Moniliophthora roreri Genome and Transcriptome

  • Lyndel W. MeinhardtEmail author
  • Bryan A. Bailey


Frosty pod rot disease of cacao is one of the most destructive diseases of cacao and at this time is limited to regions in South America and Central America. Frosty pod rot is caused by a fungal pathogen Moniliophthora roreri, a basidiomycete that is closely related to another cacao pathogen that causes the witches’ broom disease, Moniliophthora perniciosa. Combined these two pathogens are the leading causes of cacao yield losses in the Americas. Both pathogens are unique in that they have long biotrophic phases after infection as the disease progresses. In this chapter, genomic and transcriptomic sequencing will be used to corroborate and hypothesize various mechanisms of the molecular interactions of the host and pathogen during the disease interaction of frosty pod rot. The systematic timing of fungal and plant gene regulation in this pathosystem appears to be a key component of this plant disease resulting in specific molecular and cellular interactions. When this coordinated gene regulation is disrupted, for example, in a resistant plant variety, the disease interaction fails.


Glycoside Hydrolase Clamp Connection Plant Cell Death Carbohydrate Esterase Acetyl Xylan Esterase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Work was funded by USDA ARS. References to a company and/or product by the USDA are only for the purposes of information and do not imply approval or recommendation of the product to the exclusion of others that may also be suitable. USDA is an equal opportunity provider and employer.


  1. Aimanianda, V., Bayry, J., Bozza, S., Kniemeyer, O., Perruccio, K., Elluru, S. R., Clavaud, C., Paris, S., Brakhage, A. A., Kaveri, S. V., Romani, L., & Latge, J. P. (2009). Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature, 460(7259), 1117–1121.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. Ali, S. S., Melnick, R. L., Crozier, J., Phillips-Mora, W., Strem, M. D., Shao, J., Zhang, D., Sicher, R., Meinhardt, L., & Bailey, B. A. (2014). Successful pod infections by Moniliophthora roreri result in differential Theobroma cacao gene expression depending on the clone’s level of tolerance. Molecular Plant Pathology, 15(7), 698–710.CrossRefPubMedGoogle Scholar
  4. Ali, S. S., Shao, J., Strem, M. D., Phillips-Mora, W., Zhang, D., Meinhardt, L., & Bailey, B. (2015). Combination of RNAseq and SNP nanofluidic array reveals the center of genetic diversity of cacao pathogen Moniliophthora roreri in the upper Magdalena Valley of Colombia and its clonality. Frontiers in Microbiology, 6, 850.PubMedCentralCrossRefPubMedGoogle Scholar
  5. Bailey, B. A., Crozier, J., Sicher, R. C., Strem, M. D., Melnick, R., Carazzolle, M. F., Costa, G. G. L., Pereira, G. A. G., Zhang, D. P., Maximova, S., Guiltinan, M., & Meinhardt, L. (2013). Dynamic changes in pod and fungal physiology associated with the shift from biotrophy to necrotrophy during the infection of Theobroma cacao by Moniliophthora roreri. Physiological and Molecular Plant Pathology, 81, 84–96.CrossRefGoogle Scholar
  6. Bailey, B. A., Melnick, R. L., Strem, M. D., Crozier, J., Shao, J., Sicher, R., Phillips-Mora, W., Ali, S. S., Zhang, D., & Meinhardt, L. (2014). Differential gene expression by Moniliophthora roreri while overcoming cacao tolerance in the field. Molecular Plant Pathology, 15(7), 711–729.CrossRefPubMedGoogle Scholar
