Abstract
Many banana cultivars (including the Plantain type) are triploid interspecific hybrids between Musa acuminata (A genome) and Musa balbisiana (B genome). M. balbisiana contains endogeneous Banana streak virus sequences (eBSVs) that can, in interspecific genome context, spontaneously release infectious viral genomes. We analyzed, a triploid progeny of 184 individuals from a cross between a tetraploid AAAB breeding accession (CRBP39) and the diploid AA accession (Pahang) with 38 SSR and eBSV-specific PCR markers. The results showed that (1) most of the alleles are found/transmitted in the expected frequency to the progeny with only 10 % biased; (2) 70 % of the loci displayed a tetrasomic allele segregation and (3) interspecific intrachromosomal recombinations occurred for all the chromosome segments surveyed. However, half of the offspring obtained resulted from maternal unbalanced gametes transmission. Analysis of gamete composition and marker association suggested the presence of a large translocation between A and B genome involving chromosome 1 and 3. The two infectious eBSVs present in the maternal parent CRBP39 are located on chromosome 1B and appeared in a higher proportion than expected in the progeny. Interestingly, we showed that both eBSVs were absent from 24 offspring that represent promising material for breeding.
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References
Bakry F (2008) Zygotic embryo rescue in bananas. Fruits 63(2):111–115
Bakry F, Carreel F, Jenny C, Horry J-P (2009) Genetic improvement of banana. Breeding plantation tree crops: tropical species. Springer, New York, pp 3–50
Baurens F-C, Bocs S, Rouard M, Matsumoto T, Miller RN, Rodier-Goud M, Mbéguié-A-Mbéguié D, Yahiaoui N (2010) Mechanisms of haplotype divergence at the RGA08 nucleotide-binding leucine-rich repeat gene locus in wild banana (Musa balbisiana). BMC Plant Biol 10:149
Bradshaw JE, Hackett CA, Pande B, Waugh R, Bryan GJ (2008) QTL mapping of yield, agronomic and quality traits in tetraploid potato (Solanum tuberosum subsp. tuberosum). Theor Appl Genet 116(2):193–211
Chabannes M, Baurens F-C, Duroy P-O, Bocs S, Vernerey M-S, Rodier-Goud M, Barbe V, Gayral P, Iskra-Caruana M-L (2013) Three infectious viral species lying in wait in the banana genome. J Virol 87(15):8624–8637
Cheesman E (1947) Classification of the bananas: The Genus Musa L. Kew Bull 106–117
Christelova P, Valarik M, Hribova E, Van den houwe I, Channeliere S, Roux N, Dolezel J (2011) A platform for efficient genotyping in Musa using microsatellite markers. AoB Plants. plr024. doi:10.1093/aobpla/plr024
Crismani W, Girard C, Mercier R (2013) Tinkering with meiosis. J Exp Bot 64(1):55–65
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(2):177–183
D’Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengelle J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, McKain MR, Leebens-Mack J, Burgess D, Freeling M, Mbeguie-A-Mbeguie D, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A, Jeridi M, Dolezel J, Roux N, Risterucci A-M, Weissenbach J, Ruiz M, Glaszmann J-C, Quetier F, Yahiaoui N, Wincker P (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410):213–217
De Langhe E, Hribova E, Carpentier S, Dolezel J, Swennen R (2010) Did backcrossing contribute to the origin of hybrid edible bananas? Ann Bot 106(6):849–857
Dodds KS, Simmonds NW (1948) Sterility and parthenocarpy in diploid hybrids of Musa. Heredity 2(1):101–117
Dolezel J, Bartos J (2005) Plant DNA Flow Cytometry and Estimation of Nuclear Genome Size. Ann Bot 95(1):99–110
