Tree Genetics & Genomes

, Volume 9, Issue 3, pp 829–840 | Cite as

Complex origin of Trinitario-type Theobroma cacao (Malvaceae) from Trinidad and Tobago revealed using plastid genomics

  • Ji Yong Yang
  • Moira Scascitelli
  • Lambert A. Motilal
  • Saemundur Sveinsson
  • Johannes M. M. Engels
  • Nolan C. Kane
  • Hannes Dempewolf
  • Dapeng Zhang
  • Kamaldeo Maharaj
  • Quentin C. B. Cronk
Original Paper

Abstract

Trinidad and Tobago has a long history of producing high-quality cacao (Theobroma cacao L.). Cacao genotypes in Trinidad and Tobago are of a highly distinctive kind, the so-called “Trinitario” cultivar group, widely considered to be of elite quality. The origin of Trinitario cacao is unclear, although it is generally considered to be of hybrid origin. We used massive parallel sequencing to identify polymorphic plastidic single nucleotide polymorphisms (cpSNPs) and polymorphic plastidic simple sequence repeats (cpSSRs) in order to determine the origin of the Trinitario cultivar group by comparing patterns of polymorphism to a reference set of ten completely sequenced chloroplast genomes (nine T. cacao and one outgroup, T. grandiflorum (Willd. ex Spreng.) Schum). Only three cpSNP haplotypes were present in the Trinitario cultivars sampled, each highly distinctive and corresponding to reference genotypes for the Criollo (CRI), Upper Amazon Forastero (UAF) and Lower Amazon Forastero (LAF) varietal groups. These three cpSNP haplotypes likely represent the founding lineages of cacao to Trinidad and Tobago. The cpSSRs were more variable with eight haplotypes, but these clustered into three groups corresponding to the three cpSNP haplotypes. The most common haplotype found in farms of Trinidad and Tobago was LAF, followed by UAF and then CRI. We conclude that the Trinitario cultivar group is of complex hybrid origin and has derived from at least three original introduction events.

Keywords

Theobroma cacao Chloroplast Microsatellites Single nucleotide polymorphisms Trinitario 

