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Complex Origin of Trinitario-Type Theobroma Cacao (Malvaceae) from Trinidad and Tobago Revealed Using Plastid Genomics

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Complex Origin of Trinitario-Type Theobroma Cacao (Malvaceae) from Trinidad and Tobago Revealed Using Plastid Genomics Tree Genetics & Genomes DOI 10.1007/s11295-013-0601-4 ORIGINAL PAPER 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 Received: 5 July 2012 /Revised: 19 December 2012 /Accepted: 9 January 2013 # Springer-Verlag Berlin Heidelberg 2013 Abstract Trinidad and Tobago has a long history of produc- one outgroup, T. grandiflorum (Willd. ex Spreng.) Schum). ing high-quality cacao (Theobroma cacao L.). Cacao geno- Only three cpSNP haplotypes were present in the Trinitario types in Trinidad and Tobago are of a highly distinctive kind, cultivars sampled, each highly distinctive and corresponding the so-called “Trinitario” cultivar group, widely considered to to reference genotypes for the Criollo (CRI), Upper Amazon be of elite quality. The origin of Trinitario cacao is unclear, Forastero (UAF) and Lower Amazon Forastero (LAF) varietal although it is generally considered to be of hybrid origin. We groups. These three cpSNP haplotypes likely represent the used massive parallel sequencing to identify polymorphic founding lineages of cacao to Trinidad and Tobago. The plastidic single nucleotide polymorphisms (cpSNPs) and cpSSRs were more variable with eight haplotypes, but these polymorphic plastidic simple sequence repeats (cpSSRs) in clustered into three groups corresponding to the three cpSNP order to determine the origin of the Trinitario cultivar group by haplotypes. The most common haplotype found in farms of comparing patterns of polymorphism to a reference set of ten Trinidad and Tobago was LAF, followed by UAF and then completely sequenced chloroplast genomes (nine T. cacao and CRI. We conclude that the Trinitario cultivar group is of complex hybrid origin and has derived from at least three Communicated by R. Sederoff original introduction events. * : : : : J. Y. Yang ( ): M. Scascitelli S. Sveinsson N. C. Kane Keywords Theobroma cacao . Chloroplast . Microsatellites . H. Dempewolf Q. C. B. Cronk . Department of Botany, University of British Columbia, Single nucleotide polymorphisms Trinitario Vancouver, BC V6T 1Z4, Canada e-mail: [email protected] Introduction L. A. Motilal Cocoa Research Unit, The University of the West Indies, St. Augustine, Trinidad, West Indies, Theobroma cacao L. (cacao) is an economically important Republic of Trinidad and Tobago crop as its seeds are the sole source of commercial chocolate. Cacao flowers are mainly pollinated by midges (Forcipomyia J. M. M. Engels Biodiversity International, 00057 Maccarese Rome, Italy species) and exhibit a high degree of outcrossing (Silva et al. 2010). Commercial cacao has two main ancestral groups, D. Zhang Criollo and Forastero, and a derived group, Trinitario SPCL, USDA-ARS, Building 001 BARC-West, (Cheesman 1944). Criollos were likely domesticated by the 10300 Baltimore Avenue, Beltsville, MD 20705, USA Mayas in Central America (Toxopeus 1985; Motamayor et al. 2002) and were spread to the Caribbean and South America K. Maharaj after the mid-16th century (Wood 1985). Criollos are now Ministry of Agriculture, Food Production Land, and Marine known to be highly susceptible to several diseases and of the Resources Affairs, Central Experiment Station, Centeno, Via Arima P.O., West Indies, three cacao groups (Criollo, Forastero, and Trinitario) they are Republic of Trinidad and Tobago the least vigorous (Toxopeus 1985; Wood 1985). Forastero is Tree Genetics & Genomes an umbrella group referring to germplasm from the Upper and Criollo and postulated a greater contribution of Forastero lin- Lower Amazon basin. It is more disease resistant and vigorous eage to the genetic composition of Trinitarios, suggesting that than Criollo (Toxopeus 1985) and has a higher yield. It is now the cacao cultivated in Trinidad prior to 1727 was the most commonly grown cacao in the world (Wood 1985). “introgressed Criollo” (i.e., with a genetic contribution from However, Forasteros are less valuable because their fermented Forastero) rather than what is now known as “pure Criollo.” beans are not generally considered to produce a high quality flavor (Wood 1985), although there are excep- Utility of plastid haplotype markers in determining tions such as the “Nacional” variety of Forastero from the origin of Trinitario cacao Ecuador (Loor et al. 2009). Genetic markers from uniparentally inherited and non- History of cacao cultivation in Trinidad and Tobago recombining organelles (e.g., chloroplasts or mitochondria) are generally of greater utility than nuclear markers in In Trinidad most of the trees were