Dolezel J, Binarova P, Lcretti S (1989) Analysis of nuclear DNA content in plant cells by Flow cytometry. Biol Plant 31(2):113–120
Duroy P-O (2012) Quels sont les enjeux au cours de l’évolution du bananier (Musa sp.) qui ont conduit au maintien de séquences virales de Banana Streak Virus dans son génome? Ph.D. thesis dissertation, University of Montpellier 2
Faure S, Noyer JL, Horry JP, Bakry F, Lanaud C, Deleon DG (1993) A molecular marker-based linkage map of diploid bananas (Musa acuminata). Theor Appl Genet 87(4):517–526
Gawel NJ, Jarret RL (1991) Chloroplast DNA restriction-fragment-length-polymorphisms (RFLPs) in Musa species. Theor Appl Genet 81(6):783–786
Gayral P, Iskra-Caruana M-L (2009) Phylogeny of banana streak virus reveals recent and repetitive endogenization in the genome of its banana host (Musa sp.). J Mol Evol 69(1):65–80
Gayral P, Blondin L, Guidolin O, Carreel F, Hippolyte I, Perrier X, Iskra-Caruana ML (2010) Evolution of endogenous sequences of banana streak virus: What can we learn from banana (Musa sp.) Evolution? J Virol 84(14):7346–7359
Gayral P, Noa-Carrazana JC, Lescot M, Lheureux F, Lockhart BEL, Matsumoto T, Piffanelli P, Iskra-Caruana ML (2008) A single Banana streak virus integration event in the banana genome as the origin of infectious endogenous pararetrovirus. J Virol 82(13):6697–710
Hippolyte I, Bakry F, Seguin M, Gardes L, Rivallan R, Risterucci AM, Jenny C, Perrier X, Carreel F, Argout X, Piffanelli P, Khan IA, Miller RNG, Pappas GJ, Mbeguie-A-Mbeguie D, Matsumoto T, De Bernardinis V, Huttner E, Kilian A, Baurens F-C, D’Hont A, Cote F, Courtois B, Glaszmann JC (2010) A saturated SSR/DArT linkage map of Musa acuminata addressing genome rearrangements among bananas. BMC Plant Biol 10(1):1–18
Iskra-Caruana ML, Baurens F-C, Gayral P, Chabannes M (2010) A four-partner plant-virus interaction: enemies can also come from within. Mol Plant Microbe Interact 23(11):1394–1402
Jain SM, Priyadarshan PM, Bakry F, Carreel F, Jenny C, Horry J-P (2009) Genetic improvement of Banana. Breeding plantation tree crops: tropical species. Springer, New York, pp 3–50
Jannoo N, Grivet L, David J, D’Hont A, Glaszmann JC (2004) Differential chromosome pairing affinities at meiosis in polyploid sugarcane revealed by molecular markers. Heredity 93(5):460–467
Jeridi M, Bakry F, Escoute J, Fondi E, Carreel F, Ferchichi A, D’Hont A, Rodier-Goud M (2011) Homoeologous chromosome pairing between the A and B genomes of Musa spp. revealed by genomic in situ hybridization. Ann Bot 108(5):975–981
Jeridi M, Perrier X, Rodier-Goud M, Ferchichi A, D’Hont A, Bakry F (2012) Cytogenetic evidence of mixed disomic and polysomic inheritance in an allotetraploid (AABB) Musa genotype. Ann Bot 110(8):1593–1606
Koning-Boucoiran CFS, Gitonga VW, Yan Z, Dolstra O, van der Linden CG, van der Schoot J, Uenk GE, Verlinden K, Smulders MJM, Krens FA, Maliepaard C (2012) The mode of inheritance in tetraploid cut roses. Theor Appl Genet 125(3):591–607
Li J, Das K, Fu G, Li Y, Tobias C, Wu R (2012) Statistical model for genetic mapping in polyploids: challenges and opportunities. In: Rifkin SA (ed) Quantitative trait loci (QTL) methods and protocols, vol 871. Springer, New York, pp 245–261
Lagoda P, Noyer J, Dambier D, Baurens F, Grapin A, Lanaud C (1998) Sequence tagged microsatellite site (STMS) markers in the Musaceae. Mol Ecol 7(5):659–663
Mbanjo E, Tchoumbougnang FO, Mouelle A, Oben J, Nyine M, Dochez C, Ferguson M, Lorenzen J (2012) Molecular marker-based genetic linkage map of a diploid banana population (Musa acuminata Colla). Euphytica 188(3):369–386
Noyer J, Dambier D, Lanaud C, Lagoda P (1997) The saturated map of diploid banana (Musa acuminata). Abstract Plant and Animal Genome V Conference
