East African highland bananas (EAHBs) are staple food crop in Uganda, Tanzania, Burundi, and other countries in the African Great Lakes region. Even though several morphologically different types exist, all EAHBs are triploid and display minimal genetic variation. To provide more insights into the genetic variation within EAHBs, genotyping using simple sequence repeat (SSR) markers, molecular analysis of ITS1-5.8S-ITS2 region of ribosomal DNA locus, and the analysis of chromosomal distribution of ribosomal DNA sequences were done. A total of 38 triploid EAHB accessions available in the Musa germplasm collection (International Transit Centre, Leuven, Belgium) were characterized. Six diploid accessions of Musa acuminata ssp. zebrina, ssp. banksii, and ssp. malaccensis representing putative parents of EAHBs were included in the study. Flow cytometric estimation of 2C nuclear DNA content revealed small differences (max ~6.5%) in genome size among the EAHB clones. While no differences in the number of 45S and 5S rDNA loci were found, genotyping using 19 SSR markers resulted in grouping the EAHB accessions into four clusters. The DNA sequence analysis of the internal transcribed spacer region indicated a relation of EAHB clones with M. acuminata and, surprisingly, also with M. schizocarpa. The results suggest that EAHB cultivars originated from a single hybrid clone with M. acuminata ssp. zebrina and ssp. banksii being its most probable parents. However, M. schizocarpa seems to have contributed to the formation of this group of banana.

Bioversity International Banana Genetic Resources Heverlee Belgium

Division of Crop Biotechnics Laboratory of Tropical Crop Improvement Katholieke Universiteit Leuven Leuven Belgium

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Olomouc Czechia

International Institute of Tropical Agriculture Banana Breeding Arusha Tanzania

International Institute of Tropical Agriculture Banana Breeding Kampala Uganda

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Alvarez I., Wendel J. F. (2003). Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29, 417–434. 10.1016/S1055-7903(03)00208-2 PubMed DOI

Bartoš J., Alkhimova O., Doleželová M., DeLanghe E., Doležel J. (2005). Nuclear genome size and genomic distribution of ribosomal DNA in Musa and Ensete (Musaceae): taxonomic implications. Cytogenet. Genome Res. 109, 50–57. 10.1159/000082381 PubMed DOI

Boonruangrod R., Fluch S., Burg K. (2009). Elucidation of origin of the present day hybrid banana cultivars using the 5′ETS rDNA sequence information. Mol. Breed. 24, 77–91. 10.1007/s11032-009-9273-z DOI

Carreel F., De Leon D. G., Lagoda P., Lanaud C., Jenny C., Horry J. P., et al. . (2002). Ascertaining maternal and paternal lineage within Musa by chloroplast and mitochondrial DNA RFLP analyses. Genome 45, 679–692. 10.1139/g02-033 PubMed DOI

Carreel F., Fauré S., González de León D., Lagoda P. J. L., Perrier X., Bakry F., et al. (1994). Evaluation of the genetic diversity in diploid bananas (Musa sp.). Genet. Sel. Evol. 26, 125s−136s.

Christelová P., De Langhe E., Hřibová E., Čížková J., Sardos J., Hušáková M., et al. (2017). Molecular and cytological characterization of the global Musa germplasm collection provides insights into the treasure of banana diversity. Biodivers. Conserv. 26, 801–824. 10.1007/s10531-016-1273-9 DOI

Christelová P., Valárik M., Hřibová E., Van den Houwe I., Channeliere S., Roux N., et al. . (2011). A platform for efficient genotyping in Musa using microsatellite markers. AoB Plants 2011:plr024. 10.1093/aobpla/plr024 PubMed DOI PMC

Čížková J., Hřibová E., Christelová P., Van den Houwe I., Häkkinen M., Roux N., et al. . (2015). Molecular and cytogenetic characterization of wild Musa species. PLoS ONE 10:e0134096. 10.1371/journal.pone.0134096 PubMed DOI PMC

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

Crane M. B., Lawrance W. J. C. (1956). The Genetics of Garden Plants, 4th Edn. London: Macmillan.

