Abstract
Cacao is an economically important commodity in Jamaica. Knowledge of the genetic diversity of Jamaican cacao germplasm is essential for their conservation and management. In spite of cacao’s economic importance in Jamaica, the crop is under studied, therefore limiting sound decisions toward improving productivity. Assessment of germplasm and on-farm genetic diversity is required to assist selecting superior genotypes to propagate and distribute across the island, as well as to use them as parental clones in breeding programs. Using 94 single nucleotide polymorphism (SNP) markers, 140 Jamaican cacao samples from two germplasm collections and a farmer’s estate along with 150 reference samples were analyzed. The principal coordinate analysis demonstrated that the majority of the Jamaican cacao selections were hybrids derived from five original germplasm groups, including Criollo, Amelonado and three Upper Amazon Forastero groups. Among the Upper Amazon groups, the Bayesian clustering analysis revealed that the Parinari (PA) ancestral lineage contributed the most (29.9%) to the Jamaican cacao germplasm. The germplasm collections showed greater diversity in terms of ancestral contributions compared to the farmer’s estate. However, the genetic differentiation between the three collecting sites was small (Fst = 0.036), indicating that samples collected from the three sites were derived from a common pool of germplasm. The current study supports the historical records and clarified the ancestry of Jamaican cacao. Although the majority of the cacao genetic groups were observed in the Jamaican cacao collections, several diversity gaps were found in both germplasm collections and in the farmer’s estate, especially germplasm with disease resistance to cacao frosty pod rot that was recently found in Jamaica.
Similar content being viewed by others
Abbreviations
- cDNA:
-
Complementary DNA
- DNA:
-
Deoxyribonucleic acid
- EST:
-
Expressed sequence tag
- PCR:
-
Polymerase chain reaction
- SNP:
-
Single nucleotide polymorphism
- TARS:
-
Tropical Agriculture Research Station
- USDA ARS:
-
United States Department of Agriculture, Agricultural Research Service
References
Aikpokpodion PO (2010) Variation in agro-morphological characteristics of cacao, Theobroma cacao L., in farmers' fields in Nigeria. J Crop Horticultural Sci 38(2):157–170. https://doi.org/10.1080/0028825X.2010.488786
Aikpokpodion PO (2012) Defining genetic diversity in the chocolate tree, Theobroma cacaol. grown in West and Central Africa. Genetic Diversity in Plants. ISBN: 978–953–51-0185-7, InTech, doi: https://doi.org/10.5772/33101
Alverson WS, Whitlock BA, Nyffeler R, Bayer C, Baum DA (1999) Phylogeny of the core Malvales: evidence from ndhF sequence data. Am J Bot 86:1474–1486
Argout X, Fouet O, Wincker P, Gramacho K et al. (2008) Towards the understanding of thecocoa transcriptome: production and analysis of an exhaustive dataset of ESTs of Theobroma cacao L. generated from various tissues and under various conditions. BMC Genomics 9:512
Argout X, Salse J, Aury JM, Guiltinan M et al (2011) The genome of Theobroma cacao. Nat Genet 43:101–109
Bartley BGD (2005) The genetic diversity of cacao and its utilization. CAB International, CABI Publishing, Wallingford
Becker H (1999) CACAO-good for agriculture and the environment. Agricultural Res Mag 47(11):2–2
Beckett ST (2000) The science of chocolate. The royal society of chemistry, London
Bekele, FL, Iwaro AD, Butler DR, Bidaisee GG (2008) Upper amazon forastero cacao (Theobroma cacao L.) 2: An overview of parinari clones from a breeder’s perspective
Boza EJ, Irish BM, Meerow AW, Tondo CL, Rodríguez OA, Ventura-López M, Gómez JA, Moore JM, Zhang D, Motamayor JC, Schnell RJ (2013) Genetic diversity, conservation, and utilization of Theobroma cacao L: genetic resources in the Dominican Republic. Genet Resour Crop Evol 60:605–619