References

  1. Arroyo-García R, Lefort F, de Andrés MT, Ibáñaez J, Borrego J, Jouve N, Cabello F, Martínez-Zapater JM (2002) Chloroplast microsatellite polymorphisms in Vitis species. Genome 45:1142–1149PubMedCrossRefGoogle Scholar
  2. Bartley BGD (2005) The genetic diversity of cacao and its utilization. CABI, Wallingford, UKCrossRefGoogle Scholar
  3. Bekele FL, Bidaisee GG, Bhola J (2007) A comparative morphological study of two Trinitario groups from the International Cocoa Genebank, Trinidad. Annual Report 2006, Cocoa Research Unit, University of the West Indies, Trinidad and Tobago, pp 34–42Google Scholar
  4. Cheesman EE (1934) The botanical programme of 1933. In Third annual report on cacao research,1933. Government Printing Office, Port-of-Spain, Trinidad, pp 1–2Google Scholar
  5. Cheesman EE (1944) Notes on the nomenclature, classification and possible relationships of cocoa populations. Trop Agric 21:144–159Google Scholar
  6. Coe SD, Coe MD (1996) The true history of chocolate. Thames and Hudson, New York, USAGoogle Scholar
  7. Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperms. Am J Bot 75:1443–1458CrossRefGoogle Scholar
  8. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  9. Engels JMM (1986) The systematic description of cacao clones and its significance for taxonomy and plant breeding. Dissertation, Agricultural University, Wageningen, Netherlands, 125pGoogle Scholar
  10. Felsenstein J (1973) Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Syst Zool 22:240–249CrossRefGoogle Scholar
  11. Felsenstein J (1989) PHYLIP — phylogeny inference package (Version 3.2). Cladistics 5:164–166Google Scholar
  12. Freeman WE (1969) Some aspects of the cacao breeding programme. Proceedings of Agricultural Society of Trinidad and Tobago, Dec 1968, pp 1–15Google Scholar
  13. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  14. Hale ML, Borland AM, Gustafsson MH, Wolff K (2004) Causes of size homoplasy among chloroplast microsatellites in closely related Clusia species. J Mol Evol 58:182–190PubMedCrossRefGoogle Scholar
  15. Huang CY, Grünheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138:1723–33PubMedCrossRefGoogle Scholar
  16. Irish BI, Goenaga R, Zhang D, Schnell R, Brown S, Motamayor JC (2010) Microsatellite fingerprinting of the USDA-ARS tropical agriculture research station cacao (Theobroma cacao L.) germplasm collection. Crop Sci 50:656–667CrossRefGoogle Scholar
  17. Jansen RK, Saski C, Lee SB, Hansen AK, Daniell H (2011) Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 28:835–847PubMedCrossRefGoogle Scholar
  18. Johnson ES, Bekele FB, Brown SJ, Song Q, Zhang D, Meinhardt LW, Schnell RJ (2009) Population structure and genetic diversity of the Trinitario cacao (Theobroma cacao L.) from Trinidad and Tobago. Crop Sci 49:564–572CrossRefGoogle Scholar
  19. Kane N, Sveinsson S, Dempewolf H, Yang JY, Zhang D, Engels JMM, Cronk Q (2012) Ultra-barcoding in cacao (Theobroma spp.; Malvaceae) using whole chloroplast genomes and nuclear ribosomal DNA. Am J Bot 99:320–329PubMedCrossRefGoogle Scholar
  20. Kim S, Lee Y-P, Lim H, Ahn Y, Sung SK (2009) Identification of highly variable chloroplast sequences and development of cpDNA-based molecular markers that distinguish four cytoplasm types in radish (Raphanus sativus L.). Theor Appl Genet 119:189–198PubMedCrossRefGoogle Scholar
  21. 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 Genetics & Genomes 5:421–433CrossRefGoogle Scholar
  22. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079PubMedCrossRefGoogle Scholar
  23. Marshall HD, Newton C, Ritland K (2002) Chloroplast phylogeography and evolution of highly polymorphic microsatellites in lodgepole pine (Pinus contorta). Theor Appl Genet 104:367–378CrossRefGoogle Scholar
  24. Matsuo M, Ito Y, Yamauchi R, Obokata J (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast–nuclear DNA flux. The Plant Cell 17:665–675PubMedCrossRefGoogle Scholar
  25. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404CrossRefGoogle Scholar
  26. 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 89:380–386PubMedCrossRefGoogle Scholar
  27. Motamayor JC, Risterucci AM, Heath M, Lanaud C (2003) Cacao domestication: II Progenitor germplasm of the Trinitario cacao cultivar. Heredity 91:322–330PubMedCrossRefGoogle Scholar
  28. Motilal LA, Zhang D, Umaharan P, Mischke S, Boccara M, Pinney S (2009) Increasing accuracy and throughput in large scale microsatellite fingerprinting of cacao field germplasm collections. Trop Plant Biol 2:23–37CrossRefGoogle Scholar
  29. Motilal LA, Zhang D, Umaharan P, Mischke S, Mooleedhar V, Meinhardt LW (2010) The relic Criollo cacao in Belize – genetic diversity and relationship with Trinitario and other cacao clones held in the International Cocoa Genebank Trinidad. Plant Genet Resource 8:106–115CrossRefGoogle Scholar
  30. 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 Resource 9:430–438CrossRefGoogle Scholar
  31. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170PubMedCrossRefGoogle Scholar
