry, 67, 1800–1807.
Gomes, K. A., Almeida, T. C., Gesteira, A. S., Lôbo, I. P., Guimarães, A. C., de Miranda, A. B., Van Sluys, M. A., da Cruz, R. S., Cascardo, J. C., & Carels, N. (2010). ESTs from seeds to assist the selective breeding of Jatropha curcas L. for Oil and active compounds. Genomics Insights, 3, 29–56.
Griffith, G. W. (1994). The breeding biology of biotypes of the witches’ broom pathogen of cocoa, Crinipellis perniciosa. Heredity, 72, 278–289.
Griffith, G. W. (2004). Witches’ brooms and frosty pods: threats to world cacao production. Biologist, 51, 71–75.
Griffith, G. W., & Hedger, J. N. (1994). Spatial distribution of mycelia of the liana (L‐) biotype of the agaric Crinipellis perniciosa (Stahel) Singer in tropical forest. New Phytologist, 127, 243–259.
Griffiths, A. J. F. (1992). Fungal senescence. Annual Review of Genetics, 26, 351–372.
Gubler, F., Kalla, R., Roberts, J. K., & Jacobsen, J. V. (1995). Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. The Plant Cell, 7, 1879–1891.
Hedger, J., Pickering, N. V., & Aragundi, J. (1987). Variability of populations of the witches’ broom disease of cocoa (Crinipellis perniciosa). Transactions of the British Mycological Society, 88, 533–546.
James, T. (2007). Analysis of mating type locus organization and synteny in mushroom fungi: beyond model species. In J. Heitman, J. W. Kronstad, J. W. Taylor, & L. A. Casselton (Eds.), Sex in fungi: molecular determination and evolutionary implications (pp. 317–331). Washington, DC: ASM Press.
Jongebloed, U., Szederkenyi, J., Hartig, K., Schobert, C., & Komor, E. (2004). Sequence of morphological and physiological events during natural ageing and senescence of a castor bean leaf: sieve tube occlusion and carbohydrate back-up precede chlorophyll degradation. Physiologia Plantarum, 120, 338–346.
Kilaru, A., Bailey, B. A., & Hasenstein, K. H. (2007). Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves. FEMS Microbiology Letters, 274, 238–244.
Kilaru, A., & Hasenstein, K. H. (2005). Development and pathogenicity of the fungus Crinipellis perniciosa on interaction with cacao leaves. Phytopathology, 95(1), 101–107.
Kües, U., & Navarro-González, M. (2010). Mating-type orthologous genes in the primarily homothallic Moniliophthora perniciosa, the causal agent of Witches’ Broom Disease in cacao. Journal of Basic Microbiology, 50, 442–551.
Leal, G. A., Albuquerque, P. S. B., & Figueira, A. (2007). Genes differentially expressed in Theobroma cacao associated with resistance to witches’ broom disease caused by Crinipellis perniciosa. Molecular Plant Pathology, 8, 279–292.
Leal, G. A., Gomes, L. H., Albuquerque, P. S., Tavares, F. C., & Figueira, A. (2010). Searching for Moniliophthora perniciosa pathogenicity genes. Fungal Biology, 114, 842–854.
Lima, L. S., Gramacho, K. P., Pires, J. L., Clement, D., Lopes, U. V., Carels, N., Gesteira, A. S., Gaiotto, F. A., Cascardo, J. C. M., & Micheli, F. (2010). Development, characterization, validation, and mapping of SSRs derived from Theobroma cacao L.-Moniliophthora perniciosa interaction ESTs. Tree Genetics and Genomes, 6(5), 663–676.
Lin, X., & Heitman, J. (2007). Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism. In J. Heitman, J. W. Kronstad, J. W. Taylor, & L. A. Casselton (Eds.), Sex in fungi: molecular determination and evolutionary implications (pp. 35–57). Washington, DC: ASM Press.
Lozano-Torres, J. L., Wilbers, R. H., Warmerdam, S., Finkers-Tomczak, A., Diaz-Granados, A., van Schaik, C. C., Helder, J., Bakker, J., Goverse, A., Schots, A., & Smant, G. (2014). Apoplastic venom allergen-like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLoS Pathogens, 10(12), e1004569.
Marelli, J.-P., Maximova, S. N., Gramacho, K. P., Kang, S., & Guiltinan, M. J. (2009). Infection biology of Moniliophthora perniciosa on Theobroma cacao and alternate solanaceous hosts. Tropical Plant Biology, 2, 149–160.
