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

. 2020 Oct 24 ; 21 (21) : . [epub] 20201024

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu srovnávací studie, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33114462

Grantová podpora
19-20303S Czech Science Foundation
LTT19 Ministry of Education, Youth and Sports of the Czech Republic
CZ.02.1.01/0.0/0.0/16_019/0000827 Ministry of Education, Youth and Sports of the Czech Republic

Edible banana cultivars are diploid, triploid, or tetraploid hybrids, which originated by natural cross hybridization between subspecies of diploid Musa acuminata, or between M. acuminata and diploid Musa balbisiana. The participation of two other wild diploid species Musa schizocarpa and Musa textilis was also indicated by molecular studies. The fusion of gametes with structurally different chromosome sets may give rise to progenies with structural chromosome heterozygosity and reduced fertility due to aberrant chromosome pairing and unbalanced chromosome segregation. Only a few translocations have been classified on the genomic level so far, and a comprehensive molecular cytogenetic characterization of cultivars and species of the family Musaceae is still lacking. Fluorescence in situ hybridization (FISH) with chromosome-arm-specific oligo painting probes was used for comparative karyotype analysis in a set of wild Musa species and edible banana clones. The results revealed large differences in chromosome structure, discriminating individual accessions. These results permitted the identification of putative progenitors of cultivated clones and clarified the genomic constitution and evolution of aneuploid banana clones, which seem to be common among the polyploid banana accessions. New insights into the chromosome organization and structural chromosome changes will be a valuable asset in breeding programs, particularly in the selection of appropriate parents for cross hybridization.

Zobrazit více v PubMed

FAOSTAT; Agriculture Organization of the United Nations; FAO. [(accessed on 30 January 2020)];2017 Available online: http://www.fao.org/home/en/

International Trade Statistics. [(accessed on 20 May 2020)];2019 Available online: https://www.wto.org/

Price N.S. The origin and development of banana and plantain cultivation. In: Gowen S., editor. Bananas and Plantains, World Crop Series. Springer; Dordrecht, The Netherlands: 1995.

Carreel F., Fauré S., Gonzalez de Leon D., Lagoda P.J.L., Perrier X., Bakry F., Tezenas du Montcel H., Lanaud C., Horry J.P. Evaluation of the genetic diversity in diploid bananas (Musa spp.) Genet. Sel. Evol. 1994;26:125–136. doi: 10.1186/1297-9686-26-S1-S125. DOI

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

Němečková A., Christelová P., Čížková J., Nyine M., van den Houwe I., Svačina R., Uwimana B., Swennen R., Doležel J., Hřibová E. Molecular and cytogenetic study of East African Highland Banana. Front. Plant Sci. 2018;9:1371. doi: 10.3389/fpls.2018.01371. PubMed DOI PMC

Perrier X., De Langhe E., Donohue M., Lentfer C., Vrydaghs L., Bakry F., Carreel F., Hippolyte I., Horry J.P., Jenny C., et al. Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc. Natl. Acad. Sci. USA. 2011;108:11311–11318. doi: 10.1073/pnas.1102001108. PubMed DOI PMC

Martin G., Carreel F., Coriton O., Hervouet C., Cardi C., Derouault P., Roques D., Salmon F., Rouard M., Sardos J., et al. Evolution of the banana genome (Musa acuminata) is impacted by large chromosomal translocations. Mol. Biol. Evol. 2017;34:2140–2152. doi: 10.1093/molbev/msx164. PubMed DOI PMC

WCSP World Checklist of Selected Plant Families. Facilitated by the Royal Botanic Gardens, Kew. [(accessed on 30 January 2020)];2018 Available online: http://wcsp.science.kew.org/

Rouard M., Droc G., Martin G., Sardos J., Hueber Y., Guignon V., Cenci A., Geigle B., Hibbins M.S., Yahiaoui N., et al. Three new genome assemblies support a rapid radiation in Musa acuminata (wild banana) Genome Biol. Evol. 2018;10:3129–3140. doi: 10.1093/gbe/evy227. PubMed DOI PMC

Sharrock S. Collecting Musa in Papua New Guinea. Identification of genetic diversity in the genus Musa. In: Jarret R.L., editor. International Network for the Improvement of Banana and Plantain. INIBAP; Montpellier, France: 1990. pp. 140–157.