Perrier X (2009) Combining biological approaches to shed light on the evolution of edible bananas. Ethnobot Res Appl 7:199–216
Pillay M, Tenkouano A, Hartman J (2002) Future challenges in Musa breeding. Crop improvement: challenges in the twenty-first century. Food Products Press Inc, New York
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639
Safar J, Noa-Carrazana JC, Vrana J, Bartos J, Alkhimova O, Sabau X, Simkova H, Lheureux F, Caruana ML, Dolezel J, Piffanelli P (2004) Creation of a BAC resource to study the structure and evolution of the banana (Musa balbisiana) genome. Genome 47(6):1182–1191
Shepherd K (eds) (1999). Cytogenetics of the genus Musa (no SB123. 3 S54). IPGRI
Simmonds NW, Shepherd K (1955) The taxonomy and origins of the cultivated bananas. J Linn Soc Lond Bot 55(359):302–312
Soltis DE, Soltis PS (1993) Molecular-data and the dynamics nature of polyploidy. Crit Rev Plant Sci 12(3):243–273
Stift M, Berenos C, Kuperus P, van Tienderen PH (2008) Segregation models for disomic, tetrasomic and intermediate inheritance in tetraploids: a general procedure applied to rorippa (yellow cress) microsatellite data. Genetics 179(4):2113–2123
Thomas DS, Turner DW, Eamus D (1998) Independent effects of the environment on the leaf gas exchange of three banana (Musa sp.) cultivars of different genomic constitution. Sci Hortic 75(1):41–57
Tomekpe K, Jenny C, Escalant JV (2004) Revue des stratégies d’amélioration conventionnelle de Musa. InfoMusa 13(2):2–5
Vanhove AC, Vermaelen W, Panis B, Swennen R, Carpentier SC (2012) Screening the banana biodiversity for drought tolerance: can an in vitro growth model and proteomics be used as a tool to discover tolerant varieties and understand homeostasis. Front Plant Sci 3(176):10–3389
Acknowledgments
Guy Noumbissié Ph.D. was financed by Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD). The SSR genotyping was performed on the Montpellier-Languedoc Roussillon Grand Plateau Technique Regional.
Author contribution
AD, FCB, MLC, MC, and FB jointly designed the study. GBN, FCB, CC, and AD designed, generated and analyzed SSR genotyping data. GBN, MC, and MLC designed experiment with eBSV markers and analyzed data. SR, FB, JCN, DY, and KT designed and performed the genetic cross and handled the progeny. AD and FCB: wrote the manuscript. MC and MLC edited the manuscript. All authors discussed the results and implications and commented on the manuscript.
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F.-C. Baurens, A. D'Hont have contributed equally to the work.
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11032_2016_459_MOESM2_ESM.pdf
Supplementary Figure 1: Localization of the 38 SSR loci on the Pahang Musa reference sequence. Chromosomes characteristics are those described in D’Hont et al, 2012. (PDF 532 kb)
11032_2016_459_MOESM3_ESM.pdf
Supplementary Figure 2: Three-way Venn diagram showing the distribution of offspring with unbalanced gamete transmission for the 3 fully informative SSR loci belonging to homo(eo)logous chromosome group 1. A: 3 alleles transmission; B: one allele transmission. Number of plants is indicated in the intersections, the total number of offspring revealed by each loci followed the marker name. (PDF 284 kb)
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Noumbissié, G.B., Chabannes, M., Bakry, F. 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 Breeding 36, 38 (2016). https://doi.org/10.1007/s11032-016-0459-x
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DOI: https://doi.org/10.1007/s11032-016-0459-x