  7. Barsottini, M. R. D., de Oliveira, J. F., Adamoski, D., Teixeira, P. J. P. L., do Prado, P. F. V., Tiezzi, H. O., Sforca, M. L., Cassago, A., Portugal, R. V., de de Oliveira, P. S. L., Zeri, A. C. D., Dias, S. M. G., Pereira, G. A. G., & Ambrosio, A. L. B. (2013). Functional diversification of cerato-platanins in Moniliophthora perniciosa as seen by differential expression and protein function specialization. Molecular Plant-Microbe Interactions, 26(11), 1281–1293.CrossRefGoogle Scholar
  8. Bayry, J., Aimanianda, V., Guijarro, J. I., Sunde, M., & Latge, J. P. (2012). Hydrophobins – unique fungal proteins. PLoS Pathog, 8(5), e1002700.PubMedCentralCrossRefPubMedGoogle Scholar
  9. Bowman, S. M., & Free, S. J. (2006). The structure and synthesis of the fungal cell wall. Bioessays, 28(8), 799–808.CrossRefPubMedGoogle Scholar
  10. Cabrera, O. G., Zaparoli, G., Medrano, F. J., Tiburcio, R. A., Lacerda, G. G., & Pereira, G. G. (2008). Functional and structural characterization of cerato-platanin proteins in Moniliophthora perniciosa, the cause of Witches’ Broom disease in cacao. Phytopathology, 98(6), S29.Google Scholar
  11. Calle, H., Cook, A. A., & Fernando, S. Y. (1982). A histological study of Witches' broom in cocoa, caused by Crinipellis perniciosa. Phytopathology, 72, 1479–1481.CrossRefGoogle Scholar
  12. Carmona-Gutierrez, D., Frohlich, K. U., Kroemer, G., & Madeo, F. (2010). Metacaspases are caspases. Doubt no more. Cell Death and Differentiation, 17(3), 377–378.CrossRefPubMedGoogle Scholar
  13. Ceita, G. D., Macedo, J. N. A., Santos, T. B., Alemanno, L., Gesteira, A. D., Micheli, F., Mariano, A. C., Gramacho, K. P., Silva, D. D., Meinhardt, L., Mazzafera, P., Pereira, G. A. G., & Cascardo, J. C. D. (2007). Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora pemiciosa. Plant Science, 173(2), 106–117.CrossRefGoogle Scholar
  14. Chen, W., Lee, M. K., Jefcoate, C., Kim, S. C., Chen, F., & Yu, J. H. (2014). Fungal cytochrome p450 monooxygenases: Their distribution, structure, functions, family expansion, and evolutionary origin. Genome Biology and Evolution, 6(7), 1620–1634.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Ciferri, R., & Parodi, E. (1933). Descrizione del fungo che causa la “Moniliasi” del cacao. Phytopathologische Zeitschrift-Journal of Phytopathology, 5, 539–542.Google Scholar
  16. Costa, G. G., Cabrera, O. G., Tiburcio, R. A., Medrano, F. J., Carazzolle, M. F., Thomazella, D. P., Schuster, S. C., Carlson, J. E., Guiltinan, M. J., Bailey, B. A., Mieczkowski, P., Pereira, G. A., & Meinhardt, L. W. (2012). The mitochondrial genome of Moniliophthora roreri, the frosty pod rot pathogen of cacao. Fungal Biology, 116(5), 551–562.CrossRefPubMedGoogle Scholar
  17. Daskalov, A., Paoletti, M., Ness, F., & Saupe, S. J. (2012). Genomic clustering and homology between HET-S and the NWD2 STAND protein in various fungal genomes. PLos One, 7(4), e34854.PubMedCentralCrossRefPubMedGoogle Scholar
  18. Davies, G. Glycoside hydrolase family 5. In CAZypedia. Accessed January 8, 2015, from
  19. Davies, G., Juge, N., & Eijsink, V. Glycoside hydrolase family 18. In CAZypedia. Accessed January 8, 2015, from
  20. 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. (2012). Moniliophthora perniciosa necrosis- and ethylene-inducing protein 2 (MpNep2) as a metastable dimer in solution: Structural and functional implications. PLos One, 7(9).Google Scholar
  21. Desrosiers, R., & Suárez, C. (1974). Monilia pod rot of cacao. London: Longman.Google Scholar
  22. do Rio, M. C. S., de Oliveira, B. V., de Tomazella, D. P. T., da Silva, J. A. F., & Pereira, G. A. G. (2008). Production of calcium oxalate crystals by the basidiomycete Moniliophthora perniciosa, the causal agent of Witches’ Broom disease of cacao. Current Microbiology, 56(4), 363–370.CrossRefPubMedGoogle Scholar
