BACKGROUND AND AIMS: Dessert and cooking bananas are vegetatively propagated crops of great importance for both the subsistence and the livelihood of people in developing countries. A wide diversity of diploid and triploid cultivars including AA, AB, AS, AT, AAA, AAB, ABB, AAS and AAT genomic constitutions exists. Within each of this genome groups, cultivars are classified into subgroups that are reported to correspond to varieties clonally derived from each other after a single sexual event. The number of those founding events at the basis of the diversity of bananas is a matter of debate. METHODS: We analysed a large panel of 575 accessions, 94 wild relatives and 481 cultivated accessions belonging to the section Musa with a set of 498 DArT markers previously developed. KEY RESULTS: DArT appeared successful and accurate to describe Musa diversity and help in the resolution of cultivated banana genome constitution and taxonomy, and highlighted discrepancies in the acknowledged classification of some accessions. This study also argues for at least two centres of domestication corresponding to South-East Asia and New Guinea, respectively. Banana domestication in New Guinea probably followed different schemes that those previously reported where hybridization underpins the emergence of edible banana. In addition, our results suggest that not all wild ancestors of bananas are known, especially in M. acuminata subspecies. We also estimate the extent of the two consecutive bottlenecks in edible bananas by evaluating the number of sexual founding events underlying our sets of edible diploids and triploids, respectively. CONCLUSIONS: The attribution of clone identity to each sample of the sets allowed the detection of subgroups represented by several sets of clones. Although morphological characterization of some of the accessions is needed to correct potentially erroneous classifications, some of the subgroups seem polyclonal.

Bioversity International Parc Scientifique Agropolis 2 1990 boulevard de la Lironde 34397 Montpellier Cedex 5 France

Bioversity International Willem De Croylaan 42 3001 Leuven Belgium

CIRAD UMR AGAP 34398 Montpellier France

Diversity Arrays Technology Pty Ltd Building 3 University of Canberra Bruce ACT 2617 Australia

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Šlechtitelů 31 78371 Olomouc Czech Republic

Zobrazit více v PubMed

Akbari M, Wenzl P, Caig V, et al. 2006. Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theoretical and Applied Genetics 113: 1409–20. PubMed

Amorim EP, Vilarinhos AD, Cohen KO, et al. 2009. Genetic diversity of carotenoid-rich bananas evaluated by Diversity Arrays Technology (DArT). Genetics and Molecular Biology 32: 96–103. PubMed PMC

Bakry F, Horry JP. 2016. Advances in genomics: applications to banana breeding. Acta Horticulturae 1114: 171–180.

Boonruangrod R, Desai D, Fluch S, Berenyi M, Burg K. 2008. Identification of cytoplasmic ancestor gene-pools of Musa acuminata Colla and Musa balbisiana Colla and their hybrids by chloroplast and mitochondrial haplotyping. Theorical and Applied Genetics 118: 43–55. PubMed

Bouchet S, Pot D, Deu M, et al. 2012. Genetic structure, linkage disequilibrium and signature of selection in sorghum: lessons from physically anchored DArT markers. PLoS One 7: e33470. doi:10.1371/journal.pone.0033470. PubMed PMC

Carreel F, Fauré S, González de León D, et al. 1994. Evaluation de la diversité génétique chez les bananiers diploïdes (Musa sp). Genetics Selection Evolution 26 (S1): 125s–136s.

Carreel F, Gonzalez de Leon D, Lagoda P, et al. 2002. Ascertaining maternal and paternal lineage within Musa by chloroplast and mitochondrial DNA RFLP analyses. Genome 45: 679–692. PubMed

Chase R, Sardos J, Ruas M, et al. 2016. The field verification activity: a cooperative approach to the management of the global Musa in-vitro collection at the International Transit Centre. Acta Horticulturae 1114: 61–65.