Mason, M. G., Ross, J. J., Babst, B. A., Wienclaw, B. N., & Beveridge, C. A. (2014). Sugar demand, not auxin, is the initial regulator of apical dominance. Proceedings of the National Academy of Sciences USA, 111, 6092–6097.
Maxwell, D. P., Wang, Y., & McIntosh, L. (1999). The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences USA, 96, 8271–8276.
Meinhardt, L. W., Bellato, C. M., Rincones, J., Azevedo, R. A., Cascardo, J. C., & Pereira, G. A. (2006). In vitro production of biotrophic-like cultures of Crinipellis perniciosa, the causal agent of witches’ broom disease of Theobroma cacao. Current Microbiology, 52(3), 191–196.
Meinhardt, L. W., Costa, G. G., Thomazella, D. P., Teixeira, P. J., Carazzolle, M. F., Schuster, S. C., Carlson, J. E., Guiltinan, M. J., Mieczkowski, P., Farmer, A., Ramaraj, T., Crozier, J., Davis, R. E., Shao, J., Melnick, R. L., Pereira, G. A., & Bailey, B. A. (2014). 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. BMC Genomics, 15, 164.
Meinhardt, L. W., Rincones, J., Bailey, B. A., Aime, M. C., Griffith, G. W., Zhang, D., & Pereira, G. A. (2008). Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: what’s new from this old foe? Molecular Plant Pathology, 9, 577–588.
Melnick, R. L., Marelli, J. P., Sicher, R. C., Strem, M. D., & Bailey, B. A. (2012). The interaction of Theobroma cacao and Moniliophthora perniciosa, the causal agent of witches’ broom disease, during parthenocarpy. Tree Genetics and Genomes, 8, 1261–1279.
Menezes, S. P., de Andrade Silva, E. M., Matos Lima, E., Oliveira de Sousa, A., Silva Andrade, B., Santos Lima Lemos, L., Peres Gramacho, K., da Silva Gesteira, A., Pirovani, C. P., & Micheli, F. (2014). The pathogenesis-related protein PR-4b from Theobroma cacao presents RNase activity, Ca(2+) and Mg(2+) dependent-DNase activity and antifungal action on Moniliophthora perniciosa. BMC Plant Biology, 14, 161.
Micheli, F., Guiltinan, M. J., Gramacho, K. P., Wilkinson, M. J., Figueira, A., Cascardo, J. C. M., Maximova, S., & Lanaud, C. (2010). Functional genomics of cacao. Advances in Botanical Research, 55, 119–177.
Mondego, J. M., Carazzolle, M. F., Costa, G. G., Formighieri, E. F., Parizzi, L. P., Rincones, J., Cotomacci, C., Carraro, D. M., Cunha, A. F., Carrer, H., Vidal, R. O., Estrela, R. C., García, O., Thomazella, D. P., de Oliveira, B. V., Pires, A. B., Rio, M. C., Araújo, M. R., de Moraes, M. H., Castro, L. A., Gramacho, K. P., Gonçalves, M. S., Neto, J. P., Neto, A. G., Barbosa, L. V., Guiltinan, M. J., Bailey, B. A., Meinhardt, L. W., Cascardo, J. C., & Pereira, G. A. (2008). A genome survey of Moniliophthora perniciosa gives new insights into Witches’ Broom Disease of cacao. BMC Genomics, 9, 548.
Monzani, P., Pereira, H. M., Melo, F. A., Meirelles, F. V., Oliva, G., & Cascardo, J. C. M. (2010). A new topology of ACBP from Moniliophthora perniciosa. Biochimica et Biophysica Acta-Proteins and Proteomics, 1804(1), 115–123.
Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., & Jones, J. D. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436–439.
Ni, M., Feretzaki, M., Sun, S., Wang, X., & Heitman, J. (2011). Sex in fungi. Annual Review of Genetics, 45, 405–430.
Orchard, J., Collin, H. A., Hardwick, K., & Isaac, S. (1994). Changes in morphology and measurement of cytokinin levels during the development of witches’ brooms on cocoa. Plant Pathology, 43, 65–72.
Pereira, J. F., Almeida, A. P., Cota, J., Pamphile, J. A., da Silva, G. F., de Araújo, E. F., Gramacho, K. P., Brommonschenkel, S. H., Pereira, G. A., & de Queiroz, M. V. (2013). Boto, a class II transposon in Moniliophthora perniciosa, is the first representative of the PIF/Harbinger superfamily in a phytopathogenic fungus. Microbiology, 159, 112–125.
