Evolution, genetics, and diversity of cacao

Theobroma cacao, the source of chocolate, cocoa, and cocoa butter, is one of the world’s most valuable crops.  Despite its economic importance, there have been relatively few evolutionary studies of cacao compared to other crops.

The goal of this website is to promote comparative studies of cacao and its wild relatives.  Below is a bibliography of literature relevant to the genetics, diversity and evolution of cacao. This is still a work in progress - no doubt many important and interesting papers are still missing.  Any suggestions or additions will be much appreciated and can be sent to Barbara Whitlock.

 

Phylogenetics of Theobroma and relatives

Borrone, JW, AW Meerow, DN Kuhn, BA Whitlock, RJ Schnell. 2007. The potential of the WRKY gene family for phylogenetic reconstruction: An example from the Malvaceae. MOLECULAR PHYLOGENETICS AND EVOLUTION 44: 1141-1154.

Carvalho, MR, FA Herrera, CA Jaramillo, et al. 2011. Paleocene Malvaceae from northern South America and their biogeographical implications. AMERICAN JOURNAL OF BOTANY 98: 1337-1355.

Silva, CRS, and A Figueira.  2005.  Phylogenetic analysis of Theobroma (Sterculiaceae) based on Kunitz-like trypsin inhibitor sequences.  PLANT SYSTEMATICS AND EVOLUTION 250: 93-104.

Whitlock, BA, and DA Baum.  1999.  Phylogenetic relationships of Theobroma and Herrania (Sterculiaceae) based on sequences of the nuclear gene vicilin.  SYSTEMATIC BOTANY 24: 128-138.

Whitlock, BA, C Bayer, and DA Baum.  2001.  Phylogenetic relationships and floral evolution of the Byttnerioideae ("Sterculiaceae" or Malvaceae s.l.) based on sequences of the chloroplast gene, ndhF.  SYSTEMATIC BOTANY 26: 420-437.

Genetic diversity of Theobroma cacao

Alves, RM, AM Sebbenn, AS Artero, and A Figueira.  2006.  Microsatellite loci transferability from Theobroma cacao to Theobroma grandiflorum.  MOLECULAR ECOLOGY NOTES 6: 1219-1221.

Bartley, BGD.  2005.  The genetic diversity of cacao and its utilization.  Oxford University Press (CABI Publishing), Oxford, UK.

Borrone, JW, DN Kuhn, and RJ Schnell.  2004.  Isolation, characterization, and development of WRKY genes as useful genetic markers in Theobroma cacao.  THEORETICAL AND APPLIED GENETICS 109: 495-507.

de la Cruz, M, R Whitkus, A Gómez-Pompa, and L Mota-Bravo.  1995.  Origins of cacao cultivation.  NATURE 375: 542-543.

Dias, LAD, JP Barriga, PY Kageyama, et al.  2003.  Variation and its distribution in wild cacao populations from the Brazilian Amazon.  BRAZILIAN ARCHIVES OF BIOLOGY AND TECHNOLOGY 46: 507-514.

Dias, LAD, J Marita, CD Cruz CD, et al.  2003. Genetic distance and its association with heterosis in cacao.  BRAZILIAN ARCHIVES OF BIOLOGY AND TECHNOLOGY 46: 339-347.

Figueira, A, J Janick, and PB Goldsbrough.  1992.  Characterization of the genes for ribosomal DNA polymorphism in Theobroma cacao.  JOURNAL OF THE AMERICAN SOCIETY FOR HORTICULTURAL SCIENCE 117: 673-677.

Figueira, A, J Janick, M Levy, and P Goldsbrough.  1994.  Re-examining the classification of theobroma cacao L. using molecular markers.  JOURNAL OF THE AMERICAN SOCIETY FOR HORTICULTURAL SCIENCE 119: 1073-1082.

Laurent, V, A-M Risterucci, and C Lanaud.  1993.  Variability for nuclear ribosomal genes within Theobroma cacao.  HEREDITY 71: 96-103.