Perrier X., Bakry F., Carreel F., Jenny F., Horry J.P., Lebot V., Hippolyte I. Combining biological approaches to shed light on the evolution of edible bananas. Ethnobot. Res. Appl. 2009;7:199–216. doi: 10.17348/era.7.0.199-216. DOI

Cheesman E.E. Classification of the bananas. Kew Bull. 1948;3:145–153. doi: 10.2307/4119749. DOI

De Langhe E., Vrydaghs L., De Maret P., Perrier X., Denham T.P. Why bananas matter: An introduction to the history of banana domestication. Ethnobot. Res. Appl. 2009;7:165–177. doi: 10.17348/era.7.0.165-177. DOI

Sand C. Petite histoire du peuplement de l’Océanie. In: Ricard M., editor. Migrations et Identités—Colloque CORAIL, Nouméa (PYF), 1988/11/21-22. Papeete. Université Française du Pacifique; 1989. [(accessed on 30 January 2020)]. pp. 39–40. Available online: http://www.documentation.ird.fr/hor/fdi:27803.

Denham T., Haberle S., Lentfer C. New evidence and revised interpretations of early agriculture in Highland New Guinea. Antiquity. 2004;78:839–857. doi: 10.1017/S0003598X00113481. DOI

Denham T. From domestication histories to regional prehistory: Using plants to re-evaluate early and mid-holocene interaction between New Guinea and Southeast Asia. Food Hist. 2010;8:3–22. doi: 10.1484/J.FOOD.1.100971. DOI

Kagy V., Wong M., Vandenbroucke H., Jenny C., Dubois C., Ollivier A., Cardi C., Mournet P., Tuia V., Roux N., et al. Traditional banana diversity in Oceania: An endangered heritage. PLoS ONE. 2016;11:e0151208. doi: 10.1371/journal.pone.0151208. PubMed DOI PMC

Simmonds N.W. The Evolution of the Bananas. Longmans; London, UK: 1962. p. 170. (Tropical Science Series).

Raboin L.M., Carreel F., Noyer J.L., Baurens F.C., Horry J.P., Bakry F., Tezenas Du Montcel H., Ganry J., Lanaud C., Lagoda P.J.L. Diploid ancestors of triploid export banana cultivars: Molecular identification of 2n restitution gamete donors and n gamete donors. Mol. Breed. 2005;16:333–341. doi: 10.1007/s11032-005-2452-7. DOI

Perrier X., Jenny C., Bakry F., Karamura D., Kitavi M., Dubois C., Hervouet C., Philippson G., De Langhe E. East African diploid and triploid bananas: A genetic complex transported from South-East Asia. Ann. Bot. 2019;123:19–36. doi: 10.1093/aob/mcy156. PubMed DOI PMC

Martin G., Cardi C., Sarah G., Ricci S., Jenny C., Fondi E., Perrier X., Glaszmann J.-C., D’Hont A., Yahiaoui N. Genome ancestry mosaics reveal multiple and cryptic contributors to cultivated banana. Plant. J. 2020;102:1008–1025. doi: 10.1111/tpj.14683. PubMed DOI PMC

Baurens F.C., Martin G., Hervouet C., Salmon F., Yohomé D., Ricci S., Rouard M., Habas R., Lemainque A., Yahiaoui N., et al. Recombination and large structural variations shape interspecific edible bananas genomes. Mol. Biol. Evol. 2019;36:97–111. doi: 10.1093/molbev/msy199. PubMed DOI PMC

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

Cooper H., Spillane C., Hodgkin T. Broadening the Genetic Bases of Crop. Production. FAO; Rome, Italy: 2001.

Tugume A.K., Lubega G.W., Rubaihayo P.R. Genetic diversity of East African Highland bananas using AFLP. Infomusa. 2003;11:28–32.

Kitavi M., Downing T., Lorenzen J., Karamura D., Onyango M., Nyine M., Ferguson M., Spillane C. 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. 2016;129:547–561. doi: 10.1007/s00122-015-2647-1. PubMed DOI

Christelová P., De Langhe E., Hřibová E., Čížková J., Sardos J., Hušáková M., van den Houwe I., Sutanto A., Kepler A.K., Swennen R., et al. Molecular and cytological characterization of the global Musa germplasm collection provides insights into the treasure of banana diversity. Biodivers. Conserv. 2017;26:801–824. doi: 10.1007/s10531-016-1273-9. DOI

Burke J.M., Arnold M.L. Genetics and the fitness of hybrids. Annu. Rev. Genet. 2001;35:31–52. doi: 10.1146/annurev.genet.35.102401.085719. PubMed DOI

Batte M., Swennen R., Uwimana B., Akech V., Brown A., Tumuhimbise R., Hovmalm H.P., Geleta M., Ortiz R. Crossbreeding East African Highland Bananas: Lessons learnt relevant to the botany of the crop after 21 years of genetic enhancement. Front. Plant. Sci. 2019;10:81. doi: 10.3389/fpls.2019.00081. PubMed DOI PMC

Bakry F., Horry J.P. Tetraploid hybrids from interploid 3×/2× crosses in cooking bananas. Fruits. 1992;47:641–655.

Tomepke K., Jenny C., Escalant J.-V. A review of conventional improvement strategies for Musa. InfoMusa. 2004;13:2–6.