Pereira, J. F., Araújo, E. F., Brommonschenkel, S. H., Queiroz, C. B., Costa, G. G., Carazzolle, M. F., Pereira, G. A., & Queiroz, M. V. (2015). MpSaci is a widespread gypsy-Ty3 retrotransposon highly represented by non-autonomous copies in the Moniliophthora perniciosa genome. Current Genetics, 61, 185–202.
Pereira, J. L., Barreto, R. W., & Bezerra, J. L. (1997). Distribuição de Crinipellis perniciosa em solanáceas selvagens no Sudeste do Brasil. Fitopatologia Brasileira, 22, 295.
Pereira, J. L., de Almeida, L. C. C., & Santos, S. M. (1996). Witches’ broom disease of cocoa in Bahia: attempts at eradication and containment. Crop Protection, 15(8), 743–752.
Pierik, R., Tholen, D., Poorter, H., Visser, E. J., & Voesenek, L. A. (2006). The Janus face of ethylene: growth inhibition and stimulation. Trends in Plant Science, 11, 176–183.
Pires, J. L., Cascardo, J. C. M., Lambert, S. V., & Figueira, A. (1998). Increasing cocoa butter yield through genetic improvement of Theobroma cacao L.: seed fat content variability, inheritance, and association with seed yield. Euphytica, 103(1), 115–121.
Pires, A. B., Gramacho, K. P., Silva, D. C., Góes-Neto, A., Silva, M. M., Muniz-Sobrinho, J. S., Porto, R. F., Villela-Dias, C., Brendel, M., Cascardo, J. C., & Pereira, G. A. (2009). Early development of Moniliophthora perniciosa basidiomata and developmentally regulated genes. BMC Microbiology, 9, 158.
Pirovani, C. P., da Silva Santiago, A., dos Santos, L. S., Micheli, F., Margis, R., da Silva Gesteira, A., Alvim, F. C., Pereira, G. A., & de Mattos Cascardo, J. C. (2010). Theobroma cacao cystatins impair Moniliophthora perniciosa mycelial growth and are involved in postponing cell death symptoms. Planta, 232, 1485–1497.
Prados-Rosales, R. C., Roldán-Rodríguez, R., Serena, C., López-Berges, M. S., Guarro, J., Martínez-del-Pozo, Á., & Di Pietro, A. (2012). A PR-1-like protein of Fusarium oxysporum functions in virulence on mammalian hosts. Journal of Biological Chemistry, 287, 21970–21979.
Pungartnik, C., da Silva, A. C., de Melo, S. A., Gramacho, K. P., de Mattos Cascardo, J. C., Brendel, M., Micheli, F., & da Silva Gesteira, A. (2009a). High-affinity copper transport and Snq2 export permease of saccharomyces cerevisiae modulate cytotoxicity of PR-10 from Theobroma cacao. Molecular Plant Microbe Interactions, 22, 39–51.
Pungartnik, C., Melo, S. C., Basso, T. S., Macena, W. G., Cascardo, J. C., & Brendel, M. (2009b). Reactive oxygen species and autophagy play a role in survival and differentiation of the phytopathogen Moniliophthora perniciosa. Fungal Genetics and Biology, 46, 461–472.
Purdy, L. H., & Schmidt, R. A. (1996). Status of cacao witches’ broom: biology, epidemiology, and management. Annual Review of Phytopathology, 34, 573–594.
Rincones, J., Scarpari, L. M., Carazzolle, M. F., Mondego, J. M. C., Formighieri, E. F., Barau, J. G., Costa, G. G. L., Carraro, D. M., Brentani, H. P., Vilas-Boas, L. A., Oliveira, B. V., Sabha, M., Dias, R., Cascardo, J. M., Azevedo, R. A., Meinhardt, L. W., & Pereira, G. A. G. (2008). Differential gene expression between the biotrophic-like and saprotrophic mycelia of the Witches' broom pathogen Moniliophthora perniciosa. Molecular Plant Microbe Interactions, 21(7), 891–908.
Rio, M. C. S., Oliveira, B. V., Thomazella, D. P., Fracassi da Silva, J. A., & Pereira, G. A. G. (2008). Production of calcium oxalate crystals by the basidiomycete Moniliophthora perniciosa, the causal agent of the Witches’ Broom Disease of cacao. Current Microbiology, 56(4), 363–370.
Rocha, H. M., & Wheeler, B. E. J. (1985). Factors influencing the production of basidiocarps and the deposition and germination of basidiospores of Crinipellis perniciosa, the causal agent of witches’ broom disease on cocoa (Theobroma cacao). Plant Pathology, 34, 319–328.
