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.
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
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
Basten CJ, Weir BS, Zeng ZB (2002) QTL cartographer: a reference manual and tutorial for QTL mapping. North Carolina State University, Raleigh
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
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
Bernhard R, Marénaud C, Sutic D (1969) Le pêcher GF 305 indicateur polyvalent des virus des espèces à noyaux. Ann Phytopathol 1:603–617
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
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
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
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
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
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
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
Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284
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
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
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
Guillet I, Audergon J-M (2001) Inheritance of the Stark Early Orange apricot cultivar resistance to plum pox virus. Acta Hort 550:111–115
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
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
Kervella J, Pascal T, Pfeiffer F, Dirlewanger E (1998) Breeding for multiresistance in peach tree. Acta Hort 465:177–184
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
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
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
Lincoln SE, Daly MJ, Lander ES (1992) Constructing genetic maps with Mapmaker/exp 3.0. Whitehead Institute Technical Report. Cambridge
Matzke M, Matzke A, Pruss G, Vance V (2001) RNA-based silencing strategies in plants. Curr Opin Genet Dev 11:221–227
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Corresponding author
Additional information
Communicated by M.-A. Grandbastien
Electronic Supplementary Material
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-004-1099-0