Coe SD, Coe MD (1996) The true history of chocolate. Thames & Hudson, London
Cosme S, Cuevas HE, Zhang D, Oleksyk TK, Irish BM (2016) Genetic diversity of naturalized cacao (Theobroma cacao L.) in Puerto Rico. Tree Genet Genomes 12(5):88. https://doi.org/10.1007/s11295-016-1045-4
Deheuvels O, Decazy B, Perez R, Roch G, Amores F (2004) The first Ecuadorean ‘Nacional’ cocoa collection based on organoleptic characteristics. Trop Sci 44:23–27
Dias LAS (2001) Origin and distribution of Theobroma cacao L.: a new scenario. In: Dias LAS (ed) Genetic improvement of cacao. FAO. http://ecoport.org/ep?SearchType=earticleView&earticleId=197&page=−2. Accessed 25 March 2013
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169
Dinarti D, Susilo AW, Meinhardt LW, Ji K, Motilal LA, Mischke S, Zhang D (2015) Genetic diversity and parentage in farmer selections of cacao from southern Sulawesi, Indonesia revealed by microsatellite markers. Breed Sci 65(5):438–446. https://doi.org/10.1270/jsbbs.65.438
Efombagn MIB, Motamayor JC, Sounigo O, Eskes AB, Nyassé S, Cilas C et al (2008) Genetic diversity and structure of farm and GenBank accessions of cacao (Theobroma cacao L.) in Cameroon revealed by microsatellite markers. Tree Genet Genomes 4:821–831
Eskes EB, Guarda D, Garci L, Garcia P (2007) Is genetic variation for sensory traits of cocoa pulp related to fine flavor cocoa traits? INGENIC Nwsl 11:22–28
Fagan HJ (1979) Growing cocoa in Jamaica. Cocoa Industry Board, Kingston
Fagan HJ (1984) An assessment of pathological research on cocoa in Jamaica from 1950 to 1980 and current research priorities. Trop Pest Manag 30:430–439
Fagan HJ, Topper BF (1988) Agronomic research on cocoa in Jamaica 1950-1980 and current research trends. Trop Agric (Trinidad) 65:290–294
Fang WP, Meinhardt LW, Mischke S, Bellato CM, Motilal L, Zhang D (2014) Accurate determination of genetic identity for a single cacao bean, using molecular markers with a nanofluidic system, ensures cocoa authentication. J Agric Food Chem 62(2):481–487
Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164–166
Fluidigm (2013) Fluidigm® SNP genotyping analysis software user guide. Rev I1, PN 68000098, South San Francisco, CA, Fluidigm Corporation https://wwwmsciencecomau/upload/pages/fluidigmtech/fluidigm-snp-genotyping-user-guide-151112pdf. Accessed 10 July 2013
Higman BW (2008) Jamaica Food. University of the West Indies Press, Kingston
International Cocoa Organization (ICCO) (2008) ICCO document: Annual report 2007/2008. International Cocoa Organization, London U.K
ICCO (2016) Fine or flavour cocoa. http://www.icco.org/about-cocoa/fine-or-flavour-cocoa.html. Accessed 7 Sept 2016
Irish BM, Goenaga R, Zhang D, Schnell R, Brown JS, Motamayor JC (2010) Microsatellite fingerprinting of the USDA-ARS tropical agriculture Research Station cacao (L.) germplasm collection. Crop Sci 50:656–667
Jamaica Information Service (JIS) (2013) CIB reports 100% increase in cocoa production. Jamaica Information Service, Kingston http://jis.gov.jm/cib-reports-100-increase-in-cocoa-production/. Accessed 11 March 2015
Ji K, Zhang D, Motilal LA, Boccara M, Lachenaud P, Meinhardt LW (2012) Genetic diversity and parentage in farmer varieties of cacao (Theobroma cacao L.) from Honduras and Nicaragua as revealed by single nucleotide polymorphism (SNP) markers. Genet Resour Crop Ev 60:441–453
Jamaica Information Service (JIS) (2015) Cocoa industry returning to path of growth. Kingston, Jamaica http://jis.gov.jm/cocoa-industry-returning-path-growth/. Accessed 7 Sept 2016