Lerceteau, E, D Crouzillat, and V Petiard.  1992.  Use of random amplified polymorphic DNA (RAPD) and restriction length polymorphism (RFLP) to evaluate genetic variability within the Theobroma genus.  INTERNATIONAL COCOA GENETIC RESOURCE WORKSHOP, PORT-OF-SPAIN, TRINIDAD AND TOBAGO, 13-17 Sept. 1992.

Lopez, CMR, AC Wetten, and MJ Wilkinson.  2004.  Detection and quantification of in vitro-culture induced chimerism using simple sequence repeat (SSR) analysis in Theobroma cacao (L.).  THEORETICAL AND APPLIED GENETICS 110: 157-166.

Motamayor, JC, AM Risterucci, PA Lopez, et al.  2002.  Cacao domestication I: the origin of the cacao cultivated by the Mayas.  HEREDITY 89: 380-386.

Motamayor, JC, AM Risterucci, M Heath, et al.  2003.  Cacao domestication II: progenitor germplasm of the Trinitario cacao cultivar.  HEREDITY 91: 322-330.

Motilal, L, D Butler.  2003.  Verification of identities in global cacao germplasm collections.  GENETIC RESOURCES AND CROP EVOLUTION 50: 799-807.

Russell, JR, F Hosein, E Johnson, R Waugh, and W Powell.  1993.  Genetic differentiation of cocoa (Theobroma cacao L.) populations revealed by RAPD analysis.  MOLECULAR ECOLOGY 2: 89-97.

Saunders, JA, S Mischke,  EA Leamy, et al.  2004.  Selection of international molecular standards for DNA fingerprinting of Theobroma cacao.  THEORETICAL AND APPLIED GENETICS 110: 41-47.

Sereno, ML, PSB Albuquerque, R Vencovsky, and A Figueira.  2006.  Genetic diversity and natural population structure of cacao (Theobroma cacao L.) from the Brazilian amazon evaluated by microsatellite markers.  CONSERVATION GENETICS 7: 13-24.

Wilde, J, R Waugh, and W Powell.  1992.  Genetic fingerprinting of Theobroma clones using randomly amplified polymorphic DNA markers.  THEORETICAL AND APPLIED GENETICS 83: 871-877.

Trognitz, B, X Scheldeman, K Hansel-Hohl, et al. 2011. Genetic population structure of cacao plantings within a young production area in Nicaragua. PLOS ONE 6: e16056.

Zhang, DP, S Mischke, R Goenaga, AA Hemeida, and JA Saunders.  2006.  Accuracy and reliability of high-throughput microsatellite genotyping for cacao clone identification. CROP SCIENCE 46: 2084-2092.

Zhang, DP, E Arevalo-Gardini, S Mischke, L Zuniga-Cernades, A Barreto-Chavez, and JA Del Aguila.  2006.  Genetic diversity and structure of managed and semi-natural populations of cocoa (Theobroma cacao) in the Huallaga and Ucayali valleys of Peru.  ANNALS OF BOTANY 98: 647-655.

Floral morphology, development, and pollination biology of Theobroma and relatives

Bayer, C.  1994.  Zur infloreszenzmorphologie der Malvales.  DISSERTATIONES BOTANICAE 212: 1-280.

Bayer, C, and JR Hoppe.  1990.  Die Blütenentwicklung von Theobroma cacao L. (Sterculiaceae).  Beiträge zur Biologie der Pflanzen 65: 301-312.

Chaidamsari, T, Samanhudi, H Sugiarti, D Santoso, GC Angenent, and RA de Maagd.  2006.  Isolation and characterization of an AGAMOUS homologue from cocoa.  PLANT SCIENCE 170: 968-975.

Erickson, BJ, AM Young, MA Strand, and EH Erickson Jr.  1987.  Polination biology of Theobroma and Herrania (Sterculiaceae): II.  Analyses of floral oils.  INSECT SCIENCE AND ITS APPLICATION 8: 301-310.

Jenny, M.  1988.  Different gynoecium types in Sterculiaceae: ontogeny and functional aspects.  Pp. 225-236 in Aspects of floral development (P Leins, SC Tucker, and PK Endress, eds.).  J. Cramer, Berlin.

