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Multidisciplinary Perspectives on Banana (Musa Spp.) Domestication

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Multidisciplinary Perspectives on Banana (Musa Spp.) Domestication PERSPECTIVE Multidisciplinary perspectives on banana (Musa spp.) domestication Xavier Perriera, Edmond De Langheb, Mark Donohuec, Carol Lentferd, Luc Vrydaghse, Frédéric Bakrya, Françoise Carreelf, Isabelle Hippolytea, Jean-Pierre Horrya, Christophe Jennyg, Vincent Leboth, Ange-Marie Risteruccia, Kodjo Tomekpea, Hugues Doutreleponte, Terry Balli, Jason Manwaringi, Pierre de Maretj, and Tim Denhamk,1 aCentre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Amélioration Génétique et Adaptation des Plantes, F-34398 Montpellier, France; bLaboratory of Tropical Crop Improvement, Katholieke Universiteit, 3001 Leuven, Belgium; cDepartment of Linguistics, Australian National University, Canberra 0200, Australia; dSchool of Social Science, University of Queensland, St. Lucia 4072, Australia; eResearch Team in Archaeo- and Palaeosciences, 1160 Brussels, Belgium; fCentre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Biologie et Génétique des Interactions Plantes-Parasites, F-34398 Montpellier, France; gCentre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Amélioration Génétique et Adaptation des Plantes, F-97130 Capesterre-Belle-Eau, Guadeloupe, France; hCentre de Coopération Internationale en Recherche Agronomique pour le Développement, Unité Mixte de Recherche Amélioration Génétique et Adaptation des Plantes, Department of Agriculture, Centre Agronomique de Recherche et de Formation du Vanuatu, 946 Port Vila, Vanuatu; iDepartment of Ancient Scripture, Brigham Young University, Provo, UT 84602; jSecrétariat, Centre d’Anthropologie Culturelle, Université Libre de Bruxelles, 1000 Brussels, Belgium; and kSchool of Geography and Environmental Science, Monash University, Victoria 3800, Australia Edited by Dolores R. Piperno, Smithsonian National Museum of Natural History and Smithsonian Tropical Research Institute, Panama City, Panama, and approved May 25, 2011 (received for review March 5, 2011) Original multidisciplinary research hereby clarifies the complex geodomestication pathways that generated the vast range of banana cultivars (cvs). Genetic analyses identify the wild ancestors of modern-day cvs and elucidate several key stages of domestication for different cv groups. Archaeology and linguistics shed light on the historical roles of people in the movement and cultivation of bananas from New Guinea to West Africa during the Holocene. The historical reconstruction of domestication processes is essential for breeding programs seeking to diversify and improve banana cvs for the future. plant genetics | historical linguistics | archaeobotany | diploid banana cultivars | triploid banana cultivars ew multidisciplinary findings tropical and subtropical regions (1). The (NG), the native area of the M. acuminata from archaeology, genetics, hundreds of cultivated varieties are prod- subsp. banksii (3), and through the appli- and linguistics clarify the ucts of centuries—in some cases millennia cation of molecular methods to banana N – complex geodomestication —of clonal (vegetative) propagation. diversity analysis (4 7). — fi pathways the geographical con g- Banana fruits can be cooked, roasted, or In the present study, we present the — urations of hybridization and dispersal even brewed (e.g., plantains; East African conclusions of two recent analyses by using simple sequence repeats (8) and DarT (9) that generated the range of modern ba- Highland cvs) or eaten raw (e.g., the nana cultivars (cvs). Although recent markers on the international collection in yellow Cavendish banana sold in super- molecular research, combined with the Guadeloupe (Centre de Coopération In- markets globally). outcomes of previous genetic studies, elu- ternationale en Recherche Agronomique pour le Développement, France) which cidates major stages of banana domesti- Musa Genetics and Domestication assembles more than 400 wild and culti- cation, such as the generation of edible Thresholds diploids and triploids, it sheds only partial vated accessions covering much of global The monocotyledon Musaceae family Musa light on the historical and sociospatial diversity. Analyses here include ad- includes the Asian and African genus ditional accessions from Cameroon and contexts of domestication. The geographic Ensete , the genetically proximal Asian Nigeria to better represent African cv di- distributions of genotypes involved in ba- Musella genus, and the East Asian genus versity (Table S1). The results of these nana domestication require human trans- Musa , which is divided into sections with analyses were integrated with previous locations of plants, most likely under 22 (Eumusa, Rhodochlamys) and 20 vegetative forms of cultivation, across vast results, including ploidy level and DNA chromosomes (Australimusa, Callimusa). content (10), anthocyanin patterns (11), regions. Linguistic analyses of (traditional) Most edible bananas belong to the Eu- local terms for bananas reveal several isozymes (12), nuclear restriction (13) musa section, and are diploid or triploid and amplified fragment length poly- striking regional-scale correspondences Musa acuminata hybrids from (A-genome) morphism (14), and chloroplastic and mi- between genetic and linguistic patterns. Musa alone or from hybridization with tochondrial restriction fragment length These multidisciplinary findings enable the balbisiana (B-genome). A minor cv group, relative dating of the principal events in including Fe’i bananas, is confined to banana geodomestication and situate ba- the Pacific region and is derived from Author contributions: P.d.M. designed research; E.D.L., nana cultivation within broader socio- Australimusa species. M.D., C.L., L.V., F.B., F.C., I.H., J.-P.H., C.J., L.V., A.-M.R., fi K.T., H.D., T.B., and J.M. performed research; X.P. analyzed spatial contexts. Archaeological ndings The evolution from wild to edible ba- data; and X.P., E.D.L., M.D., and T.D. wrote the paper. provide a timeline to anchor and calibrate nanas involved seed suppression and par- The authors declare no conflict of interest. the relative chronology. thenocarpy development. Simmonds (2) This article is a PNAS Direct Submission. Banana ranks next to rice, wheat, and proposed the first reconstruction of this 1To whom correspondence should be addressed. E-mail: maize in terms of its importance as a food complex process in the 1960s. Since then [email protected]. crop. In addition to being a major cash crop the spectrum of available genetic re- This article contains supporting information online at around the world, more than 85% of ba- sources has been greatly expanded, nota- www.pnas.org/lookup/suppl/doi:10.1073/pnas.1102001108/-/ nanas are grown for local consumption in bly with collections from New Guinea DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1102001108 PNAS | July 12, 2011 | vol. 108 | no. 28 | 11311–11318 Downloaded by guest on September 24, 2021 polymorphism (15). The synthesis of these structural heterozygosity of these hybrid major role in the development of several results sheds light upon the two founding AAcvs, caused by chromosomal re- important diploid and triploid cv groups events during banana domestication: the arrangements between parental subspecies that are now widely dispersed. For exam- transition from wild to edible diploids and of M. acuminata (17), contributed to ga- ple, M. acuminata subsp. zebrina- and the formation of triploids from edible metic sterility (18). This sterility, in asso- subsp. banksii-derived AAcvs contributed diploids (16) (Fig. S1). ciation with human selection for pulp to AAA Highland bananas of East Africa. Wild M. acuminata species are diverse enhancement, led to parthenocarpic fruits Likewise, subsp. banksii-derived AAcvs and have been differentiated into several and edibility. with the BB genome contributed to AAB subspecies (13, 16). This differentiation is A further consequence of hybrid status plantains of West Africa and the Pacific. clarified here with the identification of was erratic meiosis in edible AAcvs, Moreover, in several triploid subgroups, specific nuclear alleles, chromosomal re- thereby occasionally producing diploid specific accessions within AAcv subgroups arrangements, and chloroplast and mito- gametes (2). The fusion of diploid gametes have been identified as potential ances- chondrial patterns. The exclusive natural with haploid gametes generated sterile tors, suggesting more recent formation ranges of the subspecies are also con- triploid genotypes. Spontaneous triploid- (16, 20). For example, the 2N and N pa- firmed (Fig. 1). izations involved almost all diploid cvs rents of the common dessert banana, the The key result relevant to domestication leading, under human selection via vege- AAA “Cavendish,” are genetically close to history is that edible diploid cv subgroups tative propagation, to the diversity of “Akondro Mainty” of the AAcv “Mlali” (AAcvs) derive from hybridizations be- modern cultivated triploids, including pure subgroup and “Pisang Pipit” of the AAcv tween different M. acuminata subspecies M. acuminata varieties (AAA) and in- “Khai” subgroup, respectively (Fig. 2). in island Southeast Asia (SEA; ISEA) terspecific M. acuminata × M. balbisiana Strict vegetative propagation (i.e., clon- and western Melanesia (Fig. 2 and Fig. varieties (AAB, ABB) (19). ing) over long periods of the most popular S2), which could only be brought into Molecular phylogenetic analyses
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