Advertisement

Tree Genetics & Genomes

, 15:11 | Cite as

Genetic identity and origin of “Piura Porcelana”—a fine-flavored traditional variety of cacao (Theoborma cacao) from the Peruvian Amazon

  • Enrique Arevalo-Gardini
  • Lyndel W. Meinhardt
  • Luis C. Zuñiga
  • Juan Arévalo-Gardni
  • Lambert Motilal
  • Dapeng ZhangEmail author
Original Article
Part of the following topical collections:
  1. Germplasm Diversity

Abstract

Cacao (Theobroma cacao L.) is a tropical rainforest tree that is indigenous to the Amazon region of South America. The myriad of river basins present in the Upper Amazon are where the largest diversity of cacao populations is found. Although it is generally accepted that cacao was first cultivated in Mesoamerica, there is evidence for domestication in South America, the center of origin. “Piura Porcelana” is a traditional cacao variety from northern Peru that is cultivated for the gourmet chocolate market. The demand for fine-flavored cacao used in high-end chocolates and the corresponding premium prices paid for distinct cacao flavors provide economic incentives for the use and conservation of these traditional varieties. In the present study, we compared the genetic identity of Piura Porcelana cacao with 11 known cacao germplasm groups existing in the ex situ cacao genebanks, along with the living wild populations from the Santiago and Morona river valleys in northern Peru. The results of SNP analysis showed that Piura Porcelana shares the same general population membership with the “Nacional” cacao from Ecuador. However, Piura Porcelana significantly differed from Nacional (Fst = 0.185, P < 0.001), suggesting its unique genetic status. The high genetic similarity between Piura Porcelana and newly collected wild cacao suggested that the wild progenitors of Pirua Porcelana were from these river valleys, and this traditional variety could have been the result of independent domestication in northern Peru. These results provide new evidence of cacao domestication in the Amazon and will contribute to the sustainable use and conservation of these cacao genetic resources.

Keywords

Cacao Nacional SNP markers Peruvian Amazon Chocolate 

Abbreviations

SNP

Single-nucleotide polymorphism

DNA

Deoxyribonucleic acid

SSR

Simple sequence repeat

RNase A

Ribonuclease I or ribonucleate 3′-pyrimidinooligonucleotidohydrolase

PCR

Polymerase chain reaction

IFC

Integrated fluidic circuit

PCoA

Principle coordinate analysis

STA

Specific target amplification

Notes

Acknowledgements

Authors would like to acknowledge Rey Loor Solorzano, Wilberth Phillips-Mora, and Brian Irish for supplying the samples. Authors also express appreciation to Stephen Pinney for SNP genotyping and Sue Mischke for reviewing and editing this manuscript. 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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

All row data for the Peruvian germplasm and the reference trees are being submitted to the International Cacao germplasm Database (http://www.icgd.rdg.ac.uk/).

Supplementary material

11295_2019_1316_MOESM1_ESM.docx (21 kb)
ESM 1 (DOCX 21 kb)