Christelová P, Valarik M, Hribova E, et al. 2011. A platform for efficient genotyping in Musa using microsatellite markers. AoB PLANTS 2011 plr024 doi:10.1093/aobpla/plr024. PubMed PMC

Čížková J, Hribova E, Humplíková L, Christelová P, Suchánková P, Dolezel J. 2013. Molecular analysis and genomic organization of major DNA satellites in banana (Musa spp.). PLoS One 8(1): e54808. doi:10.1371/journal.pone.0054808. PubMed PMC

D’Hont A, Denoeud F, Aury JM, et al. 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488: 213–217. PubMed

de Jesus ON, de Oliveira e, Silva S, Amorim EP, et al. 2013. Genetic diversity and population structure of Musa accessions in ex situ conservation. BMC Plant Biology 13: 41. PubMed PMC

De Langhe E, Vrydaghs L, De Maret P, Perrier X, Denham TP. 2009. Why bananas matter: an introduction to the history of banana domestication. Ethnobotany Research and Applications 7: 165–177.

Douhovnikoff V, Dodd RS. 2003. Intra-clonal variation and a similarity threshold for identification of clones: application to Salix exigua using AFLP molecular markers. Theorical and Applied Genetics 106: 1307–1315. PubMed

Earl DA, vonHoldt BM. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620. PubMed

Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164: 1567–1587. PubMed PMC

Hippolyte I, Bakry F, Séguin M, et al. 2010. A saturated SSR/DArT linkage map of Musa acuminate addressing genome rearrangements among bananas. BMC Plant Biology 10: 65. PubMed PMC

Hippolyte I, Jenny C, Gardes L, et al. 2012. Foundation characteristics of edible Musa triploids revealed from allelic distribution of SSR markers. Annals of Botany 109: 937–951. PubMed PMC

Hřibová E, Cizkova J, Christelová P, Taudien S, de Langhe E, Dolezel J. 2011. The ITS1–5.8S-ITS2 sequence region in the Musaceae: structure, diversity and use in molecular phylogeny. PLoS One 6: e17863. doi:10.1371/journal.pone.0017863. PubMed PMC

Irish BM, Cuevas HE, Simpson SA, et al. 2014. Musa spp. germplasm management: microsatellite fingerprinting of USDA–ARS national plant germplasm system collection. Crop Science 54: 2140–2151.

Jaccoud D, Peng K, Feinstein D, Kilian A. 2001. Diversity arrays: a solid state technology for sequence information independent genotyping. Nucleic Acids Research 29: e25. doi:10.1093/nar/29.4.e25. PubMed PMC

Janssens SB, Vandelook F, De Langhe E, et al. 2016. Evolutionary dynamics and biogeography of Musaceae reveal a correlation between the diversification of the banana family and the geological and climatic history of Southeast Asia. New Phytologist 210: 1453–1465. PubMed PMC

Kagy V, Wong M, Vandenbroucke H, et al. 2016. Traditional banana diversity in Oceania: an endangered heritage. PLoS One 11: e0151208. doi:10.1371/journal.pone.0151208. PubMed PMC

Kilian A, Wenzl P, Huttner E, et al. 2012. Diversity Arrays Technology: a generic genome profiling technology on open platforms. Methods in Molecular Biology 888: 67–89. PubMed

Krieke CM, Van Eck HJ, Lebot V. 2004. Genetic of taro, Colocasia esculenta (L.) Schott, in Southeast Asia and the Pacific. Theorical and Applied Genetics 109: 761–768. PubMed

Lebot V. 1999. Biomolecular evidence for plant domestication in Sahul. Genetic Resources and Crop Evolution 46: 619–628.

Li LF, Wang HY, Zhang C, et al. 2013. Origins and domestication of cultivated banana inferred from chloroplast and nuclear genes. PLoS One 8(11): e80502. doi:10.1371/journal.pone.0080502. PubMed PMC

Meirmans PG, Van Tienderen PH. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4: 792–794.

