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Adding Value to Cocoa (Theobroma Cacao L.) Germplasm Information with Domestication History and Admixture Mapping

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Adding Value to Cocoa (Theobroma Cacao L.) Germplasm Information with Domestication History and Admixture Mapping Theor Appl Genet DOI 10.1007/s00122-006-0486-9 ORIGINAL PAPER Adding value to cocoa (Theobroma cacao L.) germplasm information with domestication history and admixture mapping Maria Marcano · Tatiana Pugh · Emile Cros · Sonia Morales · Elvis A. Portillo Páez · Brigitte Courtois · Jean Christophe Glaszmann · Jan M. M. Engels · Wilbert Phillips · Carlos Astorga · Ange Marie Risterucci · Olivier Fouet · Ventura González · Kai Rosenberg · Isabelle Vallat · Manuel Dagert · Claire Lanaud Received: 27 April 2006 / Accepted: 16 December 2006 © Springer-Verlag 2007 Abstract A sound understanding of crop history can genome scans, genomic regions involved in useful traits provide the basis for deriving novel genetic informa- were identiWed. Fifteen genomic regions involved in tion through admixture mapping. We conWrmed this, seed and fruit weight variation were highlighted. They by using characterization data from an international correspond to ten previously identiWed QTLs and Wve collection of cocoa, collected 25 years ago, and from a novel ones. Admixture mapping can help to add value contemporary plantation. We focus on the trees to genetic resources and thus, help to encourage invest- derived from three centuries of admixture between ment in their conservation. Meso-American Criollo and South American Foras- tero genomes. In both cacao sets of individuals, linkage disequilibrium extended over long genetic distances Introduction along chromosome regions, as expected in populations derived from recent admixture. Based on loose Crop genetic resources provide the foundation for sus- taining agricultural production. For most crops, large germplasm collections have been assembled and partially Communicated by J.-L. Jannink. characterised for useful traits (FAO 1998). However, crop-breeding programs can incorporate only a small part Maria Marcano and Tatiana Pugh contributed equally to this work. M. Marcano (&) · T. Pugh · E. Cros · E. A. Portillo Páez · J. M. M. Engels B. Courtois · J. C. Glaszmann · A. M. Risterucci · Bioversity International, O. Fouet · C. Lanaud Via dei Tre Denari, 472a, 00057, Centre de Coopération Internationale en Recherche Maccarese, Rome, Italy Agronomique pour le Développement, (CIRAD) TA 40/03, 34398 Montpellier Cedex 5, France W. Phillips · C. Astorga e-mail: [email protected] Centro Agronómico Tropical de Investigación y Enseñanza, P.O. Box 7170, CATIE, Turrialba, Costa Rica M. Marcano · S. Morales · M. Dagert Laboratorio de Genética y Química Celular V. González (GEQUIMCEL), Universidad de los Andes (ULA), Instituto Nacional de Investigaciones Agrícolas, La Hechicera, Mérida, Edo. Mérida, Venezuela INIA–CENIAP, Av. Universidad, Maracay, 2101 Edo. Aragua, Venezuela T. Pugh Facultad de Agronomía, K. Rosenberg · I. Vallat Universidad Central de Venezuela (UCV), VALRHONA, Les lots, 26600 Tain L’ hermitage, France Av. El Limón, Maracay, 2101 Edo. Aragua, Venezuela E. A. Portillo Páez Facultad de Agronomía. Maracaibo, Universidad del Zulia (LUZ), Edo Zulia, Venezuela 13 Theor Appl Genet of the available diversity at any given time. The long-term cation of association mapping when no candidate gene maintenance of such collections is a Wnancial burden for is available for the traits under consideration. those responsible, particularly for long-lived tree species When genotype information is available of the whose seeds are unsuited to storage. Drawing more founding population, such recent admixture of previ- immediate value from such collections is essential to ously diverged populations can be exploited for map- ensure institutional commitment to their management. ping purposes in a way that is similar to cross based Association mapping has recently emerged as a linkage mapping. Markers can be used to trace chromo- powerful method for generating genetic information somal blocks back to one of the founding populations from population samples. It is based on the non-ran- and QTLs that have diverged between these founding dom association of alleles, at two or more loci, called populations can be identiWed via trait ancestry associa- “linkage disequilibrium” (LD), in natural or cultivated tions in the admixed populations (McKeigue 2005). populations. Through LD, the genes involved in the Admixture mapping has been applied to detect variation of morphological, agronomic and other phe- genetic factors that determine hypertension, a complex notypic traits can be located in the genome if statistical human disease (Zhu et al. 2005), however, to our knowl- associations can be found between the traits and edge, it has not been exploited in plant populations. The genetic marker