Leinfellner, W.  1960.  Zur Entwicklungsgeschichte der Kronblätter der Sterculiaceae-Buettnerieae.  ÖSTERREICHISCHE BOTANISCHE ZEITSCHRIFT107: 153-176.

Swanson, J-D, JE Carlson, and MJ Guiltinan. 2008. Comparative flower development in Theobroma cacao based on temporal morphological indicators. INTERNATIONAL JOURNAL OF PLANT SCIENCES 169: 1187-1199.

van der Pijl, L.  1953.  On the flower biology of some plants from Java with general remarks on fly-traps.  ANNALES BOGORIENSES 1: 77-99.

Westerkamp, C, AA Soares, and LPD Neto.  2006.  Male and female booths with separate entrances in the tiny flowers of Guazuma ulmifolia (Malvaceae-Byttuerioideae). I. Structural integration. FLORA 201: 389-395.

Whitlock BA, C Bayer, and DA Baum.  2001.  Phylogenetic relationships and floral evolution of the Byttnerioideae ("Sterculiaceae" or Malvaceae s.l.) based on sequences of the chloroplast gene, ndhF.  SYSTEMATIC BOTANY 26: 420-437.

Young, AM.  1984.  Mechanism of pollination by Phoridae (Diptera) in some Herrania species (Sterculiaceae) in Costa Rica.  PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 86: 503-518.

Young, AM.  1994.  The chocolate tree: A natural history of cacao.  Smithsonian Institution Press, Washington, DC.

Young, AM, EH Erickson Jr., MA Strand, and BJ Erickson.  1987.  Pollination biology of Theobroma and Herrania (Sterculiaceae): I. Floral biology.  INSECT SCIENCE AND ITS APPLICATION 8: 151-164.

Genetics and genomics

Argout, X, J Salse, J-M Aury, et al. 2011. The genome of Theobroma cacao NATURE GENETICS 43: 101-108.

Bennett, AB.  2003.  Out of the Amazon: Theobroma cacao enters the genomic era.  TRENDS IN PLANT SCIENCE 8: 561-563.

Brown, SJ, D Kuhn D, R Wisser, et al.  2004.  Quantification of sources of variation and accuracy of sequence discrimination in a replicated microarray experiment.  BIOTECHNIQUES 36: 324-332.

Clement, D, AM Risterucci, JC Motamayor, et al.  2003.  Mapping quantitative trait loci for bean traits and ovule number in Theobroma cacao L.  GENOME 46: 103-111.

Clement, D, C Lanaud, X Sabau, et al.  2004.  Creation of BAC genomic resources for cocoa (Theobroma cacao L.) for physical mapping of RGA containing BAC clones.  THEORETICAL AND APPLIED GENETICS 108: 1627-1634.

Feltus, FA, CA Saski, K, Mockaitis, et al. 2011. Sequencing of a QTL-rich region of the Theobroma cacao genome using pooled BACs and the identification of trait specific candidate genes. BMC GENOMICS 12: 379.

Fouet, O, M Allegre, X Argout, et al. 2011. Structural characterization and mapping of functional EST-SSR markers in Theobroma cacao. TREE GENETICS & GENOMES 7: 799-817.

Haase, I, and M Fischer. 2007. Differentiation of Theobroma cocoa and Theobroma grandiflorum by means of PCR. JOURNAL OF CONSUMER PROTECTION AND FOOD SAFETY 2: 422-428.

Jansen RK, C Saski, S-B Lee, et al. 2011. Complete plastid genome sequences of three Rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. MOLECULAR BIOLOGY AND EVOLUTION 28: 835-847.

Jones, PG, D Allaway, DM Gilmour, et al.  2002.  Gene discovery and microarray analysis of cacao (Theobroma cacao L.) varieties.  PLANTA 216: 255-264.

Kuhn, DN, J Borrone, AW Meerow, et al.  2005.  Single-strand conformation polymorphism analysis of candidate genes for reliable identification of alleles by capillary array electrophoresis. ELECTROPHORESIS 26: 112-125.