  23. Durner, J., & Klessig, D. F. (1995). Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proceedings of the National Academy of Sciences of the United States of America, 92(24), 11312–11316.PubMedCentralCrossRefPubMedGoogle Scholar
  24. Eklöf, J., & Hehemann, J.-H. Glycoside hydrolase family 16. In CAZypedia. Accessed January 8, 2015, from
  25. Evans, H. C. (1980). Pleomorphism in Crinipellis perniciosa, causal agent of Witches’ broom disease of cocoa. Transactions of the British Mycology Society, 74, 515–526.CrossRefGoogle Scholar
  26. Evans, H. C. (1981). Pod rot of cacao caused by Moniliophthora (Monilia) roreri. London: Commonwealth Agricultural Bureau.Google Scholar
  27. Evans, H. C. (1986). A re-assessment of Moniliophthora (Monilia) pod rot of cocoa. Cocoa Growers’ Bulletin, 37, 34–43.Google Scholar
  28. Evans, H. C., Holmes, K. A., Phillips, W., & Wilkinson, M. J. (2002). What's in a name: Crinipellis, the final resting place for the frosty pod rot pathogen of cocoa? Mycologist, 16, 148–152.Google Scholar
  29. Evans, H. C., Stalpers, J. A., Samson, R. A., & Benny, G. L. (1978). Taxonomy of Monilia-roreri, an important pathogen of Theobroma-cacao in South-America. Canadian Journal of Botany-Revue Canadienne De Botanique, 56(20), 2528–2532.Google Scholar
  30. Formighieri, E. F., Tiburcio, R. A., Armas, E. D., Medrano, F. J., Shimo, H., Carels, N., Goes-Neto, A., Cotomacci, C., Carazzolle, M. F., Sardinha-Pinto, N., Thomazella, D. P. T., Rincones, J., Digiampietri, L., Carraro, D. M., Azeredo-Espin, A. M., Reis, S. F., Deckmann, A. C., Gramacho, K., Goncalves, M. S., Neto, J. P. M., Barbosa, L. V., Meinhardt, L. W., Cascardo, J. C. M., & Pereira, G. A. G. (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.CrossRefPubMedGoogle Scholar
  31. Fournier, E., & Giraud, T. (2008). Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. Journal of Evolutionary Biology, 21(1), 122–132.PubMedGoogle Scholar
  32. Frias, G. A., Purdy, L. H., & Schmidt, R. A. (1991). Infection biology of Crinipellis-perniciosa on vegetative flushes of cacao. Plant Disease, 75(6), 552–556.CrossRefGoogle Scholar
  33. Garcia, O., Macedo, J. A. N., Tiburcio, R., Zaparoli, G., Rincones, J., Bittencourt, L. M. C., Ceita, G. O., Micheli, F., Gesteira, A., Mariano, A. C., Schiavinato, M. A., Medrano, F. J., Meinhardt, L. W., Pereira, G. A. G., & Cascardo, J. C. M. (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.CrossRefPubMedGoogle Scholar
  34. Giraud, T., Refregier, G., Le Gac, M., de Vienne, D. M., & Hood, M. E. (2008). Speciation in fungi. Fungal Genetics and Biology, 45(6), 791–802.CrossRefPubMedGoogle Scholar
  35. Hammel, K. E., Mozuch, M. D., Jensen, K. A., & Kersten, P. J. (1994). H2O2 recycling during oxidation of the arylglycerol beta-aryl ether lignin structure by lignin peroxidase and glyoxal oxidase. Biochemistry, 33(45), 13349–13354.CrossRefPubMedGoogle Scholar
  36. Harper, D. B., Buswell, J. A., Kennedy, J. T., & Hamilton, J. T. (1990). Chloromethane, Methyl Donor in Veratryl Alcohol Biosynthesis in Phanerochaete chrysosporium and Other Lignin-Degrading Fungi. Applied and Environmental Microbiology, 56(11), 3450–3457.PubMedCentralPubMedGoogle Scholar
  37. Harper, D. B., & Hamilton, J. T. G. (1988). Biosynthesis of chloromethane in Phellinus-pomaceus. Journal of General Microbiology, 134, 2831–2839.Google Scholar