Ortiz R. Conventional banana and plantain breeding. Acta Hortic. 2013;986:177–194. doi: 10.17660/ActaHortic.2013.986.19. DOI

Nyine M., Uwimana B., Swennen R., Batte M., Brown A., Christelová P., Hřibová E., Lorenzen J., Doležel J. Trait variation and genetic diversity in a banana genomic selection training population. PLoS ONE. 2017;12:e0178734. doi: 10.1371/journal.pone.0178734. PubMed DOI PMC

Amorim E.P., Silva S.O., Amorim V.B.O., Pillay M. Quality improvement of cultivated Musa. In: Pillay M., Tenkouano A., editors. Banana Breeding: Progress and Challenges. CRC Press; New York, NY, USA: 2011. pp. 252–280.

Amorim E.P., dos Santos-Serejo J.A., Amorim V.B.O., Ferreira C.F., Silva S.O. Banana breeding at embrapa cassava and fruits. Acta Hortic. 2013;968:171–176. doi: 10.17660/ActaHortic.2013.986.18. DOI

Tenkouano A., Vuylsteke D., Agogbua J.U., Makumbi D., Swennen R., Ortiz R. Diploid banana hybrids TMB2x5105-1 and TMB2x9128-3 with good combining ability, resistance to black sigatoga and nematodes. HortScience. 2003;38:468–472. doi: 10.21273/HORTSCI.38.3.468. DOI

Šimoníková D., Němečková A., Karafiátová M., Uwimana B., Swennen R., Doležel J., Hřibová E. Chromosome painting facilitates anchoring reference genome sequence to chromosomes in situ and integrated karyotyping in banana (Musa spp.) Front. Plant. Sci. 2019;10:1503. doi: 10.3389/fpls.2019.01503. PubMed DOI PMC

De Langhe E., Perrier X., Donohue M., Denham T. The original Banana Split: Multi-disciplinary implications of the generation of African and Pacific Plantains in Island Southeast Asia. Ethnobot. Res. Appl. 2015;14:299–312. doi: 10.17348/era.14.0.299-312. DOI

Do Amaral C.M., de Almeida dos Santos-Serejo J., de Oliveira e Silva S., da Silva Ledo C.A., Amorim E.P. Agronomic characterization of autotetraploid banana plants derived from ‘Pisang Lilin’ (AA) obtained through chromosome doubling. Euphytica. 2015;202:435–443. doi: 10.1007/s10681-014-1320-0. DOI

Robertson W.R.B. Chromosome studies. I. Taxonomic relationships shown in the chromosomes of Tettigidae and Acrididae: V-shaped chromosomes and their significance in Acrididae, Locustidae, and Gryllidae: Chromosomes and variation. J. Morphol. 1916;27:179–331. doi: 10.1002/jmor.1050270202. DOI

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

Jiang J. Fluorescence in situ hybridization in plants: Recent developments and future applications. Chromosome Res. 2019;27:153–165. doi: 10.1007/s10577-019-09607-z. PubMed DOI

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

Idziak D., Hazuka I., Poliwczak B., Wiszynska A., Wolny E., Hasterok R. Insight into the karyotype evolution of Brachypodium species using comparative chromosome barcoding. PLoS ONE. 2014;9:e93503. doi: 10.1371/journal.pone.0093503. PubMed DOI PMC

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

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

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

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

Machado M.A., Pieczarka J.C., Silva F.H.R., O’Brien P.C.M., Ferguson-Smith M.A., Nagamachi C.Y. Extensive karyotype reorganization in the fish Gymnotus arapaima (Gymnotiformes, Gymnotidae) highlighted by zoo-FISH analysis. Front. Genet. 2018;9:8. doi: 10.3389/fgene.2018.00008. PubMed DOI PMC

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

Bi Y., Zhao Q., Yan W., Li M., Liu Y., Cheng C., Zhang L., Yu X., Li J., Qian C., et al. Flexible chromosome painting based on multiplex PCR of oligonucleotides and its application for comparative chromosome analyses in Cucumis. Plant. J. 2020;102:178–186. doi: 10.1111/tpj.14600. PubMed DOI

Shepherd K. Cytogenetics of the Genus Musa. International Network for the Improvement of Banana and Plantain; Montpellier, France: 1999.