Kuhn, DN, M Heath, RJ Wisser, et al.  2003.  Resistance gene homologues in Theobroma cacao as useful genetic markers.  THEORETICAL AND APPLIED GENETICS 107: 191-202.

Kuhn, DN, and RJ Schnell.  2005.  Use of capillary array electrophoresis single-strand conformational polymorphism analysis to estimate genetic diversity of candidate genes in germplasm collections.  METHODS IN ENZYMOLOGY 395: 238-258.

Kuhn, DN, A Figueira, U Lopes, et al. 2010. Evaluating Theobroma grandiflorum for comparative genomic studies with Theobroma cacao. TREE GENETICS & GENOMES 6: 783-792.

Lanaud, C, AM Risterucci, I Pieretti, et al.  2004.  Characterisation and genetic mapping of resistance and defence gene analogs in cocoa (Theobroma cacao L.).  MOLECULAR BREEDING 13: 211-227.

Lima, LS, KP Gramacho, JL Pires, et al. 2010. Development, characterization, validation, and mapping of SSRs derived from Theobroma cacao L.-Moniliophthora perniciosa interaction ESTs. TREE GENETICS & GENOMES 6: 663-676.

Livingstone, DS III, JC Motamayor, RJ Schnell, et al. 2011. Development of single nucleotide polymorphism markers in Theobroma cacao and comparison to simple sequence repeat markers for genotyping of Cameroon clones. MOLECULAR BREEDING 27: 93-106.

Motilal LA, D Zhang, P Umaharan et al. 2011. Microsatellite fingerprinting in the International Cocoa Genebank, Trinidad: accession and plot homogeneity information for germplasm management. PLANT GENETIC RESOURCES-CHARACTERIZATION AND UTILIZATION 9: 430-438.

Saski CA, FA Feltus, ME Staton, et al. 2011. A genetically anchored physical framework for Theobroma cacao cv. Matina 1-6. BMC GENOMICS 12: 413.

Schnell, RJ, CT Olano, JS Brown, et al.  2005.  Retrospective determination of the parental population of superior cacao (Theobroma cacao L.) seedlings and association of microsatellite alleles with productivity.  JOURNAL OF THE AMERICAN SOCIETY FOR HORTICULTURAL SCIENCE 130: 181-190.

Silva, CRS, PSB Albuquerque, FR Ervedosa, et al. 2011. 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: 973-985.

 

 

Ecological, ethnobotanical, and comparative studies

Arnold, AE, and EA Herre.  2003.  Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae).MYCOLOGIA 95: 388-398.

Bekele, FL, I Bekele, DR Butler, and GG Bidaisee.  2006.  Patterns of morphological variation in a sample of cacao (Theobroma cacao L.) germplasm from the International Cocoa Genebank, Trinidad.  GENETIC RESOURCES AND CROP EVOLUTION 53: 933-948.

Carpenter, DR, JF Hammerstone Jr., LJ Romanczyk Jr., and WM Aitken.  1994.  Lipid composition of Herrania and Theobroma seeds.  JOURNAL OF THE AMERICAN OIL CHEMISTS’ SOCIETY 71: 845-851.

de Carvalho, CGP, CMVC de Almeida, CD Cruz, et al.  2001.  Evaluation and selection of cacao hybrids in Rondonia.  PESQUISA AGROPECUARIA BRASILEIRA 36: 1043-1051.

Gove, AD, MC Fitzpatrick, JD Majer, et al. 2009. Dispersal traits linked to range size through range location, not dispersal ability, in Western Australian angiosperms. GLOBAL ECOLOGY AND BIOGEOGRAPHY 18: 596-606.

Hammerstone Jr., JF, LJ Romanczyk Jr., and WM Aitken.  1994.  Purine alkaloid distribution within Herrania and Theobroma.  PHYTOCHEMISTRY 35: 1237-1240.

Iwaro, AD, FL Bekele, and DR Butler.  2003.  Evaluation and utilisation of cacao (Theobroma cacao L.) germplasm at the International Cocoa Genebank, Trinidad .EUPHYTICA 130: 207-221.