polymorphisms. approach requires generally a lower density of markers Although association mapping has been extensively than for traditional association mapping and is particu- used for mapping disease factors in humans, its use in larly useful in admixed populations derived from two plants has only recently begun. Associations were known progenitors, with diVerent proportions of the found between polymorphisms at the DNA sequence allele aVecting the trait (Darvasi and Shifman 2005) level between the maize Dwarf8 gene implicated in We explored the value of this approach for analy- plant height, and Xowering time, in 92 inbred lines sing cocoa germplasm populations, taking advantage of (Thornsberry et al. 2001). In Arabidopsis, associations a particular hybrid group that has been recently between genotype and phenotype were reported for domesticated. four known genes involved in Xowering time and path- Theobroma cacao L. is a perennial tree native to the ogen resistance in a study that included sequenced American tropics; it was domesticated more than fragments genomewide distributed every 100 Kb 2,000 years ago by Mesoamerican peoples, who culti- (Aranzana et al. 2005). Recently, associations were vated a high-quality aromatic chocolate variety, named found in a collection of modern barley cultivars, Criollo (local), probably originating from the northern between AFLP markers and mean yield and yield sta- part of South America (Motamayor et al. 2002). After bility (Kraakman 2004). In cacao, an association study Spanish colonization, the production of Criollo spread was reported in a population which included produc- to South America and the Caribbean region to satisfy tive and non-productive clones in which 13 associated an increasing demand for cocoa in Europe. A natural markers were near previously mapped QTLs for pro- disaster in Trinidad during the 18th century led to the ductivity traits (Schnell et al. 2005). introduction to this island of a newly domesticated and During their evolution, allopatric populations are genetically divergent variety, a Forastero (foreigner) subjected to parallel drift and contrasted selection originating from Lower Amazonia. Open pollinations pressures, and can accumulate mutations, generating involving the remaining Criollo trees and the newly global divergence. Such structuring of the overall pop- introduced Forastero, gave rise to hybrid forms called ulation into independent subpopulations can generate Trinitario. Due to their vigour, Trinitario materials a pattern of LD that typically associates regions distrib- were later introduced to the South American conti- uted in the whole genome. Domestication selected nent, and gradually spread into original Criollo planta- only speciWc forms of the wild ancestors, and modern tions, leading to further crossing between Criollo and breeding focused only on a few parental genotypes. Trinitario individuals. Most of the modern Criollo vari- Both processes constituted considerable genetic bottle- eties, selected for their quality traits, result from the necks in crop populations, further accentuating LD. recombination between ancestral Criollo and invading When migrating humans carried crop cultivars with Trinitario (Motamayor et al. 2003). them, recombination events between previously diver- We have recently demonstrated that 80% of the gent populations sometimes occurred. Thus, LD was Trinitario trees originated from a very narrow genetic reduced between unlinked genome regions but was base represented by an almost monomorphic ancestral maintained within segments little aVected by recombi- Criollo form, and a small number of inter-related nation; “Global” LD was dissipated or disappeared Forastero types (Motamayor et al. 2003). The Wrst whereas “local” LD was maintained. LD enables appli- recombination between the two ancestral forms 13 Theor Appl Genet occurred 250 years ago. Since then, probably no more in both sets of individuals (collection and planta- than 6 or 7 recombination generations have occurred. tion) to evaluate population structure and deter- Modern Criollo/Trinitario varieties now constitute the mine the threshold to be used in LD analysis. basis of nearly 70% of cocoa cultivation worldwide. 2. One hundred and one microsatellites were used to Although quality and morphology of beans are the genotype the 150 individuals from the CATIE col- most distinctive traits between ancient Criollo and lection and 92 microsatellites were analyzed in the other cacao varieties, additional traits, such as growth 291 individuals from the Mérida plantation. These habit, pigmentation in diVerent plant structures, yield microsatellites were used to study the extent of potential and disease resistance, diVerentiate ancient local LD across the whole genome and to identify Criollo from Forastero cultivars. marker-trait associations. Microsatellite map posi- In this study, our objectives
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