Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Journal of Plant Protection Research

The Journal of Polish Society of Plant Protection, Committee of Plant Protection; Polish Academy of Sciences, Institute of Plant Protection – National Research Institute

4 Issues per year

CiteScore 2016: 0.84

SCImago Journal Rank (SJR) 2016: 0.332
Source Normalized Impact per Paper (SNIP) 2016: 0.829

Open Access
See all formats and pricing
More options …
Volume 56, Issue 2


Co-occurrence of pathogenic and non-pathogenic Fusarium decemcellulare and Lasiodiplodia theobromae isolates in cushion galls disease of cacao (Theobroma cacao L.)

Daynet Sosa del Castillo
  • Institute for Advanced Studies (IDEA), Laboratory of Phytopathology, Caracas, 17606, Venezuela
  • Biotechnology Research Center of Ecuador, Faculty of Life Sciences, Polytechnic School of the Coast (CIBE-ESPOL), Guayaquil, Guayas, 090112, Ecuador
  • Faculty of Engineering, Milagro State University (UNEMI), Milagro, Guayas, 091050, Ecuador
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Dercy Parra
  • Miranda Experimental Station, National Institute of Agricultural Research (INIA), Tapipa, Miranda State, 1246, Venezuela
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Carlos Noceda
  • Cellular and Molecular Plant Biotechnology (BIOCEMP)/Industrial Biotechnology, Department of Life and Agricultural Sciences, University of Armed Forces-ESPE. Av. General Rumiñahui s/n. Sangolquí, P.O. Box 171-5-231B, Ecuador
  • Faculty of Engineering, Milagro State University (UNEMI), Milagro, Guayas, 091050, Ecuador
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Simón Pérez-Martínez
  • Corresponding author
  • Institute for Advanced Studies (IDEA), Laboratory of Phytopathology, Caracas, 17606, Venezuela
  • Faculty of Engineering, Milagro State University (UNEMI), Milagro, Guayas, 091050, Ecuador: present address
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2016-07-08 | DOI: https://doi.org/10.1515/jppr-2016-0020


Flowery cushion gall of cacao is a disease complex with six types. Fusarium decemcellulare have been isolated from both flowery and green point galls and recognized as the etiological agent of the disease. In the present work we: i) identified by ITS-rDNA sequencing and/or taxonomy the cultivable fungal species or Operative Taxonomic Units (OTUs) associated with the five symptoms of cushion galls in cacao from Venezuela, and ii) determined the gall inducing capacity on cacao peeled seeds after 45 days of inoculation with suspensions of mycelia/ spores from distinct isolate types. The whole isolate collection rendered an abundance of 113 isolates with a richness of 39 OTUs (27) and eight identified at the species or genera levels, respectively, and in unidentified fungi. The dominant recovered species (≈36%) were F. decemcellulare and Lasiodiplodia theobromae. Some isolates of F. decemcellulare, L. theobromae, F. equiseti, Fusarium spp., F. solani, F. incarnatum, Rhizocthonia solani and Penicillium sp. were pathogenic. Some other isolates of the first six mentioned taxa behave as non-pathogenic. Furthermore, pathogenic and non-pathogenic isolates can also co-occur within a single plant and gall type. Moreover, 2-5 species within a single gall symptom in a single tree were identified (not necessarily at the same point in the tree), indicating a broad diversity of co-occurring taxa.

Keywords: endophytic fungi; Fusarium decemcellulare; gall disease complex; Lasiodiplodia theobromae; mycobiota; Theobroma cacao


  • Agrios G.N. 2005. Plant Pathology. Elsevier, Academic Press, USA, 952 pp.Google Scholar

  • Alexander J.V., Cook R.J. 1965. Especies de Fusarium y Calonectria asociadas con la buda del cacao en Centro América. [Fusarium species and Calonectria associated with cushion gall of cacao in Central America]. Cacao (Costa Rica) 10 (1): 16-17. (in Spanish)Google Scholar

  • Arnold A.E., Herre E.A. 2003. Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95 (3): 388-398.CrossrefGoogle Scholar

  • Arnold A.E., Maynard Z., Gilbert G.S., Coley P.D., Kursar T.A. 2000. Are tropical fungal endophytes hyperdiverse? Ecology Letters 3 (4): 267-274.CrossrefGoogle Scholar

  • Arnold A.E., Mejía L.C., Kyllo D., Rojas E.I., Maynard Z., Robbins N., Herre E.A. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences of the United States of America 100 (26): 15649-15654.Google Scholar