Lachenaud, P, and G Oliver.  2005.  Variability and selection for morphological bean traits in wild cocoa trees (Theobroma cacao L.) from French Guiana.  GENETIC RESOURCES AND CROP EVOLUTION 52: 225-231.

Lengyel, S, AD Gove, AM Latimer, et al. 2010. Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: A global survey. PERSPECTIVES IN PLANT ECOLOGY EVOLUTION AND SYSTEMATICS 12: 43-55.

Odiwe AI, O Agboola, and JF Ajiboye. 2011. The effect of land use on herbaceous species diversity in Theobroma cacao L. and Citrus sinensis plantations in Ile-Ife, southwestern Nigeria. SOUTH AFRICAN JOURNAL OF BOTANY 77: 549-549.

Niemenak, N, C Rohsius, S Elwers, DO Ndoumou, and R Lieberei.  2006.  Comparative study of different cocoa (Theobroma cacao L.) clones in terms of their phenolics and anthocyanins contents.  JOURNAL OF FOOD COMPOSITION AND ANALYSIS 19: 612-619.

Schroth, G, D Faria, M Araujo, et al. 2011. Conservation in tropical landscape mosaics: the case of the cacao landscape of southern Bahia, Brazil. BIODIVERSITY AND CONSERVATION 20: 1635-1654.

Steinberg, MK.  2002.  The globalization of a ceremonial tree: The case of cacao (Theobroma cacao) among the Mopan Maya.  ECONOMIC BOTANY 56: 58-65.

Washburn, DK, WN Washburn, and PA Shipkova. 2011. The prehistoric drug trade: widespread consumption of cacao in Ancestral Pueblo and Hohokam communities in the American Southwest. JOURNAL OF ARCHAEOLOGICAL SCIENCE 38: 1634-1640.

Classification and taxonomy

Cheesman, EE.  1944.  Notes on nomenclature, classification and possible relationships of cacao populations.  TROPICAL AGRICULTURE 21: 144-159.

Cuatrecasas, J.  1964.  Cacao and its allies: A taxonomic revision of the genus Theobroma.  CONTRIBUTIONS OF THE US NATIONAL HERBARIUM 35: 379-614.

Freytag, GF.  1951.  A revision of the genus Guazuma.  CEIBA 1: 193-225.

Schultes, RE.  1958.  A synopsis of the genus Herrania.  JOURNAL OF THE ARNOLD ARBORETUM 39: 216-295.

Townsend, CC.  1980.  44. Sterculiaceae.  Pp. 221-227 in: Flora of Iraq, volume 4 (CC Townsend and E Guest, Eds.).  Ministry of Agriculture and Agrarian Reform, Baghdad.

Whitlock, BA, C Bayer, and DA Baum.  2001.  Phylogenetic relationships and floral evolution of the Byttnerioideae ("Sterculiaceae" or Malvaceae s.l.) based on sequences of the chloroplast gene, ndhF.  SYSTEMATIC BOTANY 26: 420-437.

Seed biology and seed storage proteins

Amin, I, S Jinap, B Jamilah, et al.  2002.  Analysis of vicilin (7S)-class globulin in cocoa cotyledons from various genetic origins .JOURNAL OF THE SCIENCE OF FOOD AND AGRICULTURE 82: 728-732.

Amin, I, S Jinap, B Jamilah, et al.  2002.  Oligopeptide patterns produced from Theobroma cacao L of various genetic origins.  JOURNAL OF THE SCIENCE OF FOOD AND AGRICULTURE 82: 733-737.

Andersson, M, G Koch, and R Lieberei.  2006.  Structure and function of the seed coat of Theobroma cacao L. and its possible impact on flavour precursor development during fermentation.  JOURNAL OF APPLIED BOTANY AND FOOD QUALITY-ANGEWANDTE BOTANIK 80: 48-62.

de Bertorelli, LO, H Maldonado, P Parra, and LG de Farinas.  2006.  Electrophoretic characterization of globulins from fermented grains of three types of cocoa. INTERCIENCIA 31: 441-445.