References

  1. Argout X, Fouet O, Wincker P, Gramacho K, Legavre T, Sabau X, Risterucci A, da Silva C, Cascardo J, Allegre M, Kuhn D, Verica J, Courtois B, Loor G, Babin R, Sounigo O, Ducamp M, Guiltinan MJ, Ruiz M, Alemanno L, Machado R, Phillips W, Schnell R, Gilmour M, Rosenquist E, Butler D, Maximova S, Lanaud C (2008) Towards the understanding of the cocoa transcriptome: production and analysis of an exhaustive dataset of ESTs of Theobroma cacao L. generated from various tissues and under various conditions. BMC Genomics 9:512CrossRefGoogle Scholar
  2. Argout X, Salse J, Aury JM, Guiltinan M et al (2011) The genome of Theobroma cacao. Nat Genet 43:101–109CrossRefGoogle Scholar
  3. Barrau J (1979) Sur l’origine du cacaoyer, Theobroma cacao Linne, Sterculiacées. J d’Agr Trad Bot Applied 26:171–180Google Scholar
  4. Bartley BGD (2005) The genetic diversity of cacao and its utilization. CAB international, CABI Publishing, WallingfordCrossRefGoogle Scholar
  5. Cheesman EE (1944) Notes on the nomenclature, classification and possible relationships of cocoa populations. Trop Agric 21:144–159Google Scholar
  6. Clement CR, de Cristo-Araújo M, d’Eeckenbrugge GC, Pereira AA, Picanço-Rodrigues D (2010) Origin and domestication of native Amazonian crops. Diversity 2:72–106.  https://doi.org/10.3390/d2010072 CrossRefGoogle Scholar
  7. Coe SD, Coe MD (1996) The true history of chocolate. Thames & Hudson, LondonGoogle Scholar
  8. Cuatrecasas J (1964) Cacao & its allies, a taxonomic revision of the genus Theobroma. In Contributions From The United States National Herbarium, Washington, DC: Smithsonian Institution 35: 379–614Google Scholar
  9. 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
  10. 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
  11. 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):481–487CrossRefGoogle Scholar
  12. Felsenstein J (1989) PHYLIP-phylogeny inference package (version 3.2). Cladistics 5:164–166Google Scholar
  13. 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
  14. Gómez-Pompa A, Flores JS, Fernandez MA (1990) The sacred cacao groves of the Maya. Lat Am Antiq 1:247–257CrossRefGoogle Scholar
  15. Henderson JS, Joyce RA, Hall GR, Hurst WJ, McGovern PE (2007) Chemical and archaeological evidence for the earliest cacao beverages. Proc Natl Acad Sci 104:18937–18940CrossRefGoogle Scholar
  16. Ji K, Zhang DP, Motilal L, Boccara M, Lachenaud P, Meinhardt LW (2013) 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 Evol 60:441–453CrossRefGoogle Scholar
  17. Loor GR, Fouet O, Lemainque A et al. (2012) Insight into the wild origin, migration and domestication history of the fine flavour Nacional Theobroma cacao L variety from Ecuador. PLoS ONE 7: e48438.  https://doi.org/10.1371/journal.pone.0048438
  18. Lukman L, Zhang D, 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 7:133–143Google Scholar
  19. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Motilal L, 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 Resour-Charact Util 8:106–110 Google Scholar
  21. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II Gene frequency data. J Mol Evol 19(1983):153–170CrossRefGoogle Scholar
  22. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  23. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  24. Pound FJ (1945) A note on the cocoa population of South America. In Report and Proceedings of the 1945 Cocoa Conference, London, U.K., pp. 131–133Google Scholar
  25. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  26. Rambaut A (2009) Molecular evolution, phylogenetics and epidemiology: FigTree v1.3.1 2006–2009. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 14 April 2017
  27. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedPubMedCentralGoogle Scholar
  28. Turnbull CJ, Hadley P (2016) International Cocoa Germplasm Database (ICGD). [Online Database]. UK: CRA Ltd./ICE Futures Europe/University of Reading, Available at http://www.icgd.reading.ac.uk. Accessed 15 May 2017
  29. 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 10:561CrossRefGoogle Scholar
  30. Wood GAR (1985) History and development. In: Wood GAR, Lass RA (eds) Cocoa, 4th edn. Blackwell Science, Oxford, pp 1–10Google Scholar
  31. Zarrillo S, Gaikwad N, Lanaud C et al. (2018) The use and domestication of Theobroma cacao during the mid-Holocene in the upper Amazon. Nature Ecology & Evolution 2:1879-1888Google Scholar
  32. Zhang D, Motilal L (2016) Origin, dispersal and current global distribution of cacao genetic diversity. In: Bailey BA, Meinhardt LW (eds) Cacao diseases: a history of old enemies and new encounters. Springer, Cham, pp 3–31Google Scholar
  33. Zhang D, Boccara M, Motilal L, Mischke S, Johnson ES, Butler DR, Bailey B, Meinhardt LW (2009a) Molecular characterization of an earliest cacao (Theobroma cacao L) collection from Peruvian Amazon using microsatellite DNA markers. Tree Genet Genomes 5:595–607CrossRefGoogle Scholar
  34. Zhang D, Mischke BS, Johnson ES, Mora A, Phillips-Mora W, Meinhardt LW (2009b) Molecular characterization of an international cacao collection using microsatellite markers. Tree Genet Genomics 5:1–10CrossRefGoogle Scholar
  35. Zhang D, Mischke S, Meinhardt LW (2012) Genetic diversity and spatial structure in a new distinct Theobroma cacao L. population in Bolivia. Genet Resour Crop Evol 59:239–252Google Scholar

Copyright information

© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019

Authors and Affiliations

  • Enrique Arevalo-Gardini
    • 1
  • Lyndel W. Meinhardt
    • 2
  • Luis C. Zuñiga
    • 1
  • Juan Arévalo-Gardni
    • 1
  • Lambert Motilal
    • 3
  • Dapeng Zhang
    • 2
    Email author
  1. 1.Instituto de Cultivos Tropicales (ICT)TarapotoPeru
  2. 2.USDA/ARSSustainable Perennial Crops LaboratoryBeltsvilleUSA
  3. 3.Cocoa Research CentreThe University of the West IndiesSt. AugustineTrinidad & Tobago

Personalised recommendations