  • Arzanlou M., Bakhshi M., Karimi K., Torbati M. 2015. Multigene phylogeny reveals three new records of Colletotrichum spp. and several new host records for the mycobiota of Iran. Journal of Plant Protection Research 55 (2): 198-211.Google Scholar

  • Bourret J.A., Ford E.J. 1965. Distribución de la Calonectria rigidiuscula y otras especies de Fusarium relacionadas con la buba del cacao. [Distribution of Calonectria rigidiuscula and other Fusarium species in relations to cushion gall of cacao]. Cacao (Costa Rica) 10: 13-15. (in Spanish)Google Scholar

  • Brenes O.E., Enríquez G.A. 1982. Buba del cacao, antecedentes y datos de investigaciones en Turrialba, Costa Rica. [Buba of cacao, background and research data in Turrialba, Costa Rica]. El Cacaotero Colombiano 22: 29-38. (in Spanish)Google Scholar

  • Brunt A.A., Wharton A.L. 1960. Transmission of gall disease of cocoa. Nature 187 (4731): 80-81.Google Scholar

  • Crozier J., Thomas S.E., Aime M.C., Evans H.C., Holmes K.A. 2006. Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathology 55 (6): 783-791.CrossrefGoogle Scholar

  • Evans H.C., Holmes K.A., Thomas S.E. 2003. Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycological Progress 2 (2): 149-160.CrossrefGoogle Scholar

  • Farr D.F., Rossman A.Y. 2015. Fungal Databases. Systematic Mycology and Microbiology Laboratory, ARS, USDA. Available on: http://nt.ars-grin.gov/fungaldatabases/. [Accessed: October 30, 2015]Google Scholar

  • Frison E.A., Feliu E. 1989. FAO/IBPGR Technical Guidelines for the Safe Movement of Cocoa Germplasm. FAO-IBPGR, Rome, 29 pp.Google Scholar

  • Gregory P.H. 1977. Una vista de las enfermedades del cacao [A view of cocoa diseases]. In: Proceeding of 6ta Conferencia Internacional de Investigaciones del Cacao. [Proccedings of 6th International Cocoa Research Conference], Caracas, Venezuela, 6-12 November 1977, 20 pp. (in Spanish)Google Scholar

  • Hanada R.E., Pomella A.W.V., Costa H.S., Bezerra J.L., Loguercio L.L., Pereira J.O. 2010. Endophytic fungal diversity in Theobroma cacao (cacao) and T. grandiflorum (cupuacu) trees and their potential for growth promotion and biocontrol of black-pod disease. Fungal Biology 114 (11-12): 901-910.Web of ScienceGoogle Scholar

  • Hansen A.J. 1963. The role of Fusarium decemcellulare and Fusarium roseum in the greenpoint cushion gall complex of cacao. Revista Turrialba 13 (2): 80-87.Google Scholar

  • Hansen A.J., Capriles de Reyes L. 1963. Agalla de puntos verdes en el cacao de Venezuela y Costa Rica. [Green point galls on cacao of Venezuela and Costa Rica]. Revista Turrialba 13 (2): 128-130. (in Spanish)Google Scholar

  • Herre E.A., Mejía L.C., Kyllo D.A., Rojas E., Maynard Z., Butler A., Bael S.A. van. 2007. Ecological implications of antipathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 88 (3): 550-558.CrossrefWeb of ScienceGoogle Scholar

  • Hutchins L.M., Siller L.R., Hansen A.J. 1959. Diseases and their control: Cushion gall. Research Annual Report of CATIE 1958. Cacao (Costa Rica) 4: 6-10.Google Scholar

  • Jamali S., Nasimi Z. 2014. First report of black-foot disease, caused by Cylindrocarpon destructans, on ornamental marigold (Tagetes minuta) in Iran. Journal of Plant Protection Research 54 (3): 139-143.Google Scholar

  • Kembel S.W., Mueller R.C. 2014. Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92 (4): 303-311.CrossrefWeb of ScienceGoogle Scholar

  • Matlick B.K., Purdy L.H., Stevenson C. 1999. Technical Support to Haitian Cacao. Productive land use system (PLUS) Haití. South East Consortium for International Development (SECID) and Auburn University. SECID/Auburn PLUS Report No. 48. USAID/Haiti Economic Growth Office, 40 pp.Google Scholar

  • Mejía L.C., Herre E.A., Sparks J.P., Winter K., García M.N., Bael S.A. van, Stitt J., Shi Z., Zhang Y., Guiltinan M.J., Maximova S.N. 2014. Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Frontiers in Microbiology 5 (479): 1-16.Web of ScienceGoogle Scholar