  38. Harper, D. B., Kennedy, J. T., & Hamilton, J. T. G. (1988). Chloromethane biosynthesis in poroid fungi. Phytochemistry, 27(10), 3147–3153.CrossRefGoogle Scholar
  39. Hernandez-Ortega, A., Ferreira, P., & Martinez, A. T. (2012). Fungal aryl-alcohol oxidase: A peroxide-producing flavoenzyme involved in lignin degradation. Applied Microbiology and Biotechnology, 93(4), 1395–1410.CrossRefPubMedGoogle Scholar
  40. Hofrichter, M., Ullrich, R., Pecyna, M. J., Liers, C., & Lundell, T. (2010). New and classic families of secreted fungal heme peroxidases. Applied Microbiology and Biotechnology, 87(3), 871–897.CrossRefPubMedGoogle Scholar
  41. Holliday, P. (1957). Spread of pod rot of cacao. Commonwealth Phytopathological News, 3(1), 12.Google Scholar
  42. Holliday, P. (1971). Some tropical plant pathogenic fungi of limited distribution. Review of Plant Pathology, 50, 337–348.Google Scholar
  43. Holliday, P. (1980). Fungus diseases of tropical crops. New York: Dover Inc.Google Scholar
  44. Idnurm, A., & Howlett, B. J. (2002). Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryotic Cell, 1(5), 719–724.PubMedCentralCrossRefPubMedGoogle Scholar
  45. Iimura, Y., & Tatsumi, K. (1997). Isolation of mRNAs induced by a hazardous chemical in white-rot fungus, Coriolus versicolor, by differential display. FEBS Letters, 412(2), 370–374.CrossRefPubMedGoogle Scholar
  46. Kersten, P. J. (1990). Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proceedings of the National Academy of Sciences of the United States of America, 87(8), 2936–2940.PubMedCentralCrossRefPubMedGoogle Scholar
  47. Kim, S., Ahn, I. P., Rho, H. S., & Lee, Y. H. (2005). MHP1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Molecular Microbiology, 57 (5), 1224–1237.CrossRefPubMedGoogle Scholar
  48. Kleman-Leyer, K. M., Siika-Aho, M., Teeri, T. T., & Kirk, T. K. (1996). The cellulases Endoglucanase I and Cellobiohydrolase II of Trichoderma reesei act synergistically to solubilize native cotton cellulose but not to decrease its molecular size. Applied and Environmental Microbiology, 62(8), 2883–2887.PubMedCentralPubMedGoogle Scholar
  49. Kothe, E. (2008). Sexual attraction: On the role of fungal pheromone/receptor systems (A review). Acta Microbiologica et Immunologica Hungarica, 55(2), 125–143.CrossRefPubMedGoogle Scholar
  50. Lacourt, I., Duplessis, S., Abba, S., Bonfante, P., & Martin, F. (2002). Isolation and characterization of differentially expressed genes in the mycelium and fruit body of Tuber borchii. Applied and Environmental Microbiology, 68(9), 4574–4582.PubMedCentralCrossRefPubMedGoogle Scholar
  51. Lazan, H., Ng, S. Y., Goh, L. Y., & Ali, Z. M. (2004). Papaya beta-galactosidase/galactanase isoforms in differential cell wall hydrolysis and fruit softening during ripening. Plant Physiology and Biochemistry, 42(11), 847–853.CrossRefPubMedGoogle Scholar
  52. Liu, J. J., Sturrock, R., & Ekramoddoullah, A. K. (2010). The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Reports, 29(5), 419–436.CrossRefPubMedGoogle Scholar
  53. Maddison, A. C., Macias, G., Moreira, C., Arias, R., & Neira, R. (1995). Cocoa production in Ecuador in relation to dry-season escape from pod rot caused by Crinipellis perniciosa and Moniliophthora roreri. Plant Pathology, 44(6), 982–998.CrossRefGoogle Scholar
  54. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  55. 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(5), 577–588.CrossRefPubMedGoogle Scholar