Jamaica Information Service (JIS) (2016) Agricultural minister to spend $150 million to eradicate cocoa disease http://jis.gov.jm/agriculture-ministry-spend-150-million-eradicate-cocoa-disease/. Accessed 7 Sept 2016
Kalinowski ST, Manlove KR, Taper ML (2007) ONCOR A computer program for genetic stock identification. Department of ecology, Montana State University, Bozeman MT 59717. Available: http://www.montana.edu/kalinowski
Liendoa R, Padilla FC, Quintana A (1997) Characterization of cocoa butter extracted from Criollo cultivars of Theobroma cacao L. Food ResInt 30:727–731
Livingstone DS, Motamayor JC, Schnell RJ, Cariaga K, Freeman B, Meerow AW, Brown JS, Kuhn DN (2010) Development of single nucleotide polymorphism markers in Theobroma cacao and comparison to simple sequence repeat markers for genotyping of Cameroon clones. Mol Breed 27:93–106
Loor RG, Risterucci AM, Courtois B, Fouet O, Jeanneau M, Rosenquist E, Amores F, Vasco A, Medina M, Lanaud C (2009) Tracing the native ancestors of the modern Theobroma cacao L. population in Ecuador. Tree Genet Genomes 5:421–4733
Lukman ZD, Susilo AW, Dinarti D, Bailey B, Mischke S, Meinhardt LW (2014) Genetic identity, ancestry and parentage in farmer selections of cacao from aceh, Indonesia revealed by single nucleotide polymorphism (SNP) markers. Trop Plant Biol 7:133–143
Martínez IB, Nelson MR, Flamand MC, Bertin P (2015) Genetic diversity and population structure of anciently introduced Cuban cacao Theobroma cacao plants. Genet Resour Crop Evol 62(1):67–84
Ministry of Industry, Commerce, Agriculture and Fishers (MICAF) (2012) Agriculture minister says cocoa industry must create value-added activities. Kingston Jamaica http://www.moa.gov.jm/News/2012/2012-03-20_Agriculture_Minister_says_cocoa_industry_must_create_value-added_activities.php Accessed 11 March 2015
Mossu G (1992) Cocoa. The tropical Agriculturalist. CTA. The Macmillan Press Ltd, London
Motamayor JC, Risterucci AM, Lopez PA, Ortiz CF, Moreno A, Lanaud C (2002) Cacao domestication I: the origin of the cacao cultivated by the Mayas. Heredity 89:380–386
Motamayor JC, Risterucci AM, Heath M, Lanaud C (2003) Cacao domestication II: progenitor germplasm of the Trinitario cacao cultivar. Heredity 91:322–330
Motamayor JC, Lachenaud P, da Silva e Mota JW, Loor R, Kuhn DN, Brown JS, Schnell RJ (2008) Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PLoS One 3(10):e3311. https://doi.org/10.1371/journal.pone.0003311
Motilal LA, Zhang D, Umaharan P, Mischke S, Pinney S, Meinhardt LW (2011) Microsatellite fingerprinting in the International cocoa Genebank Trinidad: accession and plot homogeneity information for germplasm management. Plant Genet Resour 9:430–438. https://doi.org/10.1017/S147926211100058X
Padi FK, Ofori A, Takrama J, Djan E, Opoku SY, Dadzie AM, Bhattacharjee R, Motamayor JC, Zhang D (2015) The impact of SNP fingerprinting and parentage analysis on the effectiveness of variety recommendations in cacao. Tree Genet Genomes 11(3):1–14
Peakall R, Smouse PE (2006) GENALEX 6.5: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Phillips-Mora W, Castillo J, Arciniegas A, Mata A, Sánchez A, Leandro M, Astorga C, Motamayor J, Guyton B, Seguine E, Schnell R (2009) Overcoming the main limiting factors of cacao production in central America through the use of improved clones developed at CATIE. Proceedings of the 16th International cocoa research conference, COPAL; 16-21th Nov. 2009, Bali, pp 93–99
Pritchard JK, Stephens M, Donnelly P (2000) Inference population structure using multilocus genotype data. Genetics 155:945–959
Pryce M, Mitchell S, Burke A, McKenzie C, Stirling S, Ryan J, Simpson W, McGlashan D (2008) Jamaica: country report to the FAO International technical conference on plant genetic resources for food and agriculture. Kingston. URL: www.moa.gov.jm/jam/jamaica2.pdf.