Ross, J. J., O’Neill, D. P., Smith, J. J., Kerckhoffs, L. H., & Elliott, R. C. (2000). Evidence that auxin promotes gibberellin A1 biosynthesis in pea. The Plant Journal, 21, 547–552.
Salgado, L. R., Koop, D. M., Pinheiro, D. G., Rivallan, R., Le Guen, V., Nicolás, M. F., de Almeida, L. G. P., Rocha, V. R., Magalhães, M., Gerber, A. L., Figueira, A., Cascardo, J. C. M., de Vasconcelos, A. T. R., Silva, W. A., Coutinho, L. L., & Garcia, D. (2014). De novo transcriptome analysis of Hevea brasiliensis tissues by RNA-seq and screening for molecular markers. BMC Genomics, 15, 236.
Santana, L. S., Costa, M. G., Pirovani, N. M., Almeida, A. F., Alvim, F. C., & Pirovani, C. P. (2014). TcCYS4, a cystatin from cocoa, reduces necrosis triggered by MpNEP2 in tobacco plants. Genetics and Molecular Research, 13, 7636–7648.
Santos Carvalho, H. A., Ribeiro, L. F., Pirovani, C. P., Gramacho, K. P., & Micheli, F. (2013a). Activity of polygalacturonases from Moniliophthora perniciosa depends on fungus culture conditions and is enhanced by Theobroma cacao extracts. Physiological and Molecular Plant Pathology, 83, 40–50.
Santos Carvalho, H. A., Silva, E. M., Santos, S. C., & Micheli, F. (2013b). Polygalacturonases from Moniliophthora perniciosa are regulated by fermentable carbon sources and possible post-translational modifications. Fungal Genetics and Biology, 60, 110–121.
Santos, M. C., Jr., Gonçalves, P. A., Taranto, A. G., Koblitz, M. G. B., Goes-Neto, A., Pirovani, C. P., Cascardo, J. C. M., da Cruz, S. H., Zingali, R. B., Pereira, G. A. G., Dias, C. V., & de Assis, S. A. (2011). Purification, characterization and structural determination of UDP-N-Acetylglucosamine pyrophosphorylase produced by Moniliophthora perniciosa. Journal of the Brazilian Chemical Society, 22(6), 1015–U264.
Scarpari, L. M., Meinhardt, L. W., Mazzafera, P., Pomella, A. W., Schiavinato, M. A., Cascardo, J. C., & Pereira, G. A. (2005). Biochemical changes during the development of witches’ broom: the most important disease of cocoa in Brazil caused by Crinipellis perniciosa. Journal of Experimental Botany, 56, 865–877.
Shiba, T., Kido, Y., Sakamoto, K., Inaoka, D. K., Tsuge, C., Tatsumi, R., Takahashi, G., Balogun, E. O., Nara, T., Aoki, T., Honma, T., Tanaka, A., Inoue, M., Matsuoka, S., Saimoto, H., Moore, A. L., Harada, S., & Kita, K. (2013). Structure of the trypanosome cyanide-insensitive alternative oxidase. Proceedings of the National Academy of Sciences USA, 110, 4580–4585.
Silva, S. D., Luz, E. D. M. N., Almeida, O. C., Gramacho, K., & Bezerra, J. L. (2002). Redescrição da sintomatologia causada por Crinipellis perniciosa em cacaueiro. Agrotropica, 1, 1–23.
Silva, S. D., & Matsuoka, K. (1999). Histologia da interação Crinipellis perniciosa em cacaueiros suscetível e resistente à vassoura-de-bruxa. Fitopatologia Brasileira, 24, 54–59.
Souza, C. R. B., Carvalho, L. J. C. B., & Cascardo, J. C. M. (2004). Comparative gene expression study to identify genes possibly related to storage root formation in cassava. Protein and Peptide Letters, 11(6), 577–582.
Sreenivasan, T. N., & Dabydeen, S. S. (1989). Modes of penetration of young cocoa leaves by Crinipellis perniciosa. Plant Disease, 73, 478–481.
Teixeira, P. J., Thomazella, D. P., Reis, O., do Prado, P. F., do Rio, M. C., Fiorin, G. L., José, J., Costa, G. G., Negri, V. A., Mondego, J. M., Mieczkowski, P., & Pereira, G. A. (2014). High-Resolution transcript profiling of the atypical biotrophic interaction between Theobroma cacao and the fungal pathogen Moniliophthora perniciosa. The Plant Cell, 26, 4245–4269.