  • Mejía L.C., Rojas E.I., Maynard Z., Bael S. van, Arnold A.E., Hebbar P., Samuels G.J., Robbins N., Herre E.A. 2008. Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Control 46 (1): 4-14.CrossrefWeb of ScienceGoogle Scholar

  • Morales-Rondón V., Rodríguez-González M. 2006. Hongos endofitos en plantaciones de mango `Haden’ de la planicie de Maracaibo, Venezuela. [Endophytes fungi in mango ‘Haden’ orchards of Maracaibo plain, Venezuela]. Revista de la Facultad de Agronomía (LUZ) 23 (3): 273-283. (in Spanish)Google Scholar

  • Owen H. 1956. Further observations on the pathogenicity of Calonectria rigidiuscula (Berk. & Br.) Sacc. to Thebroma cacao L. Annals of Applied Biology 44 (2): 307-321.CrossrefGoogle Scholar

  • Parra D., Pérez-Martínez S., Sosa D., Rumbos R., Gutiérrez- -Cedeño B.J., Moya A. 2009. Avances en las investigaciones venezolanas sobre enfermedades del cacao. [Advances in venezuelan researches on cacao diseases]. Revista de Estudios Transdisciplinarios 1 (2): 56-75. (in Spanish)Google Scholar

  • Pérez L., Martínez E., Cantillo T. 2012. Primer reporte en Cuba de la agalla de punto verde del cacao causada por Albonectria rigidiuscula (Fusarium decemcellulare Brick). [First report in Cuba of green point gall of cocoa cushion caused by Albonectria rigidiuscula (Fusarium decemcellulare Brick)]. Fitosanidad 16 (1): 19-25. (in Spanish)Google Scholar

  • Phillips-Mora W., Cerda R. 2009. Catálogo de enfermedades del cacao en Centroamérica. [Catalog Cacao Diseases in Central America]. Technical series. Technical Manual no. 93. Tropical Agricultural Research and Higher Education Center (CATIE), Turrialba, Costa Rica, 24 pp. (in Spanish)Google Scholar

  • Ploetz R.C. 2007a. Diseases of tropical perennial crops: challenging problems in diverse environments. Plant Disease 91 (6): 644-663.CrossrefWeb of ScienceGoogle Scholar

  • Ploetz R.C. 2007b. Cacao diseases: important threats to chocolate production worldwide. Phytopathology 97 (12): 1634-1639.Web of ScienceCrossrefGoogle Scholar

  • Rai M., Agarkar G. 2014. Plant-fungal interactions: what triggers the fungi to switch among lifestyles? Critical Reviews in Microbiology 42 (3): 428-438.Web of ScienceGoogle Scholar

  • Rodriguez R.J., Jr White J.F., Arnold A.E., Redman R.S. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182 (2): 314-330.CrossrefWeb of ScienceGoogle Scholar

  • Rubini M.R., Silva-Ribeiro R.T., Pomella A.W.V., Maki C.S., Araújo W.L., dos Santos D.R., Azevedo J.L. 2005. Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. International Journal of Biological Sciences 1 (1): 24-33.CrossrefGoogle Scholar

  • Sabah Department of Agriculture 1972. Annual Report of the Department of Agriculture, Sabah. For the year 1970. Kota Kinabalu, Sabah, Malasya, 142 pp.Google Scholar

  • Saikkonen K., Faeth S.H., Helander M., Sullivan T.J. 1998. Fungal endophytes:a continuum of interactions with host plants. Annual Review of Ecology and Systematics 29: 319-343.CrossrefGoogle Scholar

  • Salas A. 1962. Manchas necróticas en hojas de plantas adultas de cacao (Theobroma cacao L.) causadas por Rhizoctonia sp. [Leaf necrotic spots on adult cacao plants (Theobroma cacao L.) caused by Rhizoctonia sp.]. Turrialba 12 (2): 93-95. (in Spanish)Google Scholar

  • White T.J., Bruns T., Lee S., Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. p. 315-322. In: “PCR Protocols: A Guide to Methods and Applications” (M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White, eds.). Academic Press, New York, USA, 482 pp. Google Scholar

About the article

Received: 2015-10-31

Accepted: 2016-04-21

Published Online: 2016-07-08

Published in Print: 2016-04-01

Citation Information: Journal of Plant Protection Research, Volume 56, Issue 2, Pages 129–138, ISSN (Online) 1899-007X, DOI: https://doi.org/10.1515/jppr-2016-0020.

Export Citation

© by Simón Pérez-Martínez. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License. BY-NC-ND 4.0

Comments (0)

Please log in or register to comment.
Log in