Chlan, CA, K Borroto, JA Kamalay, and L Dure III.  1987.  Developmental biochemistry of cottonseed embryogenesis and germination.  XIX.  Sequences and genomic organization of the alpha globulin (vicilin) genes of cottonseed.  PLANT MOLECULAR BIOLOGY 9: 533-546.

Doyle, JJ, MA Schuler, WD Godette, V Zenger, RN Beachy, and JL Slightom.  1986.  The glycosylated seed storage proteins of Glycine max and Phaseolus vulgaris.  JOURNAL OF BIOLOGICAL CHEMISTRY 261: 9228-9238.

Gove, AD, MC Fitzpatrick, JD Majer, et al. 2009. Dispersal traits linked to range size through range location, not dispersal ability, in Western Australian angiosperms. GLOBAL ECOLOGY AND BIOGEOGRAPHY 18: 596-606.

Lengyel, S, AD Gove, AM Latimer, et al. 2010. Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: A global survey. PERSPECTIVES IN PLANT ECOLOGY EVOLUTION AND SYSTEMATICS 12: 43-55.

McHenry, L, and PJ Fritz.  1992.  Comparison of the structure and nucleotide sequences of vicilin genes of cocoa and cotton raise questions about vicilin evolution.  PLANT MOLECULAR BIOLOGY 18: 1173-1176.

Reisdorff, C, C Rohsius, ADC de Souza, et al.  2004.  Comparative study on the proteolytic activities and storage globulins in seeds of Theobroma grandiflorum (Willd ex Spreng) Schum and Theobroma bicolor Humb Bonpl, in relation to their potential to generate chocolate-like aroma.  JOURNAL OF THE SCIENCE OF FOOD AND AGRICULTURE 84: 693-700.

Rohsius, C, R Matissek, and R Lieberei.  2006.  Free amino acid amounts in raw cocoas from different origins.  EUROPEAN FOOD RESEARCH AND TECHNOLOGY 222: 432-438.

Saenz de Miera, LE, and M Perez de la Vega.  1998.  A comparative study of vicilin genes in Lens: Negative evidence of concerted evolution.  MOLECULAR BIOLOGY AND EVOLUTION 15: 303-311.

Spencer, ME, and R Hodge.  1992.  Cloning and sequencing of a cDNA encoding the major storage proteins of Theobroma cacao.  PLANTA 186: 567-576.

Tai, H, L McHenry, PJ Frizt, and DB Furtek.  1991.  Nucleic acid sequence of a 21kDa cocoa seed protein with homology to the soybean trypsin inhibitors.  PLANT MOLECULAR BIOLOGY 16: 913-915.

Voight, J, B Biehl, and SKS Wazir.  1993.  The major seed proteins of Theobroma cacao L.  FOOD CHEMISTRY 47: 145-151.

Voight, J, H Heinrichs, G Voigt, and B Biehl.  1994.  Cocoa-specific aroma precursors are generated by proteolytic digestion of the vicilin-like globulin of cocoa seeds.  FOOD CHEMISTRY 50: 177-184.

Voight, J, G Voight, H Heinrichs, D Wrann, and B Biehl.  1994.  In vitro studies on the proteolytic formation of the characteristic aroma precursors of fermented cocoa seeds: The significance of endoprotease specificity.  FOOD CHEMISTRY 51: 7-14.

Voight, J, D Wrann, H Heinrichs, and B Biehl.  1994.  The proteolytic formation of essential cocoa-specific aroma precursors depends on particular chemical structures of the vicilin-class globulin of the cocoa seeds lacking in the globular storage proteins of coconuts, hazelnuts and sunflower seeds.  FOOD CHEMISTRY 51: 197-205.

Kochhar, S, K Gartenmann, M Guilloteau, et al.  2001.  Isolation and characterization of 2S cocoa seed albumin storage polypeptide and the corresponding cDNA .JOURNAL OF AGRICULTURAL AND FOOD CHEMISTRY 49: 4470-4477.