Teixeira, P. J., Thomazella, D. P., Vidal, R. O., do Prado, P. F., Reis, O., Baroni, R. M., Franco, S. F., Mieczkowski, P., Pereira, G. A., & Mondego, J. M. (2012). The fungal pathogen Moniliophthora perniciosa has genes similar to plant PR-1 that are highly expressed during its interaction with cacao. PLoS One, 7(9), e45929.
Thomazella, D. P., Teixeira, P. J., Oliveira, H. C., Saviani, E. E., Rincones, J., Toni, I. M., Reis, O., Garcia, O., Meinhardt, L. W., Salgado, I., & Pereira, G. A. (2012). The hemibiotrophic cacao pathogen Moniliophthora perniciosa depends on a mitochondrial alternative oxidase for biotrophic development. New Phytologist, 194, 1025–1034.
Tiburcio, R. A., Costa, G. G., Carazzolle, M. F., Mondego, J. M., Schuster, S. C., Carlson, J. E., Guiltinan, M. J., Bailey, B. A., Mieczkowski, P., Meinhardt, L. W., & Pereira, G. A. (2010). 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. Journal of Molecular Evolution, 70(1), 85–97.
Tymowska-Lalanne, Z., & Kreis, M. (1998). Expression of the Arabidopsis thaliana invertase gene family. Planta, 207, 259–265.
Vasconcelos, A. T. R., Ferreira, H. B., Bizarro, C. V., Bonatto, S. L., Carvalho, M. O., Pinto, P. M., Almeida, D. F., Almeida, L. G. P., Almeida, R., Alves, L., Assunção, E. N., Azevedo, V. A. C., Bogo, M. R., Brigido, M. M., Brocchi, M., Burity, H. A., Camargo, A. A., Camargo, S. S., Carepo, M. S., Carraro, D. M., Cascardo, J. C. M., et al. (2005). Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. Journal of Bacteriology, 187(16), 5568–5577.
Volodarsky, D., Leviatan, N., Otcheretianski, A., & Fluhr, R. (2009). HORMONOMETER: a tool for discerning transcript signatures of hormone action in the Arabidopsis transcriptome. Plant Physiology, 150, 1796–1805.
Wang, D., Pajerowska-Mukhtar, K., Culler, A. H., & Dong, X. (2007). Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology, 17, 1784–1790.
Westermann, A. J., Gorski, S. A., & Vogel, J. (2012). Dual RNA-seq of pathogen and host. Nature Reviews Microbiology, 10, 618–630.
Wheeler, B. E. J. (1985). The growth of Crinipellis perniciosa in living and dead cocoa tissue. In D. Moore, L. A. Casselton, D. A. Wood, & J. C. Frankland (Eds.), Developmental biology of higher fungi (pp. 103–116). Cambridge: Cambridge University Press.
Wilson, R. A., Fernandez, J., Quispe, C. F., Gradnigo, J., Seng, A., Moriyama, E., & Wright, J. D. (2012). Towards defining nutrient conditions encountered by the rice blast fungus during host infection. PLoS One, 7, e47392.
Wu, L., Chen, H., Curtis, C., & Fu, Z. Q. (2014). Go in for the kill: how plants deploy effector-triggered immunity to combat pathogens. Virulence, 5, 710–721.
Zaparoli, G., Barsottini, M. R., de Oliveira, J. F., Dyszy, F., Teixeira, P. J., Barau, J. G., Garcia, O., Costa-Filho, A. J., Ambrosio, A. L., Pereira, G. A., & Dias, S. M. (2011). 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. Biochemistry, 50, 9901–9910.
Zhu, Z. (2014). Molecular basis for jasmonate and ethylene signal interactions in Arabidopsis. Journal of Experimental Botany, 65, 5743–5748.
Acknowledgments
The authors acknowledge all researchers, students, and technician involved in WBD genome project along these 15 years and Dr. Joan Barau for the discussions about M. perniciosa evolution and reproductive strategy. We also thank São Paulo Research Foundation (FAPESP) for financial support (grants 2006/53553-3; 2009/50119-9; 2009/51018-1; 2012/09136-0).
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Mondego, J.M.C., de Toledo Thomazella, D.P., Teixeira, P.J.P.L., Pereira, G.A.G. (2016). Genomics, Transcriptomics, and Beyond: The Fifteen Years of Cacao’s Witches’ Broom Disease Genome Project. In: Bailey, B., Meinhardt, L. (eds) Cacao Diseases. Springer, Cham. https://doi.org/10.1007/978-3-319-24789-2_6
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