Oligo painting FISH was established to identify all chromosomes in banana (Musa spp.) and to anchor pseudomolecules of reference genome sequence of Musa acuminata spp. malaccensis "DH Pahang" to individual chromosomes in situ. A total of 19 chromosome/chromosome-arm specific oligo painting probes were developed and were shown to be suitable for molecular cytogenetic studies in genus Musa. For the first time, molecular karyotypes of diploid M. acuminata spp. malaccensis (A genome), M. balbisiana (B genome), and M. schizocarpa (S genome) from the Eumusa section of Musa, which contributed to the evolution of edible banana cultivars, were established. This was achieved after a combined use of oligo painting probes and a set of previously developed banana cytogenetic markers. The density of oligo painting probes was sufficient to study chromosomal rearrangements on mitotic as well as on meiotic pachytene chromosomes. This advance will enable comparative FISH mapping and identification of chromosomal translocations which accompanied genome evolution and speciation in the family Musaceae.

Banana Breeding International Institute of Tropical Agriculture Arusha Tanzania

Banana Breeding International Institute of Tropical Agriculture Kampala Uganda

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 Czech Academy of Sciences Centre of the Region Hana for Biotechnological and Agricultural Research Olomouc Czechia

Zobrazit více v PubMed

Albert P. S., Zhang T., Semrau K., Rouillard J. M., Kao Y. H., Wang C. R. (2019). Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc. Natl. Acad. Sci. U. S. A. 116 (5), 1679–1685. 10.1073/pnas.1813957116 PubMed DOI PMC

Amosova A. V., Bolsheva N. L., Zoshchuk S. A., Twardovska M. O., Yurkevich O. Y., Andreev I. O., et al. (2017). (A) Comparative molecular cytogenetic characterization of seven Deschampsia (Poaceae) species. PloS One 12 (4), e0175760. 10.1371/journal.pone.0175760 PubMed DOI PMC

Argent G. C. G. (1976). The wild bananas of Papua New Guinea. Notes R. Bot. Gard. Edinburgh. 35 (1), 77–114.

Asif M. J., Mak C., Othman R. Y. (2001). Characterization of indigenous Musa species based on flow cytometric analysis of ploidy and nuclear DNA content. Caryologia. 54 (2), 161–168. 10.1080/00087114.2001.10589223 DOI

Badaeva E. D., Amosova A. V., Goncharov N. P., Macas J., Ruban A. S., Grechishnikova I. V., et al. (2015). A set of cytogenetic markers allows the precise identification of all A-genome chromosomes in diploid and polyploid wheat. Cytogenet. Genome Res. 146 (1), 71–79. 10.1159/000433458 PubMed DOI

Balint-Kurti P., Clendennen S., Doleželová M., Valárik M., Doležel J., Beetham P. R., et al. (2000). Identification and chromosomal localization of the monkey retrotransposon in Musa sp. Mol. Gen. Genet. 263 (6), 908–915. 10.1007/s004380000265 PubMed DOI

Bartoš J., Alkhimova O., Doleželová M., De Langhe 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

Baurens F. C., Martin G., Hervouet C., Salmon F., Yohomé D., Ricci S. (2019). Recombination and large structural variations shape interspecific edible bananas genomes. Mol. Biol. Evol. 36 (1), 97–111. 10.1093/molbev/msy199 PubMed DOI PMC

Belser C., Istace B., Denis E., Dubarry M., Baurens F. C., Falentin C. (2018). Chromosome-scale assemblies of plant genomes using nanopore long reads and optical maps. Nat. Plants. 4 (11), 879–887. 10.1038/s41477-018-0289-4 PubMed DOI

Braz G. T., He L., Zhao H., Zhang T., Semrau K., Rouillard J. M. (2018). Comparative oligo-FISH mapping: An efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics. 208 (2), 513–523. 10.1534/genetics.117.300344 PubMed DOI PMC

Brown A., Tumuhimbise R., Amah D., Uwimana B., Nyine M., Mduma H. (2017). The genetic improvement of bananas and plantains (Musa spp.) In Genetic Improvement of Tropical Crops Vol. pp. Campos, HCaligari, PDS. Cham: Springer, 219–240.

