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Marker-assisted breeding of Musa balbisiana genitors devoid of infectious endogenous Banana streak virus sequences

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Abstract

Breeding new interspecific banana hybrid varieties relies on the use of Musa acuminata and M. balbisiana parents. Unfortunately, infectious alleles of endogenous Banana streak virus (eBSV) sequences are present in the genome of Musa balbisiana genitors. Upon activation by biotic and abiotic stresses, these infectious eBSVs lead to spontaneous infections by several species of Banana streak virus in interspecific hybrids harboring both Musa acuminata and M. balbisiana genomes. Here we provide evidence that seedy M. balbisiana diploids display diverse eBSV allelic combinations and that some eBSVs differ structurally from those previously reported. We also show that segregation of infectious and non-infectious eBSV alleles can be achieved in seedy M. balbisiana diploids through self-pollination or chromosome doubling of haploid lines. We report on the successful breeding of M. balbisiana diploid genitors devoid of all infectious eBSV alleles following self-pollination and on the potential of breeding additional M. balbisiana diploid genitors free of infectious eBSVs by crossing parents displaying complementary eBSV patterns. Our work paves the way to the safe use of M. balbisiana genitors for breeding banana interspecific hybrid varieties with no risk of activation of infectious eBSVs.

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Abbreviations

A:

Musa acuminata genome

B:

Musa balbisiana genome

BSD:

Black sigatoka disease

BSV:

Banana streak virus

BSGFV:

Banana streak GF virus

BSIMV:

Banana streak IM virus

BSOLV:

Banana streak OL virus

CIRAD:

Centre International de Coopération en Recherche Agronomique pour le Développement

CRB-PT:

Biological Resources Center of Tropical Plants

eBSV:

Endogenous Banana streak virus

EVE:

Endogenous viral element

FAO:

Food and Agriculture Organization of the United Nations

ITC:

International Transit Center

PKW:

‘Pisang Klutuk Wulung’

References

  • Bakry F (2008) Zygotic embryo rescue. Fruits 63:111–115

    Article  Google Scholar 

  • Bakry F, Assani A, Kerbellec F (2008) Haploid induction: androgenesis in Musa balbisiana. Fruits 63:45–49

    Article  CAS  Google Scholar 

  • Bakry F, Carreel F, Jenny C, Horry JP (2009) Genetic improvement of banana. Breeding plantation tree crops: tropical species. Springer, New York

    Google Scholar 

  • Chabannes M, Iskra-Caruana ML (2013) Endogenous pararetroviruses: a reservoir of virus infection in plants. Curr Opin Virol 3:615–620

    Article  CAS  PubMed  Google Scholar 

  • Chabannes M, Baurens FC, Duroy P-O, Bocs S, Vernerey M, Rodier-Goud M, Barbe V, Gayral P, Iskra-Caruana ML (2013) Three infectious viral species lying in wait in the banana genome. J Virol 87:8624–8637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1093/aobpla/plr024

    PubMed  PubMed Central  Google Scholar 

  • Churchill AC (2011) Mycosphaerella fijiensis, the black leaf streak pathogen of banana: progress towards understanding pathogen biology and detection, disease development, and the challenges of control. Mol Plant Pathol 12:307–328

    Article  CAS  PubMed  Google Scholar 

  • Côte FX, Galzi S, Follioti M, Lamagnère Y, Teycheney PY, Iskra-Caruana ML (2010) Micropropagation by tissue culture triggers differential expression of infectious endogenous Banana streak virus sequences (eBSV) present in the B genome of natural and synthetic interspecific banana plantains. Mol Plant Pathol 11:137–144

    Article  PubMed  Google Scholar 

  • D’Hont A, Denoeud F, Aury JM, Baurens FC, 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, Lengellé J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, Mckain MR, Leebens-Mack J, Burgess D, Freeling M, Mbéguié-A-Mbéguié 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 AM, Weissenbach J, Ruiz M, Glaszmann JC, Quétier F, Yahiaoui N, Wincker P (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217

    Article  PubMed  Google Scholar 

  • Dallot S, Acuña P, Rivera C, Ramírez P, Côte F, Lockhart BEL, Caruana ML (2001) Evidence that the proliferation stage of micropropagation procedure is determinant in the expression of Banana streak virus integrated into the genome of the FHIA 21 hybrid (Musa AAAB). Arch Virol 146:2179–2190