  56. 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., Garcia, O., Thomazella, D. P., de Oliveira, B. V., Pires, A. B., Rio, M. C., Araujo, M. R., de Moraes, M. H., Castro, L. A., Gramacho, K. P., Goncalves, 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.PubMedCentralCrossRefPubMedGoogle Scholar
  57. Morisseau, C. (2013). Role of epoxide hydrolases in lipid metabolism. Biochimie, 95(1), 91–95.PubMedCentralCrossRefPubMedGoogle Scholar
  58. Paoletti, M., & Clave, C. (2007). The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryotic Cell, 6(11), 2001–2008.PubMedCentralCrossRefPubMedGoogle Scholar
  59. Perfect, S. E., & Green, J. R. (2001). Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Molecular Plant Pathology, 2(2), 101–108.CrossRefPubMedGoogle Scholar
  60. Phillips-Mora, W. (2003).Origin, biogeography, genetic diversity and taxonomic affinities of the cacao (Theobroma cacao L.) fungus Moniliophthora roreri (Cif.) Evans et al. as determined using molecular, phytopathological and morpho-physiological evidence. In Department of Agricultural Botany, School of Plant Sciences, Vol. Doctor of Philosophy, 349. Reading: University of Reading.Google Scholar
  61. Phillips-Mora, W., Aime, M. C., & Wilkinson, M. J. (2007). Biodiversity and biogeography of the cacao (Theobroma cacao) pathogen Moniliophthora roreri in tropical America. Plant Pathology, 56(6), 911–922.CrossRefGoogle Scholar
  62. Phillips-Mora, W., Cawich, J., Garnett, W., & Aime, M. C. (2006a). First report of frosty pod rot (moniliasis disease) caused by Moniliophthora roreri on cacao in Belize. Plant Pathology, 55 (4), 584.Google Scholar
  63. Phillips-Mora, W., Coutino, A., Ortiz, C. F., Lopez, A. P., Hernandez, J., & Aime, M. C. (2006b). First report of Moniliophthora roreri causing frosty pod rot (moniliasis disease) of cocoa in Mexico. Plant Pathology, 55(4), 584.Google Scholar
  64. Pickersgill, R. Glycoside hydrolase family 28. In CAZypedia. Accessed January 8, 2015, from
  65. Pinot, F., Caldas, E. D., Schmidt, C., Gilchrist, D. G., Jones, A. D., Winter, C. K., & Hammock, B. D. (1997). Characterization of epoxide hydrolase activity in Alternaria alternata f. sp. lycopersici. Possible involvement in toxin production. Mycopathologia, 140(1), 51–58.CrossRefPubMedGoogle Scholar
  66. Popiel, D., Koczyk, G., Dawidziuk, A., Gromadzka, K., Blaszczyk, L., & Chelkowski, J. (2014). Zearalenone lactonohydrolase activity in Hypocreales and its evolutionary relationships within the epoxide hydrolase subset of a/b-hydrolases. BMC Microbiology, 14.Google Scholar
  67. Rabe, F., Ajami-Rashidi, Z., Doehlemann, G., Kahmann, R., & Djamei, A. (2013). Degradation of the plant defence hormone salicylic acid by the biotrophic fungus Ustilago maydis. Molecular Microbiology, 89(1), 179–188.CrossRefPubMedGoogle Scholar
  68. Rondon Carvajal, J. G. (1993). Cocoa genetic resources in Colombia. In: Proceedings of the International Workshop on Conservation, Characterisation and Utilisation of Cocoa Genetics Resources in the 21st Century (pp. 371–378). UWI, Trinidad: CRU.Google Scholar
  69. Rorer, J. B. (1918). Enfermedadas y plagas del cacao en el Ecuador y métodos modernos aprpiados al cultivo del cacao. Quayaquil: Ecudaor Asociación e Agricultores.Google Scholar
  70. Saupe, S. J., Clave, C., & Begueret, J. (2000). Vegetative incompatibility in filamentous fungi: Podospora and Neurospora provide some clues. Current Opinion in Microbiology, 3(6), 608–612.CrossRefPubMedGoogle Scholar
  71. Saupe, S. J., & Daskalov, A. (2012). The [Het-s] prion, an amyloid fold as a cell death activation trigger. PLoS Pathogens, 8(5), e1002687.PubMedCentralCrossRefPubMedGoogle Scholar