  32. Petit RJ, Vendramin GG (2007) Plant phylogeography based on organelle genes: an introduction. In: Weiss S, Ferrand N (eds) Phylogeography of Southern European refugia. Springer, Dordrecht, Netherlands, pp 23–97CrossRefGoogle Scholar
  33. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  34. Pound FJ (1931) The genetic constitution of the cacao crop. First annual report on cacao research 1931. Government Printing Office, Port of Spain, Trinidad, pp 10–24Google Scholar
  35. Pound FJ (1933) Criteria and methods of selection in cacao. In Second annual report on cacao research 1932. Government Printing Office, Port of Spain, Trinidad, pp 27–29Google Scholar
  36. Pound FJ (1934) The progress of selection, 1933. In Third annual report on cacao research 1933. Government Printing Office, Port of Spain, Trinidad, pp 25–28Google Scholar
  37. Pound FJ (1935) The progress of selection, 1934. In Fourth annual report on cacao research 1934. Government Printing Office, Port of Spain, Trinidad, pp 7–11Google Scholar
  38. Pound FJ (1936) The progress of selection, 1935. In Fifth annual report on cacao research 1934. Government Printing Office, Port of Spain, Trinidad, pp 7–16Google Scholar
  39. Powell W, Morgante M, Doyle JJ, McNicol JW, Tingey SV, Rafalski AJ (1996) Genepool variation in genus Glycine subgenus Soja revealed by polymorphic nuclear and chloroplast microsatellites. Genetics 144:793–803PubMedGoogle Scholar
  40. Provan J, Corbett G, McNicol JW, Powell W (1997) Chloroplast DNA variability in wild and cultivated rice (Oryza spp.) revealed by polymorphic chloroplast simple sequence repeats. Genome 40:104–110PubMedCrossRefGoogle Scholar
  41. Provan J, Russell JR, Booth A, Powell W (1999) Polymorphic chloroplast simple sequence repeat primers for systematic and population studies in the genus Hordeum. Mol Ecol 8:505–511PubMedCrossRefGoogle Scholar
  42. Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147PubMedCrossRefGoogle Scholar
  43. Rambaut A (2006–2009) FigTree. Tree figure drawing tool v.1.3.1, Institute of Evolutionary Biology, University of Edinburgh, UKGoogle Scholar
  44. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, New Jersey, USA, pp 365–386Google Scholar
  45. Shephard CY (1932) The cacao industry of Trinidad: some economic aspects, Part I. Government Printing office, Port of Spain, Trinidad, pp 95–100Google Scholar
  46. Silva CRS, Albuquerque PSB, Ervedosa FR, Mota JWS, Figueira A, Sebbenn AM (2010) Understanding the genetic diversity, spatial genetic structure and mating system at the hierarchical levels of fruits and individuals of a continuous Theobroma cacao population from the Brazilian Amazon. Heredity 106:973–985PubMedCrossRefGoogle Scholar
  47. Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear ADH sequences for phylogeny reconstruction of a recently diverged plant group. Am J Bot 85:1301–1315PubMedCrossRefGoogle Scholar
  48. Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571PubMedCrossRefGoogle Scholar
  49. Sveinsson S, Kane NC, Dempewolf H, Zhang D, Cronk QC (2010) Theobroma cacao chloroplast, complete genome. Website http://www.ncbi.nlm.nih.gov/nuccore/HQ244500 Accessed 15 January 2012
  50. Takayama K, Kajita T, Murata J, Yoichi T (2006) Phylogeography and genetic structure of Hibiscus tiliaceus – speciation of a pantropical plant with sea-drifted seeds. Mol Ecol 15:2871–2881PubMedCrossRefGoogle Scholar
  51. Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399PubMedGoogle Scholar
  52. Toxopeus H (1985) Botany, types and populations. In: Wood GAR, Lass RA (eds) Cocoa, 4th edn. Longman, London, pp 11–37Google Scholar
  53. Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci 86:4132–4136PubMedCrossRefGoogle Scholar
  54. Wood GAR (1985) History and development. In: Wood GAR, Lass RA (eds) Cocoa, 4th edn. Longman, London, pp 1–10Google Scholar
  55. Yang JY, Motilal LA, Dempewolf H, Maharaj K, Cronk QC (2011) Chloroplast microsatellite primers for cacao (Theobroma cacao) and other Malvaceae. Am J Bot 98:e372–374PubMedCrossRefGoogle Scholar
  56. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas at Austin, Texas, USAGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ji Yong Yang
    • 1
  • Moira Scascitelli
    • 1
  • Lambert A. Motilal
    • 2
  • Saemundur Sveinsson
    • 1
  • Johannes M. M. Engels
    • 3
  • Nolan C. Kane
    • 1
  • Hannes Dempewolf
    • 1
  • Dapeng Zhang
    • 4
  • Kamaldeo Maharaj
    • 5
  • Quentin C. B. Cronk
    • 1
  1. 1.Department of BotanyUniversity of British ColumbiaVancouverCanada
  2. 2.Cocoa Research UnitThe University of the West Indies, St. Augustine, TrinidadWest IndiesRepublic of Trinidad and Tobago
  3. 3.Biodiversity InternationalRomeItaly
  4. 4.SPCL, USDA-ARSBeltsvilleUSA
  5. 5.Ministry of Agriculture, Food Production Land, and Marine Resources AffairsCentral Experiment Station, Centeno, Via Arima P.O.West IndiesRepublic of Trinidad and Tobago

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