Carreel F., Fauré S., González de León D., Lagoda P. J. L., Perrier X., Bakry F. (1994). Evaluation of the genetic diversity in diploid bananas (Musa sp.). Genet. Sel. Evol. 26 (Suppl 1), 125–136. 10.1051/gse:19940709 DOI

Cheesman E. E. (1947). Classification of the bananas. The genus Ensete Horan and the genus Musa L. Kew. Bull. 2 (2), 97–117. 10.2307/4109206 DOI

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

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

Cremer T., Cremer S. (2001). (B) Chromosome territories, nuclear architecture and gene regulation in mammalian cells.. Nat. Rev. Genet. 2 (4), 292–301. 10.1038/35066075 PubMed DOI

D’Hont A., Paget-Goy A., Escoute J., Carreel F. (2000). The interspecific genome structure of cultivated banana, Musa spp. revealed by genomic DNA in situ hybridization. Theor. Appl. Genet. 100, 177–183. 10.1007/s001220050024 DOI

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

Danilova T. V., Friebe B., Gill B. S. (2014). Development of wheat single gene FISH map for analyzing homoeologous relationship and chromosomal rearrangements within the triticeae. Theor. Appl. Genet. 127 (3), 715–730. 10.1007/s00122-013-2253-z PubMed DOI PMC

Davey M. W., Gudimella R., Harikrishna J. A., Sin L. W., Khalid N., Keulemans J. (2013). A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genomics 14, 683. 10.1186/1471-2164-14-683 PubMed DOI PMC

De Capdeville G., Souza Junior M. T., Szinay D., Diniz L. E. C., Wijnker E., Swennen R., et al. (2009). The potential of high-resolution BAC-FISH in banana breeding. Euphytica 166, 431–443. 10.1007/s10681-008-9830-2 DOI

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

Doležel J., Doleželová M., Roux N., Van den houwe I. (1998). A novel method to prepare slides for high resolution chromosome studies in Musa spp. Infomusa 7, 3–4.

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

Dupouy M., Baurens F. C., Derouault P., Hervouet C., Cardi C., Cruaud C., et al. (2019). Two large reciprocal translocations characterized in the disease resistance-rich burmannica genetic group of Musa acuminata. Ann. Bot. XX, 1–11. 10.1093/aob/mcz078 PubMed DOI PMC

Ferguson-Smith M. A., Trifonov V. (2007). Mammalian karyotype evolution. Nat. Rev. Genet. 8 (12), 950–962. 10.1038/nrg2199 PubMed DOI

Filiault D. L., Ballerini E. S., Mandáková T., Aköz G., Derieg N. J., Schmutz J., et al. (2018). The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history. eLife 7, e36426. 10.7554/eLife.36426 PubMed DOI PMC

Fukui K., Kamisugi Y., Sakai F. (1994). Physical mapping of 5S rDNA loci by direct-cloned biotinylated probes in barley chromosomes. Genome. 37 (1), 105–111. 10.1139/g94-013 PubMed DOI

Gill B. S., Kimber G. (1977). Recognition of translocations and alien chromosome transfers in wheat by the Giemsa C-banding technique. Crop Sci. 17, 264–266. 10.2135/cropsci1977.0011183X001700020008x DOI

Gill B. S., Friebe B., Endo T. R. (1991). Standard karyotype and nomenclature system for description of chromosome bands and structural aberrations in wheat (Triticum aestivum). Genome 34, 830–839. 10.1139/g91-128 DOI

Greilhuber J. (1977). Why plant chromosomes do not show G-bands. Theor. Appl. Genet. 50 (3), 121–124. 10.1007/BF00276805 PubMed DOI

Häkkinen M. (2013). Reappraisal of sectional taxonomy in Musa (Musaceae). Taxon. 62 (4), 809–813. 10.12705/624.3 DOI

Hamilton J. P., Buell C. R. (2012). Advances in plant genome sequencing. Plant J. 70 (1), 177–190. 10.1111/j.1365-313X.2012.04894.x PubMed DOI

Han Y., Zhang T., Thammapichai P., Weng Y., Jiang J. (2015). Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics. 200, 771–779. 10.1534/genetics.115.177642 PubMed DOI PMC

He L., Braz G. T., Torres G. A., Jiang J. M. (2018). Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127, 505–513. 10.1007/s00412-018-0682-9 PubMed DOI

Hou L., Xu M., Zhang T., Xu Z., Wang W., Zhang J., et al. (2018). BMC Plant Biol. 18 (1), 110. 10.1186/s12870-018-1325-2 PubMed DOI PMC

Hřibová E., Doleželová M., Town C. D., Macas J., Doležel J. (2007). Isolation and characterization of the highly repeated fraction of the banana genome. Cytogenet. Genome Res. 119 (3-4), 268–274. 10.1159/000112073 PubMed DOI

Hřibová E., Doleželová M., Doležel J. (2008). Localization of BAC clones on mitotic chromosomes of Musa acuminata using fluorescence in situ hybridization. Biol. Plant 52, 445–452. 10.1007/s10535-008-0089-1 DOI

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

Idziak D., Hazuka I., Poliwczak B., Wiszynska A., Wolny E., Hasterok R. (2014). Insight into the karyotype evolution of Brachypodium species using comparative chromosome barcoding. PloS One 9 (3), e93503. 10.1371/journal.pone.0093503 PubMed DOI PMC

International Plant Genetic Resources Institute-International Network for the Improvement of Banana and Plantain/Centre de Coopération internationale en recherche agronomique pour le développement [IPGRI-INIBAP/CIRAD]International Plant Genetic Resources Institute-International Network for the Improvement of Banana and Plantain/Centre de Coopération internationale en recherche agronomique pour le développement [IPGRI-INIBAP/CIRAD] (1996). Description for Banana (Musa spp.). Int. Network for the Improvement of Banana and Plantain, Montpellier, France; Centre de coopération int. en recherche agronomique pour le développement, Montpellier, France; International Plant Genetic Resources Institute Press, Rome.