    Article  CAS  PubMed  Google Scholar 

  • Davey MW, Gudimella R, Harikrishna JA, Sin LW, Khalid N, Keulemans J (2013) A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genom 14:683

    Article  CAS  Google Scholar 

  • Duroy PO, Perrier X, Laboureau N, Jacquemoud-Collet JP, Iskra-Caruana ML (2016) How endogenous plant pararetroviruses shed light on Musa evolution. Ann Bot. doi:10.1093/aob/mcw011

    PubMed  Google Scholar 

  • Food and Agriculture Organization (2014) FAOSTAT database. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Gambley CF, Geering ADW, Steele V, Thomas JE (2008) Identification of viral and non-viral reverse transcribing elements in pineapple (Ananas comosus), including members of two new badnavirus species. Arch Virol 153:1599–1604

    Article  CAS  PubMed  Google Scholar 

  • 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 82:6697–6710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 84:7346–7359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geering ADW, McMichael LA, Dietzgen RG, Thomas JE (2000) Genetic diversity among Banana streak virus isolates from Australia. Phytopathology 90:921–927

    Article  CAS  PubMed  Google Scholar 

  • Geering ADW, Olszewski NE, Dahal G, Thomas JE, Lockhart BEL (2001) Analysis of the distribution and structure of integrated Banana streak virus DNA in a range of Musa cultivars. Mol Plant Pathol 2:207–213

    Article  CAS  PubMed  Google Scholar 

  • Geering AD, Parry JN, Thomas JE (2011) Complete genome sequence of a novel badnavirus, banana streak IM virus. Arch Virol 156:733–737

    Article  CAS  PubMed  Google Scholar 

  • Geering ADW, Maumus M, Copetti D, Choisne N, Zwickl DJ, Zytnicki M, McTaggart AR, Scalabrin S, Vezzulli S, Quesneville H, Teycheney PY (2014) Endogenous florendoviral elements are major components of plant genomes and hallmarks of virus evolution. Nat Commun 5:5269. doi:10.1038/ncomms6269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grapin A, Noyer JL, Carreel F, Dambier D, Baurens FC, Lanaud C, Lagoda PJL (1998) Diploid Musa acuminata genetic diversity assayed with sequence-tagged microsatellite sites. Electrophoresis 19:1374–1380

    Article  CAS  PubMed  Google Scholar 

  • Harper G, Osuji JO, Heslop-Harrison J, Hull R (1999) Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255:207–213

    Article  CAS  PubMed  Google Scholar 

  • 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 FC, 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 10:65

    Article  PubMed  PubMed Central  Google Scholar 

  • Hippolyte I, Jenny C, Gardes L, Bakry F, Rivallan R, Pomies V, Cubry P, Tomekpe K, Risterucci AM, Roux N, Rouard M, Arnaud E, Kolesnikova-Allen M, Perrier X (2012) Foundation characteristics of edible Musa triploids revealed from allelic distribution of SSR markers. Ann Bot 109:937–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iskra-Caruana ML, Baurens FC, Gayral P, Chabannes M (2010) A four-partner plant-virus interaction: enemies can also come from within. Mol Plant Microbe Interact 23:1394–1402

    Article  CAS  PubMed  Google Scholar 

  • Jain SM, Priyadarshan PM, Bakry F, Carreel F, Jenny C, Horry JP (2009) Genetic improvement of banana. Breeding plantation tree crops: tropical species. Springer, New York

    Book  Google Scholar 

  • Lagoda PJL, Noyer JL, Dambier D, Baurens F-C, Grapin A, Lanaud C (1998) Sequence tagged microsatellite site (STMS) markers in the Musaceae. Mol Ecol 7:659–663

    CAS  PubMed  Google Scholar 

  • Lapeyre De, de Bellaire L, Foure E, Abadie C, Carlier J (2010) Black leaf streak disease is challenging the banana industry. Fruits 65:327–342

    Article  Google Scholar 

  • Le Provost G, Iskra-Caruana ML, Acina I, Teycheney PY (2006) Improved detection of episomal Banana streak viruses by multiplex immunocapture PCR. J Virol Methods 137:7–13

    Article  PubMed  Google Scholar 

  • Lockhart BE, Menke J, Dahal G, Olszewski NE (2000) Characterization and genomic analysis of tobacco vein clearing virus, a plant pararetrovirus that is transmitted vertically and related to sequences integrated in the host genome. J Gen Virol 81:1579–1585

