Molecular Breeding

, 36:74 | Cite as

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

  • Marie Umber
  • Jean-Philippe Pichaut
  • Benoît Farinas
  • Nathalie Laboureau
  • Bérenger Janzac
  • Kaïssa Plaisir-Pineau
  • Gersende Pressat
  • Franc-Christophe Baurens
  • Matthieu Chabannes
  • Pierre-Olivier Duroy
  • Chantal Guiougou
  • Jean-Marie Delos
  • Christophe Jenny
  • Marie-Line Iskra-Caruana
  • Frédéric Salmon
  • Pierre-Yves Teycheney
Article

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.

Keywords

Musa Endogenous viral element Banana streak virus Infectious alleles Marker-assisted breeding 

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’

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical standards

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

Supplementary material

11032_2016_493_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 17 kb)
11032_2016_493_MOESM2_ESM.xlsx (19 kb)
Supplementary material 2 (XLSX 18 kb)

References

  1. Bakry F (2008) Zygotic embryo rescue. Fruits 63:111–115CrossRefGoogle Scholar
  2. Bakry F, Assani A, Kerbellec F (2008) Haploid induction: androgenesis in Musa balbisiana. Fruits 63:45–49CrossRefGoogle Scholar
  3. Bakry F, Carreel F, Jenny C, Horry JP (2009) Genetic improvement of banana. Breeding plantation tree crops: tropical species. Springer, New YorkGoogle Scholar
  4. Chabannes M, Iskra-Caruana ML (2013) Endogenous pararetroviruses: a reservoir of virus infection in plants. Curr Opin Virol 3:615–620CrossRefPubMedGoogle Scholar
  5. 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 87:8624–8637CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 PubMedPubMedCentralGoogle Scholar
  7. 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 12:307–328CrossRefPubMedGoogle Scholar
  8. 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 11:137–144CrossRefPubMedGoogle Scholar
  9. 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 488:213–217CrossRefPubMedGoogle Scholar
  10. 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 146:2179–2190CrossRefPubMedGoogle Scholar
  11. 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 14:683CrossRefGoogle Scholar
  12. 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 PubMedGoogle Scholar
  13. Food and Agriculture Organization (2014) FAOSTAT database. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  14. 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 153:1599–1604CrossRefPubMedGoogle Scholar
  15. 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 82:6697–6710CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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 84:7346–7359CrossRefPubMedPubMedCentralGoogle Scholar
  17. Geering ADW, McMichael LA, Dietzgen RG, Thomas JE (2000) Genetic diversity among Banana streak virus isolates from Australia. Phytopathology 90:921–927CrossRefPubMedGoogle Scholar
  18. 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 2:207–213CrossRefPubMedGoogle Scholar
  19. Geering AD, Parry JN, Thomas JE (2011) Complete genome sequence of a novel badnavirus, banana streak IM virus. Arch Virol 156:733–737CrossRefPubMedGoogle Scholar
  20. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 19:1374–1380CrossRefPubMedGoogle Scholar
  22. Harper G, Osuji JO, Heslop-Harrison J, Hull R (1999) Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255:207–213CrossRefPubMedGoogle Scholar
  23. 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 10:65CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 109:937–951CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 23:1394–1402CrossRefPubMedGoogle Scholar
  26. 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 YorkCrossRefGoogle Scholar
  27. 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 7:659–663PubMedGoogle Scholar
  28. Lapeyre De, de Bellaire L, Foure E, Abadie C, Carlier J (2010) Black leaf streak disease is challenging the banana industry. Fruits 65:327–342CrossRefGoogle Scholar
  29. 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 137:7–13CrossRefPubMedGoogle Scholar
  30. 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 81:1579–1585CrossRefPubMedGoogle Scholar
  31. 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 92:1158–1163CrossRefGoogle Scholar
  32. 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 255:214–220CrossRefPubMedGoogle Scholar
  33. 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 36:38CrossRefGoogle Scholar
  34. Ortiz R, Swennen R (2014) From crossbreeding to biotechnology-facilitated improvement of banana and plantain. Biotechnol Adv 32:158–169CrossRefPubMedGoogle Scholar
  35. 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 108:11311–11318CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ploetz RC (2006) Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense. Phytopathology 96:653–656CrossRefPubMedGoogle Scholar
  37. Ravi I, Uma S, Vaganan MM, Mustaffa MM (2013) Phenotyping bananas for drought resistance. Front Physiol 4:9CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 22:4836–4845CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 101:948–955CrossRefGoogle Scholar
  40. Robinson JC (1996) Bananas and plantain. CABI International, WallingfordGoogle Scholar
  41. 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 343–362Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Marie Umber
    • 1
    • 2
  • Jean-Philippe Pichaut
    • 1
    • 3
  • Benoît Farinas
    • 1
  • Nathalie Laboureau
    • 4
  • Bérenger Janzac
    • 1
  • Kaïssa Plaisir-Pineau
    • 1
  • Gersende Pressat
    • 1
  • Franc-Christophe Baurens
    • 6
  • Matthieu Chabannes
    • 4
  • Pierre-Olivier Duroy
    • 4
    • 5
  • Chantal Guiougou
    • 1
  • Jean-Marie Delos
    • 1
  • Christophe Jenny
    • 6
  • Marie-Line Iskra-Caruana
    • 4
  • Frédéric Salmon
    • 1
  • Pierre-Yves Teycheney
    • 1
  1. 1.CIRAD UMR AGAPCapesterre-Belle EauFrance
  2. 2.INRA UR ASTROPetit-BourgFrance
  3. 3.Vilmorin SALa MénitréFrance
  4. 4.CIRAD UMR BGPIMontpellierFrance
  5. 5.Institut de Biotechnologie UNIL, EPFL-LBTMLausanneSwitzerland
  6. 6.CIRAD UMR AGAPMontpellierFrance

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