supposedly destroyed by phylogeographical studies because there is no recombination disease in the 18th century (Shephard 1932; Cheesman 1944) that hinders the study of parental origin (Petit and Vendramin especially by a disastrous outbreak in 1727. A new cultigen 2007). Chloroplast (plastid) markers have proven useful for called Trinitario was later documented in Trinidad, seemingly distinguishing among different cultivars in several crop spe- having arisen through natural hybridization between the local cies including soya (Powell et al. 1996), rice (Provan et al. surviving Criollo trees and the Forastero planted between the 1997), barley (Provan et al. 1999) and grapevine (Arroyo- remaining Criollo (Pound 1931; Cheesman 1944; Engels Garcia et al. 2002). Thus, plastid markers should be useful to 1986;CoeandCoe1996; Bartley 2005). The hybrids, untangle the complex origin of the Trinitario trees currently throughout the island of Trinidad, showed variation in their found in Trinidad and Tobago. A recent sequencing effort combination of parental characters and a selection program characterized the full chloroplast genome of ten cacao geno- based primarily on yield led to the identification of 100 types (Kane et al. 2012), allowing the discovery of 78 single Trinitario trees now known as the Imperial College Selection nucleotide polymorphisms (SNPs). We used ten of these SNPs (ICS) accessions (Pound 1933, 1934, 1935, 1936;Cheesman to determine the chloroplast contributions of reference geno- 1934). A more recent germplasm collection of accessions types of UAF, LAF, and Criollo to the cacao trees farmed from relic estates in Trinidad (TRD) has also been made across Trinidad and Tobago. In addition we analyzed plastid (Bekele et al. 2007). In the 1940s, a breeding program was DNA variation at nine polymorphic simple sequence repeats established by the Ministry of Agriculture in Trinidad under (SSRs) to assess the genetic composition and haplotype di- which locally selected Trinitarios were crossed with geno- versity of Trinitario cacao from Trinidad and Tobago. types from South America. This work generated the Trinidad Selected Hybrids (TSH) and has provided a basis for all modern cacao breeding programs (Freeman 1969). Materials and methods However, modern breeding programs have been affected by the lack of comprehensive characterization of the available Cacao material studied cacao genetic resources, coupled with problems of accession mislabeling (Motilal et al. 2009, 2011; Irish et al. 2010). Ten complete chloroplast genome reference sequences were used for polymorphic plastidic single nucleotide polymor- Previous studies on the origin of the Trinitario cacao phism (cpSNP) development. These consisted of nine T. ca- cao accessions and one outgroup, T. grandiflorum.TheT. With the accumulation of molecular analyses, primarily micro- cacao accessions included a Criollo genotype (accession: satellite data, new scenarios for the origin of the Trinitario Criollo-22), a UAF genotype (Scavina-6, accession: varietal group have been suggested. Motamayor et al. (2003) MIA29885), and a LAF genotype (Amelonado, accession: proposed that Trinitarios originated by hybridization between a TARS 16542). These three reference accessions were selected small number of Lower Amazon Amelonado-Forastero (LAF) to represent standard exemplars of the three varietal groups. genotypes and Criollo, while less than 10 % of Trinitario The remaining T. cacao accessions were of Trinitario geno- accessions bore alleles from the other main Forastero variety, types (see Kane et al. 2012 for further details). the Upper Amazon Forastero (UAF). Johnson et al. (2009) In total, 95 Trinitario cacao trees were genotyped in this found that Criollo played an important role in the origin of study (see Tables 1 and 2). Sixty-four accessions were Trinitario accessions and they considered that the limited num- collected from 33 different farms in Trinidad (Fig. 1); eight ber of Trinitarios with UAF alleles resulted from intensive accessions were collected from six different farms in Tobago breeding efforts to integrate UAF disease resistance traits into (Fig. 2). The remaining 23 samples were reference Trinitario Trinitario. Motilal et al. (2010) downplayed the contribution of accessions from the International Cocoa Genebank, Tree Genetics & Genomes Table 1 Haplotype diversity of Trinitarios collected from farms in Table 1 (continued) Trinidad and Tobago, based on cpSSR and cpSNP analysis Sample Provenance Farm Location cpSSR cpSNP Sample Provenance Farm Location cpSSR cpSNP ID Haplotype Haplotype ID Haplotype Haplotype K143 Trinidad G Moruga 8 LAF K087 Trinidad AF Aripo 2 LAF K146 Trinidad G Moruga 8 LAF K088 Trinidad AF Aripo 2 LAF K147 Trinidad G Moruga 8 LAF K089 Trinidad E
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