Fauré S., Noyer J.L., Horry J.P., Bakry F., Lanaud C., de León D.G. A molecular marker-based linkage map of diploid bananas (Musa acuminata) Theor. Appl. Genet. 1993;87:517–526. doi: 10.1007/BF00215098. PubMed DOI

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

Mbanjo E.G.N., Tchoumbougnang F., Mouelle A.S., Oben J.E., Nyine M., Dochez C., Ferguson M.E., Lorenzen J. Molecular marker-based genetic linkage map of a diploid banana population (Musa acuminata Colla) Euphytica. 2012;188:369–386. doi: 10.1007/s10681-012-0693-1. DOI

Noumbissié G.B., Chabannes M., Bakry F., Ricci S., Cardi C., Njembele J.C., Yohoume D., Tomekpe K., Iskra-Caruana M.L., D’Hont A., et al. Chromosome segregation in an allotetraploid banana hybrid (AAAB) suggests a translocation between the A and B genomes and results in eBSV-free offsprings. Mol. Breed. 2016;36:38–52. doi: 10.1007/s11032-016-0459-x. DOI

Carreel F., Gonzalez de Leon D., Lagoda P., Lanaud C., Jenny C., Horry J., Tezenas du Montcel H. Ascertaining maternal and paternal lineage within Musa by chloroplast and mitochondrial DNA RFLP analyses. Genome. 2002;45:679–692. doi: 10.1139/g02-033. PubMed DOI

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

Dupouy M., Baurens F.C., Derouault P., Hervouet C., Cardi C., Cruaud C., Istace B., Labadie K., Guiougou C., Toubi L., et al. Two large reciprocal translocations characterized in the disease resistance-rich burmannica genetic group of Musa acuminata. Ann. Bot. 2019;124:31–329. doi: 10.1093/aob/mcz078. PubMed DOI PMC

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

Horry J.P. Chimiotaxonomie et organisation génétique dans le genre Musa (III) Fruits. 1989;44:573–578.

Lebot V., Aradhya M.K., Manshardt R.M., Meilleur B.A. Genetic relationships among cultivated bananas and plantains from Asia and the Pacific. Euphytica. 1993;67:163–175. doi: 10.1007/BF00040618. DOI

Hippolyte I., Jenny C., Gardes L., Bakry F., Rivallan R., Pomies V., Cubry P., Tomekpe K., Risterucci A.M., Roux N., et al. Foundation characteristics of edible Musa triploids revealed from allelic distribution of SSR markers. Ann. Bot. 2012;109:937–951. doi: 10.1093/aob/mcs010. PubMed DOI PMC

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

Sandoval J.A., Côte F.X., Escoute J. Chromosome number variations in micropropagated true-to-type and off-type banana plants (Musa AAA Grande Naine cv.) In Vitro Cell. Dev. Biol. Plant. 1996;32:14–17. doi: 10.1007/BF02823007. DOI

Shepherd K., Da Silva K.M. Mitotic instability in banana varieties. Aberrations in conventional triploid plants. Fruits. 1996;51:99–103.

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

Čížková J., Hřibová E., Christelová P., van den Houwe I., Häkkinen M., Roux N., Swennen R., Doležel J. Molecular and cytogenetic characterization of wild Musa species. PLoS ONE. 2015;10:e0134096. doi: 10.1371/journal.pone.0134096. PubMed DOI PMC

Roux N., Toloza A., Radecki Z., Zapata-Arias F.J., Doležel J. Rapid detection of aneuploidy in Musa using flow cytometry. Plant. Cell Rep. 2003;21:483–490. doi: 10.1007/s00299-002-0512-6. PubMed DOI

Sedlazeck F.J., Rescheneder P., Smolka M., Fang H., Nattestad M., von Haeseler A., Schatz M.C. Accurate detection of complex structural variations using single-molecule sequencing. Nat. Methods. 2018;15:461–468. doi: 10.1038/s41592-018-0001-7. PubMed DOI PMC

Hu L., Liang F., Cheng D., Zhang Z., Yu G., Zha J., Wang Y., Xia Q., Yuan D., Tan Y., et al. Location of balanced chromosome-translocation breakpoints by long-read sequencing on the Oxford Nanopore platform. Front. Genet. 2020;10:1330. doi: 10.3389/fgene.2019.01313. PubMed DOI PMC

Soto D.C., Shew C., Mastoras M., Schmidt J.M., Sahasrabudhe R., Kaya G., Andrés A.M., Dennis M.Y. Identification of structural variations in chimpanzees using optical mapping and nanopore sequencing. Genes. 2020;11:276. doi: 10.3390/genes11030276. PubMed DOI PMC

Perrier X., Jacquemoud-Collet J.P. DARwin Software. [(accessed on 20 May 2020)];2006 Available online: http://darwin.cirad.fr/

FigTree v1.4.0. [(accessed on 20 May 2020)]; Available online: http://tree.bio.ed.ac.uk/software/figtree/

D’Hont A., Denoeud F., Aury J.M., Baurens F.C., Carreel F., Garsmeur O., Noel B., Bocs S., Droc G., Rouard M., et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature. 2012;488:213–217. doi: 10.1038/nature11241. PubMed DOI

Doležel J., Doleželová M., Roux N., van den Houwe I. A novel method to prepare slides for high resolution chromosome studies in Musa spp. Infomusa. 1998;7:3–4.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...