  72. Schlumberger, S., Kristan, K. C., Ota, K., Frangez, R., Molgomicron, J., Sepcic, K., Benoit, E., & Macek, P. (2014). Permeability characteristics of cell-membrane pores induced by ostreolysin A/pleurotolysin B, binary pore-forming proteins from the oyster mushroom. FEBS Letters, 588 (1), 35–40.CrossRefPubMedGoogle Scholar
  73. Song, G., Cheng, C., Li, Y., Shaw, N., Xiao, Z. C., & Liu, Z. J. (2014). Crystal structure of the N-terminal methyltransferase-like domain of anamorsin. Proteins, 82(6), 1066–1071.CrossRefPubMedGoogle Scholar
  74. Suárez, C. (1971).Estudio del mecanismo de penetración v del processo de infección de Monilia roreri Cif. Par. en frutos de cacao (Theobroma cacao L.). In Facultad de Agronomia y Veterinaria, Vol. Ing. Agr., 59 Guayaquil, Ecuador: Universidad de Guayaquil.Google Scholar
  75. Talbot, N. J., Kershaw, M. J., Wakley, G. E., De Vries, O., Wessels, J., & Hamer, J. E. (1996). MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell, 8(6), 985–999.PubMedCentralCrossRefPubMedGoogle Scholar
  76. Teixeira, P. J., Thomazella, D. P., Reis, O., do Prado, P. F., do Rio, M. C., Fiorin, G. L., Jose, 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. Plant Cell, 26(11), 4245–4269.PubMedCentralCrossRefPubMedGoogle Scholar
  77. Teixeira, P. J. P. L., Thomazella, D. P. T., Vidal, R. O., do Prado, P. F. V., Reis, O., Baroni, R. M., Franco, S. F., Mieczkowski, P., Pereira, G. A. G., & Mondego, J. M. C. (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).Google Scholar
  78. ten Have, R., & Teunissen, P. J. (2001). Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chemical Reviews, 101(11), 3397–3413.CrossRefPubMedGoogle Scholar
  79. Tiburcio, R. A., Costa, G. G. L., Carazzolle, M. F., Mondego, J. M. C., Schuster, S. C., Carlson, J. E., Guiltinan, M. J., Bailey, B. A., Mieczkowski, P., Meinhardt, L. W., & Pereira, G. A. G. (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.CrossRefPubMedGoogle Scholar
  80. Turnbull, C. J. & Hadley, P. (2015). International Cocoa Germplasm Database (ICGD). CRU Ltd/NYSE Liffe/University of Reading.Google Scholar
  81. van den Brink, J., & de Vries, R. P. (2011). Fungal enzymes sets for plant polysaccharide degradation. Applied Microbiology and Biotechnology, 91(6), 1477–1492.PubMedCentralCrossRefPubMedGoogle Scholar
  82. van Hall, C. J. (1914). Cocoa. London: Macmillan.Google Scholar
  83. Wessels, J., De Vries, O., Asgeirsdottir, S. A., & Schuren, F. (1991). Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell, 3(8), 793–799.PubMedCentralCrossRefPubMedGoogle Scholar
  84. Williams, S. Glycoside hydolase family 76. In CAZypedia. Accessed January 8, 2015, from
  85. Wright, G. D., & Sutherland, A. D. (2007). New strategies for combating multidrug-resistant bacteria. Trends in Molecular Medicine, 13(6), 260–267.CrossRefPubMedGoogle Scholar
  86. Yang, D. D., Francois, J. M., & de Billerbeck, G. M. (2012). Cloning, expression and characterization of an aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium strain BKM-F-1767. BMC Microbiology, 12, 126.PubMedCentralCrossRefPubMedGoogle Scholar
  87. Zhang, J., Siika-Aho, M., Tenkanen, M., & Viikari, L. (2011). The role of acetyl xylan esterase in the solubilization of xylan and enzymatic hydrolysis of wheat straw and giant reed. Biotechnology for Biofuels, 4(1), 60.PubMedCentralCrossRefPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Sustainable Perennial Crops Laboratory, United States Department of AgricultureAgricultural Research ServiceBeltsvilleUSA

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