Janssens S. B., Vandelook F., De Langhe E., Verstraete B., Smets E., Van den Houwe I., 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 Phytol. 210 (4), 1453–1465. 10.1111/nph.13856 PubMed DOI PMC

Jiang J., Gill B. S., Wang G. L., Ronald P. C., Ward D. C. (1995). Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc. Natl. Acad. Sci. U. S. A. 92 (10), 4487–4491. 10.1073/pnas.92.10.4487 PubMed DOI PMC

Jiang J. (2019). Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosom. Res. 27 (3), 153–165. 10.1007/s10577-019-09607-z PubMed DOI

Křivánková A., Kopecký D., Stočes Š., Doležel J., Hřibová E. (2017). Repetitive DNA: a versatile tool for karyotyping in Festuca pratensis Huds. Cytogenet. Genome Res. 151 (2), 96–105. 10.1159/000462915 PubMed DOI

Kamaté K., Brown S., Durand P., Bureau J. M., De Nay D., Trinh T. H. (2001). Nuclear DNA content and base composition in 28 taxa of Musa. Genome. 44, 622–627. 10.1139/g01-058 PubMed DOI

Kim J. S., Childs K. L., Islam-Faridi M. N., Menz M. A., Klein R. R., Klein P. E. (2002). Integrated karyotyping of sorghum by in situ hybridization of landed BACs. Genome. 45, 402–412. 10.1139/g01-141 PubMed DOI

Koo D. H., Zhao H., Jiang J. (2016). Chromatin-associated transcripts of tandemly repetitive DNA sequences revealed by RNA-FISH. Chromosome Res. 24 (4), 467–480. 10.1007/s10577-016-9537-5 PubMed DOI

Lapitan N. L. V., Brown S. E., Kennard W., Stephens J. L., Knudson D. L. (1997). FISH physical mapping with barley BAC clones. Plant J. 11, 149–156. 10.1046/j.1365313X.1997.11010149.x DOI

Li L. F., Häkkinen 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), 1–10. 10.1016/j.ympev.2010.06.021 PubMed DOI

Liu W., Rouse M., Friebe B., Jin Y., Gill B., Pumphrey M. O. (2011). Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from Aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosome Res. 19 (5), 669–682. 10.1007/s10577-011-9226-3 PubMed DOI

Lysák M. A., Doleželová M., Horry J. P., Swennen R., Doležel J. (1999). Flow cytometric analysis of nuclear DNA content in Musa. Theor. Appl. Genet. 98 (8), 1344–1350. 10.1007/s001220051201 DOI

Lysák M. A., Fransz P. F., Ali H. B. M., Schubert I. (2001). Chromosome painting in A. thaliana. Plant J. 28, 689–697. 10.1046/j.1365-313x.2001.01194.x PubMed DOI

Mandáková T., Lysák M. A. (2008). Chromosomal phylogeny and karyotype evolution in x = 7 crucifer species (Brassicaceae). Plant Cell 20, 2559–2570. 10.1105/tpc.108.062166 PubMed DOI PMC

Mandáková T., Marhold K., Lysák M. A. (2013). The widespread crucifer species Cardamine flexulosa is an allotetraploid with a conserved subgenomic structure. New Phytol. 201, 982–992. 10.1111/nph.12567 PubMed DOI

Martin G., Baurens F. C., Droc G., Rouard M., Cenci A., Kilian A., et al. (2016). Improvement of the banana “Musa acuminata“ reference sequence using NGS data and semi-automated bioinformatics methods. BMC Genomics 17, 1–12. 10.1186/s12864-016-2579-4 PubMed DOI PMC

Meng Z., Zhang Z. L., Yan T. Y., Lin Q. F., Wang Y., Huang W. Y., et al. (2018). Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front. Plant Sci. 9, 1624. 10.3389/fpls.2018.01624 PubMed DOI PMC

Murata M., Heslop-Harrison J. S., Motoyoshi F. (1997). Physical mapping of the 5S ribosomal RNA genes in Arabidopsis thaliana by multi-color fluorescence in situ hybridization with cosmid clones. Plant J. 12 (1), 31–37. 10.1046/j.1365-313X.1997.12010031.x PubMed DOI

