Skip to main content

Advertisement

Log in

Analogues of virus resistance genes map to QTLs for resistance to sharka disease in Prunus davidiana

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Plum pox virus (PPV), the causative agent of sharka disease in Prunoideae, is one of the most serious problems affecting stone fruit production in Europe and America. Resistance to PPV was previously described in a Prunus davidiana clone, P1908, and introduced into peach (Prunus persica) genotypes. Genetic resistance to PPV displays a complex pattern of quantitative inheritance. An analysis of quantitative trait loci (QTLs) for resistance was performed on an F1 interspecific peach population obtained from a cross between the susceptible nectarine cultivar Summergrand and P. davidiana. The hybrids were graft-inoculated with PPV in duplicate following a classical procedure. The incidence of infection was evaluated four times, over two vegetative cycles, by symptom observation and enzyme-linked immunoadsorbent assays (ELISA). Restriction of systemic downward movement of the PPV virus was also evaluated by testing the susceptible rootstocks. Using both analysis of variance and non-parametric tests, six genomic regions involved in PPV resistance were detected. Depending on the scoring data considered, between 22 and 51% of the phenotypic variance could be explained by the quantitative model. One QTL, located in the distal region of linkage group 1, maps in a genomic region that is syntenic to the location of a resistance gene previously identified in the apricot cv. Goldrich. Some QTLs appeared to be temporally specific, reflecting the environmental dependence of PPV-resistance scoring. Candidate gene fragments were amplified by PCR, isolated and mapped on the peach interspecific linkage map. We report here the co-localization of three analogues of virus resistance genes with two distinct genomic regions linked to PPV resistance in P. davidiana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Albar L, Lorieux M, Ahmadi N, Rimbault I, Pinel A, Sy AA, Fargette D, Ghesquière A (1998) Genetic basis and mapping of the resistance to rice yellow mottle virus I QTLs identification and relationship between resistance and plant morphology. Theor Appl Genet 97:1145–1154

    Article  Google Scholar 

  • Asins MJ, Bernet GP, Ruiz C, Cambra M, Guerri J, Carbonell EA (2004) QTL analysis of citrus tristeza virus-citradia interaction. Theor Appl Genet 108:603–611

    Article  Google Scholar 

  • Basten CJ, Weir BS, Zeng ZB (2002) QTL cartographer: a reference manual and tutorial for QTL mapping. North Carolina State University, Raleigh

    Google Scholar 

  • Bendahmane A, Kanyuka KV, Baulcombe DC (1997) High resolution and physical mapping of the Rx gene for extreme resistance to potato virus X in tetraploid potato. Theor Appl Genet 95:153–162

    Article  Google Scholar 

  • Bendahmane A, Kanyuka KV, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–791

    Article  Google Scholar 

  • Bernhard R, Marénaud C, Sutic D (1969) Le pêcher GF 305 indicateur polyvalent des virus des espèces à noyaux. Ann Phytopathol 1:603–617

    Google Scholar 

  • Caranta C, Palloix A, Lefebvre V, Daubèze AM (1997) QTLs for a component of partial resistance to cucumber mosaic virus in pepper: restriction of virus installation in host cells. Theor Appl Genet 94:431–438

    Article  Google Scholar 

  • Caranta C, Pflieger S, Lefebvre V, Daubèze AM, Thabuis A, Palloix A (2002) QTLs involved in the restriction of cucumber mosaic virus (CMV) long-distance movement in pepper. Theor Appl Genet 104:586–591

    Article  Google Scholar 

  • Dalmay T, Hamilton A, Rudd S, Angell S, Baulcombe DC (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553

    Article  Google Scholar 

  • Dalmay T, Horsefield R, Braunstein T, Baulcombe DC (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20:2069–2078

    Article  Google Scholar 

  • Dicenta F, Martinez-Gomez P, Burgos L, Egea J (2000) Inheritance of resistance to plum pox potyvirus (PPV) in apricot, Prunus armeniaca. Plant Breeding 119:161–164

    Article  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Calderé F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci U S A 101:9891–9896

    Article  Google Scholar 

  • Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32:927–934

    Article  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    Article  CAS  PubMed  Google Scholar 

  • Fagard M, Boutet S, Morel JB, Bellini C, Vaucheret H (2000) AGO1, QDE-2 and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc Natl Acad Sci U S A 97:11650–11654

    Article  Google Scholar 

  • Foulongne M, Pascal T, Arus P, Kervella J (2003) The potential of Prunus davidiana for introgression into peach (Prunus persica L. Batsch) assessed by comparative mapping. Theor Appl Genet 107:227–238

    Article  Google Scholar 

  • Gao Z, Eyers S, Thomas C, Ellis N, Maule A (2004) Identification of markers tightly linked to sbm recessive genes for resistance to Pea seed-borne mosaic virus. Theor Appl Genet. online first

  • Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887

    CAS  PubMed  Google Scholar 

  • Guillet I, Audergon J-M (2001) Inheritance of the Stark Early Orange apricot cultivar resistance to plum pox virus. Acta Hort 550:111–115