Crouch H. K., Crouch J. H., Jarret R. L., Cregan P. B., Ortiz R. (1998). Segregation of microsatellite loci in haploid and diploid gametes of Musa. Crop Sci. 38, 211–217. 10.2135/cropsci1998.0011183X003800010035x DOI

De Langhe E., Hřibová E., Carpentier S., Doležel J., Swennen R. (2010). Did backcrossing contribute to the origin of hybrid edible bananas? Ann. Bot. 106, 849–857. 10.1093/aob/mcq187 PubMed DOI PMC

De Langhe E. A. L. (1961). La taxonomie du bananier plantain en Afrique Equatoriale. J. Agric. Trop. Bot. Appl. 8, 419–449.

D'Hont A., Denoeud F., Aury J. M., Baurens F. C., Carreel F., Garsmeur O., et al. . (2012). The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213–217. 10.1038/nature11241 PubMed DOI

Doležel J., Bartos J., Voglmayr H., Greilhuber J. (2003). Nuclear DNA content and genome size of trout and human. Cytometry A 51, 127–128. 10.1002/cyto.a.10013 PubMed DOI

Doležel J., Doleželová M., Novák F. J. (1994). Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata and M. balbisiana). Biol. Plant. 36, 351–357. 10.1007/BF02920930 DOI

Doleželová M., Valárik M., Swennen R., Horry J. P., Doležel J. (1998). Physical mapping of the 18S-25S and 5S ribosomal RNA genes in diploid bananas. Biol. Plant. 41, 497–505. 10.1023/A:1001880030275 DOI

Duchoslav M., Šafářová L., Jandová M. (2013). Role of adaptive and non-adaptive mechanisms forming complex patterns of genome size variation in six cytotypes of polyploid Allium oleraceum (Amaryllidaceae) on a continental scale. Ann. Bot. 111, 419–431. 10.1093/aob/mcs297 PubMed DOI PMC

Eckert A. J., Liechty J. D., Tearse B. R., Pande B., Neale D. B. (2010). DnaSAM: software to perform neutrality testing for large datasets with complex null models. Mol. Ecol. Resour. 10, 542–545. 10.1111/j.1755-0998.2009.02768.x PubMed DOI

Gascuel O. (1997). BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14, 685–695. 10.1093/oxfordjournals.molbev.a025808 PubMed DOI

Gouy M., Guindon S., Gascuel O. (2010). SeaView version 4: a multiple graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27, 221–224. 10.1093/molbev/msp259 PubMed DOI

Guindon S., Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704. 10.1080/10635150390235520 PubMed DOI

Harpke D., Peterson A. (2008). 5.8S motifs for identification of pseudogenic ITS regions. Botany 86, 300–305. 10.1139/B07-134 PubMed DOI

Heslop-Harrison J. S., Schwarzacher T. (2007). Domestication, genomics and the future for banana. Ann. Bot. 100, 1073–1084. 10.1093/aob/mcm191 PubMed DOI PMC

Hippolyte I., Bakry F., Seguin M., Gardes L., Rivallan R., Risterucci A. M., et al. . (2010). A saturated SSR/DArT linkage map of Musa acuminata addressing genome rearrangements among bananas. BMC Plant Biol. 10:65. 10.1186/1471-2229-10-65 PubMed DOI PMC

Hippolyte I., Jenny C., Gardes L., Bakry F., Rivallan R., Pomies V., et al. . (2012). Foundation characteristics of edible Musa triploids revealed from allelic distribution of SSR markers. Ann. Bot. 109, 937–951. 10.1093/aob/mcs010 PubMed DOI PMC

Hřibová E., Čížková J., Christelová P., Taudien S., De Langhe E., Doležel J. (2011). The ITS-5.8S-ITS2 sequence region in the Musaceae: structure, diversity and use in molecular phylogeny. PLoS ONE 6:e17863. 10.1371/journal.pone.0017863 PubMed DOI PMC