    Article  CAS  PubMed  Google Scholar 

  • Meyer JB, Kasdorf GGF, Nel LH, Pietersen G (2008) Transmission of activated-episomal Banana streak OL badnavirus (BSOLV) to cv. Williams banana (Musa sp.) by three mealybug species. Plant Dis 92:1158–1163

    Article  CAS  Google Scholar 

  • Ndowora T, Dahal G, LaFleur D, Harper G, Hull R, Olszewski N, Lockhart B (1999) Evidence that badnavirus infection in Musa can originate from integrated sequences. Virology 255:214–220

    Article  CAS  PubMed  Google Scholar 

  • Noumbissié GB, Chabannes M, Bakry F, Ricci S, Cardi C, Njembele JC, Yohoume D, Tomekpe K, Iskra Caruana ML, d’Hont A, Baurens FC (2016) 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 36:38

    Article  Google Scholar 

  • Ortiz R, Swennen R (2014) From crossbreeding to biotechnology-facilitated improvement of banana and plantain. Biotechnol Adv 32:158–169

    Article  CAS  PubMed  Google Scholar 

  • Perrier X, De Langhe E, Donohue M, Lentfer C, Vrydaghs L, Bakry F, Carreel F, Hippolyte I, Horry J-P, Jenny C, Lebot V, Risterucci AM, Tomekpe K, Doutrelepont H, Ball T, Manwaring J, De Maret P, Denham T (2011) Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc Natl Acad Sci USA 108:11311–11318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ploetz RC (2006) Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense. Phytopathology 96:653–656

    Article  PubMed  Google Scholar 

  • Ravi I, Uma S, Vaganan MM, Mustaffa MM (2013) Phenotyping bananas for drought resistance. Front Physiol 4:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Richert-Pöggeler KR, Noreen F, Schwarzacher T, Harper G, Hohn T (2003) Induction of infectious petunia vein clearing (pararetro) virus from endogenous provirus in petunia. EMBO J 22:4836–4845

    Article  PubMed  PubMed Central  Google Scholar 

  • Risterucci AM, Grivet L, N’Goran JKA, Pieretti I, Flament MH, Lanaud C (2000) A high-density linkage map of Theobroma cacao L. Theor Appl Genet 101:948–955

    Article  CAS  Google Scholar 

  • Robinson JC (1996) Bananas and plantain. CABI International, Wallingford

    Google Scholar 

  • Teycheney PY, Geering ADW (2011) Endogenous viral sequences in plant genomes. In: Caranta C, Aranda MA, Tepfer M, Lopez-Moya JJ (eds) Recent advances in plant virology. Caister Academic Press, Norfolk, pp 343–362

    Google Scholar 

Download references

Acknowledgments

The authors wish to thank Frédéric Bakry and Léonidas Féréol for providing some doubled haploid lines and Guillaume Fort for technical help. This work was supported by the European Regional Development Fund. This paper is dedicated to the memory of Jacky Ganry.

Author information

Author notes

  1. Marie Umber

    Present address: INRA UR ASTRO, Domaine Duclos, 97170, Petit-Bourg, France

  2. Jean-Philippe Pichaut

    Present address: Vilmorin SA, Route du Manoir, 49250, La Ménitré, France

  3. Pierre-Olivier Duroy

    Present address: Institut de Biotechnologie UNIL, EPFL-LBTM, CH A1-398, Station 6, 1015, Lausanne, Switzerland

Authors and Affiliations

  1. CIRAD UMR AGAP, 97130, Capesterre-Belle Eau, Guadeloupe, France

    Marie Umber, Jean-Philippe Pichaut, Benoît Farinas, Bérenger Janzac, Kaïssa Plaisir-Pineau, Gersende Pressat, Chantal Guiougou, Jean-Marie Delos, Frédéric Salmon & Pierre-Yves Teycheney

  2. CIRAD UMR BGPI, 34398, Montpellier, France

    Nathalie Laboureau, Matthieu Chabannes, Pierre-Olivier Duroy & Marie-Line Iskra-Caruana

  3. CIRAD UMR AGAP, 34098, Montpellier, France

    Franc-Christophe Baurens & Christophe Jenny

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  1. Marie Umber
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Correspondence to Pierre-Yves Teycheney.

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All experiments and data analysis were performed according to ethical standards.

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Umber, M., Pichaut, JP., Farinas, B. et al. Marker-assisted breeding of Musa balbisiana genitors devoid of infectious endogenous Banana streak virus sequences. Mol Breeding 36, 74 (2016). https://doi.org/10.1007/s11032-016-0493-8

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