Meirmans PG. 2015. Seven common mistakes in population genetics and how to avoid them. Molecular Ecology 24: 3223–3231. PubMed

Noyer JL, Causse S, Tomepke K, Bouet A, Baurens FC. 2005. A new image of plantain diversity assessed by SSR, AFLP and MSAP markers. Genetica 124: 61–69. PubMed

Perrier X, Jacquemoud-Collet JP. 2006. DARwin software version 5.0. CIRAD: http://www.darwin.cirad.fr/darwin.

Perrier X, Flori A, Bonnot F. 2003. Data analysis methods In: P Hamon, M Seguin, X Perrier, JC Glaszmann, eds. Genetic diversity of cultivated tropical plants. Montpellier: Enfield, Sciences Publisher, 43–76.

Perrier X, Bakry F, Carreel F, et al. 2009. Combining biological approaches to shed light on the evolution of edible bananas. Ethnobotany Research and Applications 7: 199–216.

Perrier X, De Langhe E, Donohue M, et al. 2011. Multidisciplinary perspectives on banana (Musa spp.) domestication. Proceedings of the National Academy of Sciences of the USA 108: 11311–11318. PubMed PMC

Pritchard JK, Stephens M, Donnelly PJ. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959. PubMed PMC

Raboin LM, Carreel F, Noyer JL, et al. 2005. Diploid ancestors of triploid export banana cultivars: molecular identification of 2n restitution gamete donors and n gamete donors. Molecular Breeding 16: 333–341.

Risterucci AM, Hippolyte I, Perrier X, et al. 2009. Development and assessment of diversity arrays technology for high-throughput DNA analyses in Musa. Theoretical and Applied Genetics 119: 1093–1103. PubMed

Roorkiwal M, von Wettberg EJ, Upadhyaya HD, Warschefsky E, Rathore A, Varshney RK. 2014. Exploring germplasm diversity to understand the domestication process in Cicer spp. using SNP and DArT Markers. PLoS One 9: e102016. doi:10.1371/journal.pone.0102016. PubMed PMC

Shepherd K. 1999. Cytogenetics of the genus Musa. Montpellier: INIBAP.

Simmonds NW. 1962. The evolution of bananas. London: Longmans.

Simmonds NW, Shepherd K. 1955. The taxonomy and origins of the cultivated bananas. Journal of the Linnean Society of London 55: 302–312.

Sokal RR, Michener CD. 1958. A statistical method for evaluating systematic relationships. Scientific Bulletin of the University of Kansas 38: 1409–1438.

Ude G, Pillay M, Nwakanma D, Tenkouano A. 2002. Genetic diversity in Musa acuminata Colla and Musa balbisiana Colla and some of their natural hybrids using AFLP markers. Theoretical and Applied Genetics 104: 1246–1252. PubMed

Valmayor RV. 2001. Classification and characterization of Musa exotica, M. alinsanaya and M. acuminata ssp. errans. Infomusa 10: 35–39.

Valmayor RV, Jamaluddin SH, Silayoi B, et al. 2000. Banana cultivars names and synonyms in South-East Asia. Los Baños: INIBAP.

Visser B, Ramanatha Rao V. 2005. Gene flow and the management of ex-situ collections In: C de Vicente, ed. Issues on gene flow and germplasm management. Topical Reviews in Agricultural Biodiversity. Rome: IPGRI.

Wittenberg AH, van der Lee T, Cayla C, Kilian A, Visser RG, Schouten HJ. 2005. Validation of the high-throughput marker technology DArT using the model plant Arabidopsis thaliana. Molecular Genetics and Genomics 274: 30–39. PubMed

Striking variation in chromosome structure within Musa acuminata subspecies, diploid cultivars, and F1 diploid hybrids

Molecular and Cytogenetic Study of East African Highland Banana

A Genome-Wide Association Study on the Seedless Phenotype in Banana (Musa spp.) Reveals the Potential of a Selected Panel to Detect Candidate Genes in a Vegetatively Propagated Crop