Hřibová E., Neumann P., Matsumoto T., Roux N., Macas J, Doležel J. (2010). Repetitive part of the banana (Musa acuminata) genome investigated by low-depth 454 sequencing. BMC Plant Biol. 10:204. 10.1186/1471-2229-10-204 PubMed DOI PMC

Huson D. H., Bryant D. (2006). Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267. 10.1093/molbev/msj030 PubMed DOI

Karamura D. A. (1998). Numerical Taxonomic Studies of the East African Highland Bananas (Musa AAA-East Africa) in Uganda. Montpelier: INIBAP.

Katoh K., Kuma K., Toh H., Miyata T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518. 10.1093/nar/gki198 PubMed DOI PMC

Kitavi M., Downing T., Lorenzen J., Karamura D., Onyango M., Nyine M., et al. . (2016). The triploid East African Highland Banana (EAHB) genepool is genetically uniform arising from a single ancestral clone that underwent population expansion by vegetative propagation. Theor. Appl. Genet. 129, 547–561. 10.1007/s00122-015-2647-1 PubMed DOI

Lagoda P. J., Noyer J. L., Dambier D., Baurens F. C., Grapin A., Lanaud C. (1998). Sequence tagged microsatellite site (STMS) markers in the Musaceae. Mol. Ecol 7, 659–663. PubMed

Lejju B. J., Robertshaw P., Taylor D. (2006). Africa's earliest bananas? J. Archaeol. Sci. 33, 102–113. 10.1016/j.jas.2005.06.015 DOI

Lejju B. J., Taylorl D., Robertshaw P. (2005). Late-Holocene environmental variability at Munsa archaeological site, Uganda: a multicore, multiproxy approach. Holocene 15, 1044–1061. 10.1191/0959683605hl877ra DOI

Li L.-F., Hakkinen M., Yuan Y.-M., Hao G., Ge X.-J. (2010). Molecular phylogeny and systematics of the banana family (Musaceae) inferred from multiple nuclear and chloroplast DNA fragments, with a special reference to the genus Musa. Mol. Phylogenet. Evol. 57, 1–10. 10.1016/j.ympev.2010.06.021 PubMed DOI

Li L. F., Wang H. Y., Zhang C., Wang X. F., Shi F. X., Chen W. N., et al. . (2013). Origins and domestication of cultivated banana inferred from chloroplast and nuclear genes. PLoS ONE 8:e80502. 10.1371/journal.pone.0080502 PubMed DOI PMC

Li P., Qi Z. C., Liu L. X., Ohi-Toma T., Lee J., Hsieh T. H., et al. . (2017). Molecular phylogenetics and biogeography of the mint tribe Elsholtzieae (Nepetoideae, Lamiaceae), with an emphasis on its diversification in East Asia. Sci. Rep. 7:2057. 10.1038/s41598-017-02157-6 PubMed DOI PMC

Lira-Medeiros C. F., Parisod C., Fernandes R. A., Mata C. S., Cardoso M. A., Ferreira P. C. (2010). Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLOS ONE 5:e10326. 10.1371/journal.pone.0010326 PubMed DOI PMC

Liu A. Z., Kress W. J., Li D. Z. (2010). Phylogenetic analyses of the banana family (Musaceae) based on nuclear ribosomal (ITS) and chloroplast (trnL-F) evidence. Taxon 59, 20–28. 10.2307/27757047 DOI

Liu K., Muse S. V. (2005). PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21, 2128–2129. 10.1093/bioinformatics/bti282 PubMed DOI

Michener C. D., Sokal R. R. (1957). A quantitative approach to a problem of classification. Evolution 11, 490–499. 10.1111/j.1558-5646.1957.tb02884.x DOI

Nei M. (1973). Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. U.S.A. 70, 3321–3323. 10.1073/pnas.70.12.3321 PubMed DOI PMC