    Google Scholar 

  • Hurtado MA, Romero C, Vilanova S, Abbott AG, Llacer G, Badenes ML (2002) Genetic linkage maps of two apricot cultivars (Prunus armeniaca L) and mapping of PPV (sharka) resistance. Theor Appl Genet 105:182–191

    Article  CAS  PubMed  Google Scholar 

  • Jahn M, Paran I, Hoffmann K, Radwanski ER, Livingstone KD, Grube RC, Aftergoot E, Lapidot M, Moyer J (2000) Genetic mapping of the Tsw locus for resistance to the Tospovirus Tomato spotted wilt virus in Capsicum spp and its relationship to the Sw-5 gene for resistance to the same pathogen in tomato. Mol Plant-Microbe Int 13:673–682

    Google Scholar 

  • Kervella J, Pascal T, Pfeiffer F, Dirlewanger E (1998) Breeding for multiresistance in peach tree. Acta Hort 465:177–184

    Google Scholar 

  • Lambert P, Hagen LS, Arus P, Audergon JM (2004) Genetic linkage maps of two apricot cultivars (Prunus armeniaca L) compared with the almond Texas × peach Earlygold reference map for Prunus. Theor Appl Genet 108:1120–1130

    Article  CAS  PubMed  Google Scholar 

  • Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429

    CAS  PubMed  Google Scholar 

  • Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso) 4E during potyvirus infection. Curr Biol 12:1046–1051

    Article  Google Scholar 

  • Lincoln SE, Daly MJ, Lander ES (1992) Constructing genetic maps with Mapmaker/exp 3.0. Whitehead Institute Technical Report. Cambridge

    Google Scholar 

  • Matzke M, Matzke A, Pruss G, Vance V (2001) RNA-based silencing strategies in plants. Curr Opin Genet Dev 11:221–227

    Article  Google Scholar 

  • Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–639

    Article  Google Scholar 

  • Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542

    Article  Google Scholar 

  • Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, Le Gall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol 132:1272–1282

    Article  CAS  PubMed  Google Scholar 

  • Parrella G, Ruffel S, Moretti A, Morel C, Palloix A, Caranta C (2002) Recessive resistance genes against potyviruses are localized in colinear genomic regions of the tomato (Lycopersicon spp.) and pepper (Capsicum spp) genomes. Theor Appl Genet 105:855–861

    Article  Google Scholar 

  • Pascal T, Kervella J, Pfeiffer F, Sauge MH, Esmenjaud D (1998) Evaluation of the interspecific progeny Prunus.persica cv. Summergrand × Prunus.davidiana for disease resistance and some agronomic features. Acta Hort 465:185–192

    Google Scholar 

  • Pernet A, Hoisington D, Ditinger J, Jewell D, Jiang GC, Khairallah M, Letourmy P, Marchand JL, Glaszmann JC, Gonzales de Leon D (1999) Genetic mapping of maize streak virus resistance from the Mascarene source. II. Resistance in line CIRAD390 and stability across germplasm. Theor Appl Genet 99:525–539

    Google Scholar 

  • Pflieger S, Lefebvre V, Caranta C, Blattes A, Goffinet B, Palloix A (1999) Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. Genome 42:1100–1110

    Article  CAS  PubMed  Google Scholar 

  • Quilot B, Wu BH, Kervella J, Génard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet (in press)

  • Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A, Lakatos L, Banfalvi Z, Burgyan J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640

    Article  Google Scholar 

  • Vilanova S, Romero C, Abbott AG, Llacer G, Badenes ML (2003) An apricot (Prunus armeniaca L.) F2 progeny linkage map based on SSR and AFLP markers, mapping plum pox virus resistance and self-incompatibility. Theor Appl Genet 107:239–247

    Article  CAS  PubMed  Google Scholar 

  • Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

    Article  Google Scholar 

  • Xie Z, Fan B, Chen C, Chen Z (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci U S A 98:6516–6521

    Article  Google Scholar 

  • Yu D, Fan B, MacFarlane SA, Chen Z (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant-Microbe Int 16:206–216

    Google Scholar 

Download references

Acknowledgements

This research was supported by a grant from the Inter-Regional Fund (InterReg III), between Aquitaine and Euskadi (B 03786, 2001–2003). The authors are very grateful to C. Caranta (INRA, U.G.A.F.L, Avignon) for giving them the opportunity to refer to unpublished data on pepper resistance to potyviruses. We also thank Dr L. Hagen and Dr P. Butcher (King’s Park and Botanic Garden, Perth, WA, Australia) for correcting the manuscript. The present work has been carried out in compliance with French laws governing genetic experimentation

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Decroocq.

Additional information

Communicated by M.-A. Grandbastien

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Decroocq, V., Foulongne, M., Lambert, P. et al. Analogues of virus resistance genes map to QTLs for resistance to sharka disease in Prunus davidiana. Mol Genet Genomics 272, 680–689 (2005). https://doi.org/10.1007/s00438-004-1099-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-004-1099-0

Keywords

Navigation