Murgha Y. E., Rouillard J. M., Gulari E. (2014). Methods for the preparation of large quantities of complex single-stranded oligonucleotide libraries. PloS One 9, e94752. 10.1371/journal.pone.0094752 PubMed DOI PMC

Němečková A., Christelová P., Čížková J., Nyine M., Van den houwe I., Svačina R., et al. (2018). Molecular and cytogenetic study of East African Highland Banana. Front. Plant Sci. 9, 1371. 10.3389/fpls.2018.01371 PubMed DOI PMC

Neumann P., Navrátilová A., Koblížková A., Kejnovský E., Hřibová E., Hobza R., et al. (2011). Plant cytogenetic perspective. Mob. DNA 2 (1), 4. 10.1186/1759-8753-2-4 PubMed DOI PMC

Novák P., Hřibová E., Neumann P., Koblížková A., Doležel J., Macas J. (2014). Genome-wide analysis of repeat diversity across the family Musaceae. PloS One 9 (6), e98918. 10.1371/journal.pone.0098918 PubMed DOI PMC

Ortiz R., Swennen R. (2014). From crossbreeding to biotechnology-facilitated improvement of banana and plantain. Biotechnol. Adv. 32, 158–169. 10.1016/j.biotechadv.2013.09.010 PubMed DOI

Osuji J. O., Crouch J., Harrison G., Heslop-Harrison J. S. (1998). Molecular cytogenetics of Musa species, cultivars and hybrids: location of 18S-5.8S-25S and 5S rDNA and telomere-like sequences. Ann. Bot. 82, 243–248. 10.1006/anbo.1998.0674 DOI

Qu M., Li K., Han Y., Chen L., Li Z., Han Y. (2017). Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet. Genome Res. 153, 158–164. 10.1159/000485283 PubMed DOI

Said M., Hřibová E., Danilova T. V., Karafiátová M., Čížková J., Friebe B., et al. (2018). The Agropyron cristatum karyotype, chromosome structure and cross-genome homoeology as revealed by fluorescence in situ hybridization with tandem repeats and wheat single-gene probes. Theor. Appl. Genet. 131 (10), 2213–2227. 10.1007/s00122-018-3148-9 PubMed DOI PMC

Schubert I., Fransz P. F., Fuchs J., De Jong J. H. (2001). Chromosome painting in plants. Methods Cell Sci. 23, 57–69. 10.1023/A:1013137415093 PubMed DOI

Simmonds N. W., Shepherd K. (1955). The taxonomy and origins of the cultivated bananas. J. Linn. Soc. Bot. 55, 302–312. 10.1111/j.1095-8339.1955.tb00015.x DOI

Simmonds N. W. (1956). Botanical results of the banana collecting expeditions, 1954-5. Kew Bull. 11, 463–489. 10.2307/4109131 DOI

Speicher M. R., Ballard S. G., Ward D. C. (1996). Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nat. Genet. 12 (4), 368–375. 10.1038/ng0496-368 PubMed DOI

The Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 6814, 796–815. 10.1038/35048692 PubMed DOI

The International Brachypodium Initiative (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463 (7282), 763–768. 10.1038/nature08747 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 (2), 89–100. 10.1023/A:1014945730035 PubMed DOI

Xin H., Zhang T., Han Y., Wu Y., Shi J., Xi M., et al. (2018). Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma. 127, 313–321. 10.1007/s00412-018-0664-y PubMed DOI

Zimin A. V., Puiu D., Hall R., Kingan S., Clavijo B. J., Salzberg S. L. (2017). The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. Gigascience. 6 (11), 1–7. 10.1093/gigascience/gix097 PubMed DOI PMC

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

Bulked Oligo-FISH for Chromosome Painting and Chromosome Barcoding

Advances in the Molecular Cytogenetics of Bananas, Family Musaceae

Chromosome and Genome Diversity in the Genus Trifolium (Fabaceae)

Limitation of current probe design for oligo-cross-FISH, exemplified by chromosome evolution studies in duckweeds

The Evolution of Chromosome Numbers: Mechanistic Models and Experimental Approaches

Karyotype Differentiation in Cultivated Chickpea Revealed by Oligopainting Fluorescence in situ Hybridization

The Puzzling Fate of a Lupin Chromosome Revealed by Reciprocal Oligo-FISH and BAC-FISH Mapping

Chromosome Painting in Cultivated Bananas and Their Wild Relatives (Musa spp.) Reveals Differences in Chromosome Structure

Fonio millet genome unlocks African orphan crop diversity for agriculture in a changing climate

The Formation of Sex Chromosomes in Silene latifolia and S. dioica Was Accompanied by Multiple Chromosomal Rearrangements