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Rambaut A (2009) Molecular evolution, phylogenetics and epidemiology: FigTree v1.3.1 2006–2009: http://tree.bio.ed.ac.uk/software/figtree/
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shahzadi I, Ahmed R, Hassan A, Shah MM (2010) Optimization of DNA extraction fromseeds and fresh tissues of wild marigold (Tagetes minuta) for polymerase chain reaction analysis. Genet Mol Res 9(1):386–393
Sounigo O, Bekele F, Iwaro D, Thévenin J-M, Bidaisee G, Umaharan P, Sankar A, Sukha D, Boccara M, Butler DR, Eskes AB (2005) Description of the CFC/ICCO/IPGRI project collection. Proceedings of the 14th International cocoa research conference, October 13–17 2003, Accra, Ghana, Nigeria, Cocoa Producers’ Alliance, 21–32
Takrama J, Ji K, Meinhardt L, Mischke S, Opoku SY, Padi FK, Zhang D (2014) Verification of genetic diversity of introduced cacao germplasm in Ghana using single nucleotide polymorphism (SNP) markers. Afr J Biotechnol 13:2127–2136
Topper BF (1979) Growing cocoa in Jamaica. Cocoa Industry Board, Kingston
Urquhart DH (1957) Report on the expansion of the cocoa industry in Jamaica. Publications. Cadbury Brothers Ltd, Bournville
Vignal A, Milan D, SanCristobal M, Eggen A (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genet Sel Evol 34(3):275–306
Wang J, Lin M, Crenshaw A, Hutchinson A, Hicks B, Yeager M, Berndt S, Huang WY, Hayes RB, Chanock SJ, Jones RC, Ramakrishnan R (2009) High throughput single nucleotide polymorphism genotyping using nanofluidic dynamic arrays. BMC Genomics 10:561
Wood GAR, Lass RA (1985) Cocoa, 4th edn. Longman, London
World Cocoa Foundation (2014) http://www.worldcocoafoundation.org/wpcontent/uploads/Cocoa-Market-Update-as-of-4-1-2014.pdf Accessed 31 Aug 2016
Zhang D, Motilal L (2016) Origin, dispersal and current global distribution of cacao genetic diversity. In: Bailey BA, Meinhardt LW (eds) Cacao Diseases. Springer International Publishing, New York
Zhang D, Mischke S, Goenaga R, Hemeida AA, Saunders JA (2006) Accuracy and reliability of high-throughput microsatellite genotyping for cacao clone identification. Crop Sci 46:2084–2092
Zhang D, Mischke BS, Johnson ES, Mora A, Phillips-Mora W, Meinhardt LW (2009) Molecular characterization of an International cacao collection using microsatellite markers. Tree Genet Genomics 5:1–10
Zhang D, Gardini EA, Motilal L, Baligar V, Bailey B, Zuñiga-Cernades L et al (2011) Dissecting genetic structure in farmer selections of Theobroma cacao in the Peruvian Amazon: implications for on farm conservation and rehabilitation. Trop Plant Biol 4(2):106–116
Zhang D, Figueira A, Motilal L, Lachenaud P, Meinhardt LW (2012) Theobroma. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, plantation and ornamental crops. Springer, Berlin, pp 277–296. https://doi.org/10.1007/978-3-642-21201-7_13
Acknowledgements
We would like to give special thanks to Stephen Pinney (USDA-ARS) and Lin Zhou (Nanjing Agricultural University, China) for assistance with SNP genotyping using the nanofluidic array system. We also thank Sue Mischke (USDA-ARS) for editing the manuscript. References by USDA to a company and/or product 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. This project was supported in part by grants from The University of the West Indies, Mona Campus Research and Publications Committee and Inter-American Development Bank Multilateral Investment Fund (IDB MIF) through the Jamaica Cocoa Farmers’ Association (JCFA). Special thanks to Mr. Desmond Jadusingh owner of Bachelor’s Hall Estate who graciously accommodated the research on his farm.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest.
Additional information
Communicated by: Philippe Lashermes
Electronic supplementary material
ESM 1
(DOCX 46.0 kb)
Rights and permissions
About this article
Cite this article
Lindo, A.A., Robinson, D.E., Tennant, P.F. et al. Molecular Characterization of Cacao (Theobroma cacao) Germplasm from Jamaica Using Single Nucleotide Polymorphism (SNP) Markers. Tropical Plant Biol. 11, 93–106 (2018). https://doi.org/10.1007/s12042-018-9203-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12042-018-9203-5