Nwakanma D. C., Pillay M., Okoli B. E., Tenkouano A. (2003). PCR-RFLP of ribosomal DNA internal transcribed spacer (ITS) provides markers for the A and B genomes in Musa L. Theor. Appl. Genet. 108, 154–159. 10.1007/s00122-003-1402-1 PubMed DOI

Ong-Abdullah M., Ordway J. M., Jiang N., Ooi S. E., Kok S. Y., Sarpan N., et al. . (2015). Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537. 10.1038/nature15365 PubMed DOI PMC

Perrier X., Bakry F., Carreel F., Jenny C., Horry J. P., Lebot V., et al. (2009). Combining biological approaches to shed light on the evolution of edible bananas. Ethnobot. Res. Appl. 7, 199–216. 10.17348/era.7.0.199-216 DOI

Perrier X., De Langhe E., Donohue M., Lentfer C., Vrydaghs L., Bakry F., et al. . (2011). Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc. Natl. Acad. Sci. U.S.A. 108, 11311–11318. 10.1073/pnas.1102001108 PubMed DOI PMC

Pillay M., Ogundiwin E., Nwakanma D. C., Ude G., Tenkouano A. (2001). Analysis of genetic diversity and relationships in East African banana germplasm. Theor. Appl. Genet. 102, 965–970. 10.1007/s001220000500 DOI

Poggio L., Realini M. F., Fourastie M. F., Garcia A. M., Gonzalez G. E. (2014). Genome downsizing and karyotyping constancy in diploid and polyploid congeners: a model of genome size variation. AoB Plants 6:plu029 10.1093/aobpla/plu029 PubMed DOI PMC

Sardos J., Perrier X., Doležel J., Hřibová E., Christelová P., Van den houwe I., et al. (2016). DArT whole genome profiling provides insights on the evolution and taxonomy of edible Banana (Musa spp.). Ann. Bot 118, 1269–1278. 10.1093/aob/mcw170 PubMed DOI PMC

Shepherd K. (1957). Banana cultivars in East Africa. Trop. Agric. 34, 277–286.

Ssebuliba R., Talengera D., Makumbi D., Namanya P., Tenkouano A., Tushemereirwe W., et al. (2006). Reproductive efficiency and breeding potential of East African highland (Musa AAA-EA) bananas. Field Crops Res. 95, 250–255. 10.1016/j.fcr.2005.03.004 DOI

Ssebuliba R. N., Rubaihayo P., Tenkouano A., Makumbi D., Talengera D., Magambo M. (2005). Genetic diversity among East African Highland bananas for female fertility. Afr. Crop Sci. J 13, 13–26.

Staden R. (1996). The Staden sequence analysis package. Mol Biotechnol. 5, 233–241. 10.1007/BF02900361 PubMed DOI

Tugume A. K., Lubega G. W., Rubaihayo P. R. (2002). Genetic diversity of East African Highland bananas using AFLP. Infomusa 11, 28–32.

Ude G., Pillay M., Ogundiwin E., Tenkouano A. (2003). Genetic diversity in an African plantain core collection using AFLP and RAPD markers. Theor. Appl. Genet. 107, 248–255. 10.1007/s00122-003-1246-8 PubMed DOI

Valárik M., Šimková H., Hřibová E., Šafář J., Doleželová M., Doležel J. (2002). Isolation, characterization and chromosome localization of repetitive DNA sequences in bananas (Musa spp.). Chromosome Res. 10, 89–100. 10.1023/A:1014945730035 PubMed DOI

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Advances in the Molecular Cytogenetics of Bananas, Family Musaceae

Telomere-to-telomere gapless chromosomes of banana using nanopore sequencing

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The Utility of Graph Clustering of 5S Ribosomal DNA Homoeologs in Plant Allopolyploids, Homoploid Hybrids, and Cryptic Introgressants

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Chromosome Painting Facilitates Anchoring Reference Genome Sequence to Chromosomes In Situ and Integrated Karyotyping in Banana (Musa Spp.)

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